THE WORKS
OF
FRANCIS MAITLAND BALFOUR.
VOL. III.
Memorial Edition.
Cambridge:
PRINTED BY C. J. CLAY, M.A. AND SON,
AT THE UNIVERSITY PRESS.
Memorial Edition.
THE WORKS
OF
FRANCIS MAITLAND BALFOUR,
M.A., LL.D., F.R.S.,
FELLOW OF TRINITY COLLEGE,
AND PROFESSOR OF ANIMAL MORPHOLOGY IN THE UNIVERSITY OF
CAMBRIDGE.
EDITED BY
M. FOSTER, F.R.S.,
PROFESSOR OF PHYSIOLOGY IN THE UNIVERSITY OF CAMBRIDGE;
AND
ADAM SEDGWICK, M.A.,
FELLOW AND LECTURER OF TRINITY COLLEGE, CAMBRIDGE.
VOL. III.
A TREATISE ON COMPARATIVE EMBRYOLOGY.
Vol. II. Vertebrata.
London:
MACMILLAN AND CO.
1885
[_The Right of Translation is reserved._]
PREFACE TO VOLUME II.
The present volume completes my treatise on Comparative Embryology.
The first eleven chapters deal with the developmental history of the
Chordata. These are followed by three comparative chapters completing
the section of the work devoted to Systematic Embryology. The
remainder of the treatise, from Chapter XIV. onwards, is devoted to
Organogeny. For the reasons stated in the introduction to this part
the organogeny of the Chordata has been treated with much greater
fulness than that of the other groups of Metazoa.
My own investigations have covered the ground of the present volume
much more completely than they did that of the first volume; a not
inconsiderable proportion of the facts recorded having been directly
verified by me.
The very great labour of completing this volume has been much
lightened by the assistance I have received from my friends and
pupils. Had it not been for their co-operation a large number of the
disputed points, which I have been able to investigate during the
preparation of the work, must have been left untouched.
My special thanks are due to Mr Sedgwick, who has not only devoted a
very large amount of time and labour to correcting the proofs, but has
made for me an index of this volume, and has assisted me in many other
ways.
Dr Allen Thomson and Professor Kleinenberg of Messina have undertaken
the ungrateful task of looking through my proof-sheets, and have made
suggestions which have proved most valuable. To Professors Parker,
Turner, and Bridge, I am also greatly indebted for their suggestions
with reference to special chapters of the work.
CONTENTS OF VOLUME II.
CHAPTER I. CEPHALOCHORDA. Pp. 1-8.
Segmentation and formation of the layers, pp. 1-3. Central nervous
system, pp. 3, 4. Mesoblast, p. 5. General history of larva, pp. 6-8.
CHAPTER II. UROCHORDA. Pp. 9-39.
_Solitaria_, pp. 9-23. Development of embryo, pp. 9-15. Growth and
structure of free larva, pp. 15-19. Retrogressive metamorphosis, pp.
19-23. _Sedentaria_, p. 23. _Natantia_, pp. 23-28. _Doliolidæ_, pp.
28, 29. _Salpidæ_, pp. 29-34. _Appendicularia_, p. 34. Metagenesis,
pp. 34-38.
CHAPTER III. ELASMOBRANCHII. Pp. 40-67.
Segmentation and formation of the layers, pp. 40-47. Epiblast, p. 47.
Mesoblast, pp. 47-51. Hypoblast and notochord, pp. 51-54. General
features of the embryo at successive stages, pp. 55-62. The yolk-sack,
pp. 62-66.
CHAPTER IV. TELEOSTEI. Pp. 68-82.
Segmentation and formation of the layers, pp. 68-73. General history
of the layers, pp. 73-75. General development of the embryo, pp.
76-81.
CHAPTER V. CYCLOSTOMATA. Pp. 83-101.
Segmentation and formation of the layers, pp. 83-86. Mesoblast and
notochord, pp. 86, 87. General history of the development, pp. 87-97.
Metamorphosis, pp. 97-100. Myxine, p. 100.
CHAPTER VI. GANOIDEI. Pp. 102-119.
_Acipenser_, pp. 102-110. Segmentation and formation of the layers,
pp. 102-104. General development of the embryo and larva, pp. 104-110.
_Lepidosteus_, pp. 111-119. Segmentation, pp. 111, 112. General
development of embryo and larva, pp. 112-119. General observations on
the embryology of Ganoids, p. 119.
CHAPTER VII. AMPHIBIA. Pp. 120-144.
Oviposition and impregnation, pp. 120, 121. Formation of the layers,
pp. 121-124. Epiblast, pp. 125-127. Mesoblast and notochord, pp. 128,
129. Hypoblast, pp. 129-131. _General growth of the embryo_, pp.
131-143. Anura, pp. 131-141. Urodela, pp. 141-143. Gymnophiona, p.
143.
CHAPTER VIII. AVES. Pp. 145-201.
Segmentation and formation of the layers, pp. 145-166. General history
of the germinal layers, pp. 166-169. General development of the
embryo, pp. 169-180. _Foetal membranes_, pp. 185-199. Amnion, pp.
185-191. Allantois, pp. 191-193. Yolk-sack, pp. 193-199.
CHAPTER IX. REPTILIA. Pp. 202-213.
_Lacertilia_, pp. 202-209. Segmentation and formation of the layers,
pp. 202-207. General development of the embryo, p. 208. Embryonic
membranes and yolk-sack, pp. 208-210. _Ophidia_, p. 210. _Chelonia_,
pp. 210-212.
CHAPTER X. MAMMALIA. Pp. 214-274.
Segmentation and formation of the layers, pp. 214-227. General growth
of the embryo, pp. 227-232. Embryonic membranes and yolk-sack, pp.
232-239. Comparative history of the Mammalian foetal membranes, pp.
239-257. Comparative histology of the placenta, pp. 257-259. Evolution
of the placenta, pp. 259-261. Development of the Guinea-pig, pp.
262-265. The human embryo, pp. 265-270.
CHAPTER XI. COMPARISON OF THE FORMATION OF THE GERMINAL LAYERS AND OF
THE EARLY STAGES IN THE DEVELOPMENT OF VERTEBRATES. Pp. 275-310.
Formation of the gastrula, pp. 275-292. The formation of the mesoblast
and of the notochord, pp. 292-300. _The epiblast_, pp. 300-304.
Formation of the central nervous system, pp. 301-304. Formation of the
organs of special sense, p. 304. Summary of organs derived from the
three germinal layers, pp. 304-306. Growth in length of the Vertebrate
embryo, pp. 306-309. The evolution of the allantois and amnion, pp.
309, 310.
CHAPTER XII. OBSERVATIONS ON THE ANCESTRAL FORM OF THE CHORDATA. Pp.
311-330.
General considerations, pp. 311-316. The medullary canal, pp. 316,
317. The origin and nature of the mouth, pp. 317-321. The cranial
flexure, pp. 321, 322. The postanal gut and neurenteric canal, pp.
322-325. The body-cavity and mesoblastic somites, p. 325. The
notochord, pp. 325, 326. Gill clefts, pp. 326, 327. Phylogeny of the
Chordata, pp. 327-329.
CHAPTER XIII. GENERAL CONCLUSIONS. Pp. 331-388.
I. Mode of origin and homologies of the germinal layers, pp. 331-360.
Formation of the primary germinal layers, pp. 332, 333. Invagination,
pp. 333-335. Delamination, pp. 335-338. Phylogenetic significance of
delamination and invagination, pp. 338-345. Homologies of the germinal
layers, pp. 345, 346. The origin of the mesoblast, pp. 346-360.
II. Larval forms: their nature, origin, and affinities. Preliminary
considerations, pp. 360-362. Types of larvæ, pp. 363-384. Phylogenetic
conclusions, pp. 384, 385. General conclusions and summary, pp. 385,
386.
PART II. ORGANOGENY;
INTRODUCTION. Pp. 391, 392.
CHAPTER XIV. THE EPIDERMIS AND ITS DERIVATIVES. Pp. 393-399.
Protective epidermic structures, pp. 393-397. Dermal skeletal
structures, p. 397. Glands, pp. 397, 398.
CHAPTER XV. THE NERVOUS SYSTEM. Pp. 400-469.
The origin of the nervous system, pp. 400-405. Nervous system of the
Invertebrata, pp. 405-414. _Central nervous system of the Vertebrata_,
pp. 415-447. Spinal chord, pp. 415-419. General development of the
brain, pp. 419-423. Hind-brain, pp. 424-427. Mid-brain, pp. 427, 428.
General development of fore-brain, pp. 428-430. Thalamencephalon, pp.
430-435. Pituitary body, pp. 435-437. Cerebral Hemispheres, pp.
437-444. Olfactory lobes, pp. 444, 445. General conclusions as to the
central nervous system of the Vertebrata, pp. 445-447. _Development of
the cranial and spinal nerves_, pp. 448-466. Spinal nerves, pp.
448-455. Cranial nerves, pp. 455-466. _Sympathetic nervous system_,
pp. 466-468.
CHAPTER XVI. ORGANS OF VISION. Pp. 470-511.
Coelenterata, pp. 471, 472. Mollusca, pp. 472-479. Chætopoda, p. 479.
Chætognatha, p. 479. Arthropoda, pp. 479-483. Vertebrata general, pp.
483-490. Retina, pp. 490-492. Optic nerve, pp. 492, 493. Choroid
fissure, p. 493. Lens, pp. 494, 495. Vitreous humour, pp. 494, 495.
Cornea, pp. 495-497. Aqueous humour, p. 497. _Comparative development
of Vertebrate eye_, pp. 497-506. Ammocoete eye, pp. 498, 499. Optic
vesicles, p. 499. Lens, p. 499. Cornea, p. 500. Optic nerve and
choroid fissure, pp. 500-505. Iris and ciliary processes, p. 506.
Accessory organs connected with the eye, p. 506. Eyelids, p. 506.
Lacrymal glands, p. 506. Lacrymal duct, pp. 506, 507. _Eye of the
Tunicata_, pp. 507-509. Accessory eyes in the Vertebrata, pp. 509,
510.
CHAPTER XVII. AUDITORY ORGAN, OLFACTORY ORGAN, AND SENSE ORGANS OF THE
LATERAL LINE. Pp. 512-541.
Auditory organs, pp. 512-531. General structure of auditory organs,
pp. 512, 513. Auditory organs of the Coelenterata, pp. 513-515.
Auditory organs of the Mollusca, pp. 515, 516. Auditory organs of the
Crustacea, p. 516. _Auditory organs of the Vertebrata_, pp. 516-530.
Auditory vesicle, pp. 517-524. Organ of Corti, pp. 524-527. Accessory
structures connected with the organ of hearing of terrestrial
vertebrata, pp. 527-530. Auditory organ of the Tunicata, pp. 530, 531.
Bibliography of Auditory organs, p. 531.
Olfactory organs, pp. 531-538. Bibliography of Olfactory organs, p.
538. Sense organs of the lateral line, pp. 538-540. Bibliography of
sense organs of lateral line, pp. 540, 541.
CHAPTER XVIII. THE NOTOCHORD, THE VERTEBRAL COLUMN, THE RIBS, AND THE
STERNUM. Pp. 542-563.
Introductory remarks on the origin of the skeleton, pp. 542-544.
Bibliography of the origin of the skeleton, pp. 544, 545. The
notochord and its cartilaginous sheath, pp. 545-549. _The vertebral
arches and the vertebral bodies_, pp. 549-559. Cyclostomata, p. 549.
Elasmobranchii, pp. 549-553. Ganoidei, p. 553. Teleostei, p. 553.
Amphibia, pp. 553-556. Reptilia, pp. 556, 557. Aves, pp. 557, 558.
Mammalia, pp. 558, 559. Bibliography of the notochord and vertebral
column, p. 560. _Ribs_, pp. 560-562. _Sternum_, pp. 562, 563.
Bibliography of the ribs and sternum, p. 563.
CHAPTER XIX. THE SKULL. Pp. 564-598.
Preliminary remarks, pp. 564, 565. The cartilaginous cranium, pp.
565-571. The parachordals and notochord, pp. 566, 567. The trabeculæ,
pp. 567-570. The sense capsules, pp. 570, 571. The branchial skeleton,
pp. 572-591. General structure of, pp. 572-575. _Mandibular and hyoid
arches_, pp. 575-591. Elasmobranchii, pp. 576-579. Teleostei, pp.
579-581. Amphibia, pp. 581-588. Sauropsida, pp. 588, 589. Mammalia,
pp. 589-591. Membrane bones and ossifications of the cranium, pp.
592-597. Membrane bones, pp. 592-595. Ossifications of the
cartilaginous cranium, pp. 595-597. Labial cartilages, p. 597.
Bibliography of the skull, p. 598.
CHAPTER XX. PECTORAL AND PELVIC GIRDLES AND THE SKELETON OF THE LIMBS.
Pp. 599-622.
The Pectoral girdle, pp. 599-606. Pisces, pp. 599-601. _Amphibia and
Amniota_, pp. 601, 602. Lacertilia, p. 603. Chelonia, p. 603. Aves,
pp. 603, 604. Mammalia, p. 604. Amphibia, p. 605. Bibliography of
Pectoral girdle, pp. 605, 606.
The Pelvic girdle, pp. 606-608. Pisces, pp. 606, 607. _Amphibia and
Amniota_, pp. 606, 607. Amphibia, p. 607. Lacertilia, p. 607.
Mammalia, p. 608. Bibliography of Pelvic girdle, p. 608. _Comparison
of pectoral and pelvic girdles_, pp. 608, 609.
Limbs, pp. 609-622. The piscine fin, pp. 609-618. The cheiropterygium,
pp. 618-622. Bibliography of limbs, p. 622.
CHAPTER XXI. THE BODY CAVITY, THE VASCULAR SYSTEM AND THE VASCULAR
GLANDS. Pp. 623-666.
The body cavity, pp. 623-632. General, pp. 623, 624. _Chordata_, pp.
624-632. Abdominal pores, pp. 626, 627. Pericardial cavities, pleural
cavities and diaphragm, pp. 627-632. Bibliography of body cavity, p.
632.
The vascular system, pp. 632-663. General, pp. 632, 633. The heart,
pp. 633-643. Bibliography of the heart, p. 643. Arterial system, pp.
643-651. Bibliography of the arterial system, p. 651. Venous system,
pp. 651-663. Bibliography of the venous system, p. 663. Lymphatic
system and spleen, p. 664. Bibliography of spleen, p. 664. Suprarenal
bodies, pp. 664-666. Bibliography of suprarenal bodies, p. 666.
CHAPTER XXII. THE MUSCULAR SYSTEM. Pp. 667-679.
Evolution of muscle-cells, pp. 667, 668. _Voluntary muscular system of
the Chordata_, pp. 668-679. Muscular fibres, pp. 668, 669. Muscular
system of the trunk and limbs, pp. 673-676. The somites and muscular
system of the head, pp. 676-679. Bibliography of muscular system, p.
679.
CHAPTER XXIII. EXCRETORY ORGANS. Pp. 680-740.
Platyelminthes, pp. 680, 681. Mollusca, pp. 681, 682. Polyzoa, pp.
682, 683. Branchiopoda, p. 683. Chætopoda, pp. 683-686. Gephyrea, pp.
686, 687. Discophora, pp. 687, 688. Arthropoda, pp. 688, 689.
Nematoda, p. 689. Excretory organs and generative ducts of the
Craniata, pp. 689-737. General, pp. 689, 690. Elasmobranchii, pp.
690-699. Cyclostomata, pp. 700, 701. Teleostei, pp. 701-704. Ganoidei,
pp. 704-707. Dipnoi, p. 707. Amphibia, pp. 707-713. Amniota, pp.
713-727. General conclusions and summary, pp. 728-737. Pronephros, pp.
728, 729. Mesonephros, pp. 729-732. Genital ducts, pp. 732-736.
Metanephros, pp. 736, 737. _Comparison of the excretory organs of the
Chordata and Invertebrata_, pp. 737, 738. Bibliography of Excretory
organs, pp. 738-740.
CHAPTER XXIV. GENERATIVE ORGANS AND GENITAL DUCTS. Pp. 741-753.
Generative organs, pp. 741-748. Porifera, p. 741. Coelenterata, pp.
741-743. Chætopoda and Gephyrea, p. 743. Chætognatha, pp. 743-745.
Polyzoa, p. 745 Nematoda, p. 745. Insecta, p. 745. Crustacea, pp. 745,
746. Chordata, pp. 746-748. Bibliography of generative organs, p. 748.
Genital ducts, pp. 748-753.
CHAPTER XXV. THE ALIMENTARY CANAL AND ITS APPENDAGES IN THE CHORDATA.
Pp. 754-780.
Mesenteron, pp. 754-774. Subnotochordal rod, pp. 754-756. Splanchnic
mesoblast and mesentery, pp. 756-758. _Respiratory division of the
Mesenteron_, pp. 758-766. Thyroid body, pp. 759-762. Thymus gland, pp.
762, 763. Swimming bladder and lungs, pp. 763-766, _The middle
division of the Mesenteron_, pp. 766-771. Cloaca, pp. 766, 767.
Intestine, pp. 767, 768. Liver, pp. 769, 770. Pancreas, pp. 770, 771.
_Postanal section of the Mesenteron_, pp. 771-774.
The stomodæum, pp. 774-778. Comparative development of oral cavity,
pp. 774-776. Teeth, pp. 776-778.
The proctodæum, pp. 778-780. Bibliography of alimentary canal, p. 780.
EMBRYOLOGY.
CHAPTER I.
CEPHALOCHORDA.
The developmental history of the Chordata has been studied far more
completely than that of any of the groups so far considered; and the
results which have been arrived at are of striking interest and
importance. Three main subdivisions of this group can be recognized:
(1) the Cephalochorda containing the single genus Amphioxus; (2) the
Urochorda or Tunicata; and (3) the Vertebrata[1]. The members of the
second and probably of the first of these groups have undergone
degeneration, but at the same time the members of the first group
especially undergo a less modified development than that of other
Chordata.
[1] The term Vertebrata is often used to include the
Cephalochorda. It is in many ways convenient to restrict its use
to the forms which have at any rate some indications of vertebræ;
a restriction which has the further convenience of restoring to
the term its original limitations. In the first volume of this
work the term Craniata was used for the forms which I now propose
to call Vertebrata.
CEPHALOCHORDA.
Our knowledge of the development of Amphioxus is mainly due to
Kowalevsky (Nos. 1 and 2). The ripe eggs appear to be dehisced into
the branchial or atrial cavity, and to be transported thence through
the branchial clefts into the pharynx, and so through the mouth to the
exterior. (Kowalevsky, No. 1, and Marshall, No. 5.)
[FIG. 1. THE SEGMENTATION OF AMPHIOXUS. (Copied from Kowalevsky.)
B. Stage with four equal segments.
C. Stage after the four segments have become divided by an
equatorial furrow into eight equal segments.
D. Stage in which a single layer of cells encloses a central
segmentation cavity.
E. Somewhat older stage in optical section.
_sg._ segmentation cavity.]
When laid the egg is about 0.105 mm. in diameter. It is invested by a
delicate membrane, and is somewhat opaque owing to the presence of
yolk granules, which are however uniformly distributed through it, and
proportionately less numerous than in the ova of most Chordata.
Impregnation is external and the segmentation is nearly regular (fig.
1). A small segmentation cavity is visible at the stage with four
segments, and increases during the remainder of the segmentation; till
at the close (fig. 1 E) the embryo consists of a blastosphere formed
of a single layer of cells enclosing a large segmentation cavity. One
side of the blastosphere next becomes invaginated, and during the
process the embryo becomes ciliated, and commences to rotate. The
cells forming the invaginated layer become gradually more columnar
than the remaining cells, and constitute the hypoblast; and a
structural distinction between the epiblast and hypoblast is thus
established. In the course of the invagination the segmentation cavity
becomes gradually obliterated, and the embryo first assumes a
cup-shaped form with a wide blastopore, but soon becomes elongated,
while the communication of the archenteron, or cavity of invagination,
with the exterior is reduced to a small blastopore (fig. 2 A), placed
at the pole of the long axis which the subsequent development shews to
be _the hinder end of the embryo_. The blastopore is often known in
other Chordata as the anus of Rusconi. Before the invagination is
completed the larva throws off the egg-membrane, and commences to lead
a free existence.
[FIG. 2. EMBRYOS OF AMPHIOXUS. (After Kowalevsky.)
The parts in black with white lines are epiblastic; the shaded parts
are hypoblastic.
A. Gastrula stage in optical section.
B. Slightly later stage after the neural plate _np_ has become
differentiated, seen as a transparent object from the dorsal side.
C. Lateral view of a slightly older larva in optical section.
D. Dorsal view of an older larva with the neural canal completely
closed except for a small pore (_no_) in front.
E. Older larva seen as a transparent object from the side.
_bl._ blastopore (which becomes in D the neurenteric canal); _ne._
neurenteric canal; _np._ neural or medullary plate; _no._ anterior
opening of neural canal; _ch._ notochord; _so^I_, _so^{II}._ first
and second mesoblastic somites.]
Up to this stage the larva, although it has acquired a cylindrical
elongated form, has only the structure of a simple two-layered
gastrula; but the changes which next take place give rise on the one
hand to the formation of the central nervous system, and on the other
to the formation of the notochord and mesoblastic somites[2]. The
former structure is developed from the epiblast and the two latter
from the hypoblast.
[2] The protovertebræ of most embryologists will be spoken of as
mesoblastic somites.
The formation of the central nervous system commences with the
flattening of the dorsal surface of the embryo. The flattened area
forms a plate (fig. 2 B and fig. 3 A, _np_), extending backwards to
the blastopore, which has in the meantime passed round to the dorsal
surface. The sides of the plate become raised as two folds, which are
most prominent posteriorly, and meet behind the blastopore, but shade
off in front. The two folds next unite dorsally, so as to convert the
previous groove into a canal[3]--the neural or medullary canal. They
unite first of all over the blastopore, and their line of junction
extends from this point forwards (fig. 2 C, D, E). There is in this
way formed a tube on the floor of which the blastopore opens behind,
and which is itself open in front. Finally the medullary canal is
formed for the whole length of the embryo. The anterior opening
persists however for some time. The communication between the neural
and alimentary tracts becomes interrupted when the caudal fin appears
and the anus is formed. The neural canal then extends round the end of
the notochord to the ventral side, but subsequently retreats to the
dorsal side and terminates in a slight dilatation.
[3] The details of this process are spoken of below.
In the formation of the medullary canal there are two points deserving
notice--viz. (1) the connection with the blastopore; (2) the relation
of the walls of the canal to the adjoining epiblast. With reference to
the first of these points it is clear that the fact of the blastopore
opening on the floor of the neural canal causes a free communication
to exist between the archenteron or gastrula cavity and the neural
canal; and that, so long as the anterior pore of the neural canal
remains open, the archenteron communicates indirectly with the
exterior (_vide_ fig. 2 E). It must not however be supposed (as has
been done by some embryologists) that the pore at the front end of the
neural canal represents the blastopore carried forwards. It is even
probable that what Kowalevsky describes as the carrying of the
blastopore to the dorsal side is really the commencement of the
formation of the neural canal, the walls of which are continuous with
the lips of the blastopore. This interpretation receives support from
the fact that at a later stage, when the neural and alimentary canals
become separated, the neural canal extends round the posterior end of
the notochord to the ventral side. The embryonic communication between
the neural and alimentary canals is common to most Chordata; and the
tube connecting them will be called the neurenteric canal. It is
always formed in fundamentally the same manner as in Amphioxus. With
reference to the second point it is to be noted that Amphioxus is
exceptional amongst the Chordata in the fact that, before the closure
of the neural groove, the layer of cells which will form the neural
tube becomes completely separated from the adjoining epiblast (fig. 3
A), and forms a structure which may be spoken of as the medullary
plate; and that in the closure of the neural canal the lateral
epiblast forms a complete layer above this plate before the plate
itself is folded over into a closed canal. This peculiarity will be
easily understood from an examination of fig. 3 A, B and C.
[FIG. 3. SECTIONS OF AN AMPHIOXUS EMBRYO AT THREE STAGES.
(After Kowalevsky.)
A. Section at gastrula stage.
B. Section of an embryo slightly younger than that represented in
fig. 2 D.
C. Section through the anterior part of an embryo at the stage
represented in fig. 2 E.
_np._ neural plate; _nc._ neural canal; _mes._ archenteron in A and
B, and mesenteron in C; _ch._ notochord; _so._ mesoblastic somite.]
The formation of the mesoblastic somites commences, at about the same
time as that of the neural canal, as a pair of hollow outgrowths of
the walls of the archenteron. These outgrowths, which are shewn in
surface view in fig. 2 B and D, _so_, and in section in fig. 3 B and
C, _so_, arise near the front end of the body and gradually extend
backwards as wing-like diverticula of the archenteric cavity. As they
grow backwards their dorsal part becomes divided by transverse
constrictions into cubical bodies (fig. 2 D and E), which, with the
exception of the foremost, soon cease to open into what may now be
called the mesenteron, and form the mesoblastic somites. Each
mesoblastic somite, after its separation from the mesenteron, is
constituted of two layers, an inner one--the splanchnic--and an
outer--the somatic, and a cavity between the two which was originally
continuous with the cavity of the mesenteron. Eventually the dorsal
parts of the outgrowths become separated from the ventral, and form
the muscle-plates, while their cavities atrophy. The cavity of the
ventral part, which is not divided into separate sections by the above
described constrictions, remains as the true body cavity. The ventral
part of the inner layer of the mesoblastic outgrowths gives rise to
the muscular and connective tissue layers of the alimentary tract, and
the dorsal part to a section of the voluntary muscular system. The
ventral part of the outer layer gives rise to the somatic mesoblast,
and the dorsal to a section of the voluntary muscular system. The
anterior mesoblastic somite long retains its communication with the
mesenteron, and was described by Max Schultze, and also at first by
Kowalevsky, as a glandular organ. While the mesoblastic somites are
becoming formed the dorsal wall of the mesenteron develops a median
longitudinal fold (fig. 3 B, _ch_), which is gradually separated off
from before backwards as a rod (fig. 3 C, _ch_), underlying the
central nervous system. This rod is the notochord. After the
separation of those parts the remainder of the hypoblast forms the
wall of the mesenteron.
With the formation of the central nervous system, the mesoblastic
somites, the notochord, and the alimentary tract the main systems of
organs are established, and it merely remains briefly to describe the
general changes of form which accompany the growth of the larva into
the adult. By the time the larva is but twenty-four hours old there
are formed about seventeen mesoblastic somites. The body, during the
period in which these are being formed, remains cylindrical, but
shortly afterwards it becomes pointed at both ends, and the caudal fin
appears. The fine cilia covering the larva also become replaced by
long cilia, one to each cell. The mesenteron is still completely
closed, but on the right side of the body, at the level of the front
end of the mesenteron, the hypoblast and epiblast now grow together,
and a perforation becomes formed through their point of contact, which
becomes the mouth. The anus is probably formed about the same time if
not somewhat earlier[4].
[4] The lateral position of the mouth in the embryo Amphioxus has been
regarded as proving that the mouth represents a branchial cleft,
but the general asymmetry of the organs is such that no great
stress can, I think, be laid on the position of the mouth.
[FIG. 4. SECTIONS THROUGH TWO ADVANCED EMBRYOS OF
AMPHIOXUS TO SHEW THE FORMATION OF THE PERIBRANCHIAL CAVITY. (After
Kowalevsky.)
In A are seen two folds of the body wall with a prolongation of the
body cavity. In B the two folds have coalesced ventrally, forming a
cavity into which a branchial cleft is seen to open.
_mes._ mesenteron; _br.c._ branchial cavity; _pp._ body cavity.]
Of the subsequent changes the two most important are (1) the formation
of the gill slits or clefts; (2) the formation of the peribranchial or
atrial cavity.
The formation of the gill slits is, according to Kowalevsky's
description, so peculiar that one is almost tempted to suppose that
his observations were made on pathological specimens. The following is
his account of the process. Shortly after the formation of the mouth
there appears on the ventral line a coalescence between the epiblast
and hypoblast. Here an opening is formed, and a visceral cleft is thus
established, which passes to the left side, viz. the side opposite the
mouth. A second and apparently a third slit are formed in the same
way. The stages immediately following were not observed, but in the
next stage twelve slits were present, no longer however on the left
side, but in the median ventral line. There now appears on the side
opposite the mouth, and the same therefore as that originally occupied
by the first three clefts, a series of fresh clefts, which in their
growth push the original clefts over to the same side as the mouth.
Each of the fresh clefts becomes divided into two, which form the
permanent clefts of their side.
The gill slits at first open freely to the exterior, but during their
formation two lateral folds of the body wall, containing a
prolongation of the body cavity, make their appearance (fig. 4 A), and
grow downwards over the gill clefts, and finally meet and coalesce
along the ventral line, leaving a widish cavity between themselves and
the body wall. Into this cavity, which is lined by epiblast, the gill
clefts open (fig. 4 B, _br.c_). This cavity--which forms a true
peribranchial cavity--is completely closed in front, but owing to the
folds not uniting completely behind it remains in communication with
the exterior by an opening known as the atrial or abdominal pore.
The vascular system of Amphioxus appears at about the same time as the
first visceral clefts.
BIBLIOGRAPHY.
(1) A. Kowalevsky. "Entwicklungsgeschichte des Amphioxus lanceolatus."
_Mém. Acad. Impér. des Sciences de St Pétersbourg_, Series VII. Tom.
xi. 1867.
(2) A. Kowalevsky. "Weitere Studien über die Entwicklungsgeschichte
des Amphioxus lanceolatus." _Archiv f. mikr. Anat._, Vol. XIII. 1877.
(3) Leuckart u. Pagenstecher. "Untersuchungen über niedere Seethiere."
_Müller's Archiv_, 1858.
(4) Max Schultze. "Beobachtung junger Exemplare von Amphioxus." _Zeit.
f. wiss. Zool._, Bd. III. 1851.
(5) A. M. Marshall. "On the mode of Oviposition of Amphioxus." _Jour.
of Anat. and Phys._, Vol. X. 1876.
CHAPTER II.
UROCHORDA[5].
[5] The following classification of the Urochorda is adopted in
the present chapter.
I. Caducichordata.
{Solitaria _ex. Ascidia_.
A. SIMPLICIA {Socialia _ex. Clavellina_.
{Sedentaria _ex. Botryllus_.
B. COMPOSITA {Natantia _ex. Pyrosoma_.
{Salpidæ.
C. CONSERTA {Doliolidæ.
II. Perennichordata.
_Ex. Appendicularia_.
In the Solitaria, except Cynthia, the eggs are generally laid, and
impregnation is effected sometimes before and sometimes after the eggs
have left the atrial cavity. In Cynthia and most Caducichordata
development takes place within the body of the parent, and in the
Salpidæ a vascular connection is established between the parent and
the single foetus, forming a structure physiologically comparable with
the Mammalian placenta.
Solitaria. The development of the Solitary Ascidians has been more
fully studied than that of the other groups, and appears moreover to
be the least modified. It has been to a great extent elucidated by the
splendid researches of Kowalevsky (Nos. 18 and 20), whose statements
have been in the main followed in the account below. Their truth seems
to me to be established, in spite of the scepticism they have met with
in some quarters, by the closeness of their correspondence with the
developmental phenomena in Amphioxus.
The type most fully investigated by Kowalevsky is Ascidia (Phallusia)
mammillata; and the following description must be taken as more
especially applying to this type.
The segmentation is complete and regular. A small segmentation cavity
appears fairly early, and is surrounded, according to Kowalevsky, by a
single layer of cells, though on this point Kupffer (No. 27) and Giard
(No. 11) are at variance with him.
[FIG. 5. TRANSVERSE SECTION THROUGH THE FRONT END OF AN EMBRYO OF
PHALLUSIA MAMMILLATA. (After Kowalevsky.)
The embryo is slightly younger than that represented in fig. 8 III.
_mg._ medullary groove; _al._ alimentary tract.]
The segmentation is followed by an invagination of nearly the same
character as in Amphioxus. The blastosphere resulting from the
segmentation first becomes flattened on one side, and the cells on the
flatter side become more columnar (fig. 8 I.). Very shortly a
cup-shaped form is assumed, the concavity of which is lined by the
more columnar cells. The mouth of the cup or blastopore next becomes
narrowed; while at the same time the embryo becomes oval. The
blastopore is situated not quite at a pole of the oval but in a
position which subsequent development shews to _be on the dorsal side
close to the posterior end of the embryo_. The long axis of the oval
corresponds with the long axis of the embryo. At this stage the embryo
consists of two layers; a columnar hypoblast lining the central cavity
or archenteron, and a thinner epiblastic layer. The dorsal side of the
embryo next becomes flattened (fig. 8 II.), and the epiblast covering
it is shortly afterwards marked by an axial groove continued forwards
from the blastopore to near the front end of the body (fig. 5, _mg_).
This is the medullary groove, and it soon becomes converted into a
closed canal--the medullary or neural canal--below the external skin
(fig. 6, _n.c_). The closure is effected by the folds on each side of
the furrow meeting and coalescing dorsally. The original medullary
folds fall into one another behind the blastopore so that the
blastopore is situated on the floor of the groove, and, on the
conversion of the groove into a canal, the blastopore connects the
canal with the archenteric cavity, and forms a short neurenteric
canal. The closure of the medullary canal commences at the blastopore
and is thence continued forwards, the anterior end of the canal
remaining open. The above processes are represented in longitudinal
section in fig. 8 III, _n_. When the neural canal is completed for its
whole length, it still communicates by a terminal pore with the
exterior. In the relation of the medullary canal to the blastopore, as
well as in the closure of the medullary groove from behind forwards,
the Solitary Ascidians agree closely with Amphioxus.
[FIG. 6. TRANSVERSE OPTICAL SECTION OF THE TAIL OF AN EMBRYO OF
PHALLUSIA MAMMILLATA. (After Kowalevsky.)
The section is from an embryo of the same age as fig. 8 IV.
_ch._ notochord; _n.c._ neural canal; _me._ mesoblast; _al._
hypoblast of tail.]
The cells of the dorsal wall of the archenteron immediately adjoining
the front and sides of the blastopore have in the meantime assumed a
somewhat different character from the remaining cells of the
archenteron, and give rise to a body which, when viewed from the
dorsal surface, has somewhat the form of a horseshoe. This body was
first observed by Metschnikoff. On the elongation of the embryo and
the narrowing of the blastopore the cells forming this body arrange
themselves as a broad linear cord, two cells wide, underlying about
the posterior half of the neural canal (fig. 7, _ch_). They form the
rudiment of the notochord, which, as in Amphioxus, is derived from the
dorsal wall of the archenteron. They are seen in longitudinal section
in fig. 8 II. and III. _ch_.
With the formation of the notochord the body of the embryo becomes
divided into two distinct regions--a posterior region where the
notochord is present, and an anterior region into which it is not
prolonged. These two regions correspond with the tail and the trunk of
the embryo at a slightly later stage. The section of the archenteric
cavity in the trunk dilates and constitutes the permanent mesenteron
(figs. 7, _al_, and 8 III. and IV. _dd_). It soon becomes shut off
from the slit-like posterior part of the archenteron. The nervous
system in this part also dilates and forms what may be called the
cephalic swelling (fig. 8 IV.), and the pore at its anterior extremity
gradually narrows and finally disappears. In the region of the tail we
have seen that the dorsal wall of the archenteron becomes converted
into the notochord, which immediately underlies the posterior part of
the medullary canal, and soon becomes an elongated cord formed of a
single or double row of flattened cells. The lateral walls of the
archenteron (fig. 7, _me_) in the tail become converted into elongated
cells arranged longitudinally, which form powerful lateral muscles
(fig. 8 IV. _m_). After the formation of the notochord and of the
lateral muscles there remains of the archenteron in the tail only the
ventral wall, which according to Kowalevsky forms a simple cord of
cells (fig. 6, _al_). It is however not always present, or else has
escaped the attention of other observers. It is stated by Kowalevsky
to be eventually transformed into blood corpuscles. The neurenteric
canal leads at first into the narrow space between the above
structures, which is the remnant of the posterior part of the lumen of
the archenteron. Soon both the neurenteric canal and the caudal
remnant of the archenteron become obliterated.
[FIG. 7. OPTICAL SECTION OF AN EMBRYO OF PHALLUSIA MAMMILLATA.
(After Kowalevsky.)
The embryo is of the same age as fig. 8 III, but is seen in
longitudinal horizontal section.
part of body; _ch._ notochord; _me._ mesoblast.]
During the above changes the tail becomes considerably elongated and,
owing to the larva being still in the egg-shell, is bent over to the
ventral side of the trunk.
[FIG. 8. VARIOUS STAGES IN THE DEVELOPMENT OF PHALLUSIA MAMMILLATA.
(From Huxley; after Kowalevsky.)
The embryos are represented in longitudinal vertical section.
I. Commencing gastrula stage. _fh._ segmentation cavity.
II. Late gastrula stage with flattened dorsal surface. _eo._
blastopore; _ch._ notochord; _dd._ hypoblast.
III. A more advanced embryo with a partially-formed neural tube.
_ch._ and _dd._ as before; _n._ neural tube; _c._ epiblast.
IV. Older embryo in which the formation of the neural tube is
completed. _dd._ hypoblast enclosing persistent section of
alimentary tract; _dd´._ hypoblast in the tail; _m._ muscles.
V. Larva just hatched. The end of the tail is not represented. _a._
eye; _gb._ dilated extremity of neural tube with otolith projecting
into it; _Rg._ anterior swelling of the spinal division of the
neural tube; _f_. anterior pore of neural tube; _Rm._ posterior part
of neural tube; _o._ mouth; _Chs._ notochord; _kl._ atrial
invagination; _dd._ branchial region of alimentary tract; d.
commencement of oesophagus and stomach; _dd´._ hypoblast in the
tail; _m._ muscles; _hp._ papilla for attachment.
VI. Body and anterior part of the tail of a two days' larva. _klm._
atrial aperture; en. endostyle; _ks._ branchial sack; _1ks. 2ks._
branchial slits; _bb._ branchial vessel between them; _ch._ axial
portion of notochord; _chs._ peripheral layer of cells. Other
reference letters as before.]
The larva at this stage is represented in a side view in fig. 8 IV.
The epidermis is formed throughout of a single layer of cells. In the
trunk the mesenteron is shewn at _dd_ and the dilated part of the
nervous system, no longer communicating with the exterior, at _n_. In
the tail the notochord is shewn at _ch_, the muscles at _m_, and the
solid remnant of the ventral wall of the archenteron at _dd´_. The
delicate continuation of the neural canal in the tail is seen above
the notochord at _n_. An optical section of the tail is shewn in fig.
6. It is worthy of notice that the notochord and muscles are formed in
the same manner as in Amphioxus, except that the process is somewhat
simplified. The mode of disappearance of the archenteric cavity in the
tail, by the employment of the whole of its walls in the formation of
various organs, is so peculiar, that I feel some hesitation in
accepting Kowalevsky's statements on this head[6].
[6] It is more probable that this part of the alimentary tract is
equivalent to the postanal gut of many Vertebrata, which is at
first a complete tube, but disappears later by the simple
absorption of the walls.
The larva continues to grow in length, and the tail becomes further
curled round the ventral side of the body within the egg-membrane.
Before the tail has nearly reached its full length the test becomes
formed as a cuticular deposit of the epiblast cells (O. Hertwig, No.
13, Semper, No. 37). It appears first in the tail and gradually
extends till it forms a complete investment round both tail and trunk,
and is at first totally devoid of cells. Shortly after the
establishment of the test there grow out from the anterior end of the
body three peculiar papillæ, developed as simple thickenings of the
epidermis. At a later stage, after the hatching of the larva, these
papillæ develop glands at their extremities, secreting a kind of
glutinous fluid[7]. After these papillæ have become formed cells first
make their appearance in the test; and there is simultaneously formed
a fresh inner cuticular layer of the test, to which at first the cells
are confined, though subsequently they are found in the outer layer
also. On the appearance of cells in the test the latter must be
regarded as a form, though a very abnormal one, of connective tissue.
When the tail of the larva has reached a very considerable length the
egg-membrane bursts, and the larva becomes free. The hatching takes
place in Asc. canina about 48-60 hours after impregnation. The free
larva (fig. 8 V.) has a swollen trunk, and a very long tail, which
soon becomes straightened out. It has a striking resemblance to a
tadpole (_vide_ fig. 10).
[7] It is probable that these papillæ are very primitive organs
of the Chordata. Structures, which are probably of the same
nature, are formed behind the mouth in the larvæ of Amphibia, and
in front of the mouth in the larvæ of Ganoids (Acipenser,
Lepidosteus), and are used by these larvæ for attaching
themselves.
In the free larval condition the Ascidians have in many respects a
higher organization than in the adult state. It is accordingly
convenient to divide the subsequent development into two periods, the
first embracing the stages from the condition represented in fig. 8 V.
up to the full development of the free larva, and the second the
period from the full development of the larva to the attainment of the
fixed adult condition.
_Growth and Structure of the free larva._
The nervous system. The nervous system was left as a closed tube
consisting of a dilated anterior division, and a narrow posterior one.
The former may be spoken of as the brain, and the latter as the spinal
cord; although the homologies of these two parts are quite uncertain.
The anterior part of the spinal cord lying within the trunk dilates
somewhat (fig. 8 V. and VI. _Rg_) and there may thus be distinguished
a trunk and a caudal section of the spinal cord.
[FIG. 9. LARVA OF ASCIDIA MENTULA. (From Gegenbaur; after Kupffer.)
Only the anterior part of the tail is represented.
_N´_. anterior swelling of neural tube; _N._ anterior swelling of
spinal portion of neural tube; _n._ hinder part of neural tube;
_ch._ notochord; _K._ branchial region of alimentary tract; _d._
oesophageal and gastric region of alimentary tract; _O._ eye; _a._
otolith; _o._ mouth; _s._ papilla for attachment.]
The original single vesicle of the brain becomes divided by the time
the larva is hatched into two sections (fig. 9)--(1) an anterior
vesicle with, for the most part, thin walls, in which unpaired
auditory and optic organs make their appearance, and (2) a posterior
nearly solid cephalic ganglion, through which there passes a narrow
continuation of the central canal of the nervous system. This ganglion
consists of a dorsal section formed of distinct cells, and a ventral
section formed of a punctated material with nuclei. The auditory
organ[8] consists of a 'crista acustica' (fig. 9), in the form of a
slight prominence of columnar cells on the ventral side of the
anterior cerebral vesicle; to the summit of which a spherical otolith
is attached by fine hairs. In the crista is a cavity containing clear
fluid. The dorsal half of the otolith is pigmented: the ventral half
is without pigment. The crista is developed _in situ_, but the otolith
is formed from a single cell on the dorsal side of the cerebral
vesicle, which forms a projection into the cavity of the vesicle, and
then travels (in a manner not clearly made out) round the right side
of the vesicle till it comes to the crista; to which it is at first
attached by a narrow pedicle. The fully developed eye (figs. 8 VI. and
9, _O_) consists of a cup-shaped retina, which forms a prominence
slightly on the right side of the posterior part of the dorsal wall of
the anterior cerebral vesicle, and of refractive media. The retina is
formed of columnar cells, the inner ends of which are imbedded in
pigment. The refractive media of the eye are directed towards the
cavity of the cerebral vesicle, and consist of a biconvex lens and a
meniscus. Half the lens is imbedded in the cavity of the retina and
surrounded by the pigment, and the other half is turned toward a
concavo-convex meniscus which corresponds in position with the cornea.
The development of the meniscus and lens is unknown, but the retina is
formed (fig. 8 V. _a_) as an outgrowth of the wall of the brain. At
the inner ends of the cells of this outgrowth a deposit of pigment
appears.
[8] For a fuller account of the organs of sense _vide_ the
chapters on the eye and ear.
The trunk section of the spinal cord (fig. 9, _N_) is separated by a
sharp constriction from the brain. It is formed of a superficial layer
of longitudinal nervous fibres, and a central core of ganglion cells.
The layer of fibres diminishes in thickness towards the tail, and
finally ceases to be visible. Kupffer detected three pairs of nerves
passing off from the spinal cord to the muscles of the tail. The
foremost of these arises at the boundary between the trunk and the
tail, and the two others at regular intervals behind this point.
The mesoblast and muscular system. It has already been stated that the
lateral walls of the archenteron in the tail give rise to muscular
cells. These cells lie about three abreast, and appear not to increase
in number; so that with the growth of the tail they grow enormously in
length, and eventually become imperfectly striated. The mesoblast
cells at the hinder end of the trunk, close to its junction with the
tail, do not become converted into muscle cells, but give rise to
blood corpuscles; and the axial remnant of the archenteron undergoes a
similar fate. According to Kowalevsky the heart is formed during
larval life as an elongated closed sack on the right side of the
endostyle.
The notochord. The notochord was left as a rod formed of a single row
of cells, or in As. canina and some other forms of two rows, extending
from just within the border of the trunk to the end of the tail.
According to Kowalevsky, Kupffer, Giard, etc. the notochord undergoes
a further development which finds its only complete parallel amongst
Chordata in the doubtful case of Amphioxus.
There appear between the cells peculiar, highly refractive discs (fig.
8 V. _Chs_). These become larger and larger, and finally, after
pushing the remnants of the cells with their nuclei to the sides,
coalesce together to form a continuous axis of hyaline substance. The
remnants of the cells with their nuclei form a sheath round the
hyaline axis (fig. 8 VI. _ch._). Whether the axis is to be regarded as
formed of an intercellular substance, or of a differentiation of parts
of the cells is still doubtful. Kupffer inclines to the latter view:
the analogy of the notochord of higher types appears to me to tell in
favour of the former one.
The alimentary tract. The anterior part of the primitive archenteron
alone retains a lumen, and from this part the whole of the permanent
alimentary tract (mesenteron) becomes developed. The anterior part of
it grows upwards, and before hatching an involution of the epiblast on
the dorsal side, just in front of the anterior extremity of the
nervous system, meets and opens into this upgrowth, and gives rise to
the permanent mouth (fig. 8 V. _o_).
Kowalevsky states that a pore is formed at the front end of the
nervous tube leading into the mouth (fig. 8 V. and VI. _f_) which
eventually gives rise to the ciliated sack, which lies in the adult at
the junction between the mouth and the branchial sack. Kupffer however
was unable to find this opening; but Kowalevsky's observations are
confirmed by those of Salensky on Salpa.
From the hinder end of the alimentary sack an outgrowth directed
dorsalwards makes its appearance (figs. 8 V. and 9, _d_), from which
the oesophagus, stomach and intestine become developed. It at first
ends blindly. The remainder of the primitive alimentary sack gives
rise to the branchial sack of the adult. Just after the larva has
become hatched, the outgrowth to form the stomach and oesophagus, etc.
bends ventralwards and to the right, and then turns again in a dorsal
and left direction till it comes close to the dorsal surface, somewhat
to the left of and close to the hinder end of the trunk. The first
ventral loop of this part gives rise to the oesophagus, which opens
into the stomach; from this again the dorsally directed intestine
passes off.
On the ventral wall of the branchial sack there is formed a narrow
fold with thickened walls, which forms the endostyle. It ends
anteriorly at the stomodæum and posteriorly at the point where the
solid remnant of the archenteron in the tail was primitively
continuous with the branchial sack. The whole of the alimentary wall
is formed of a single layer of hypoblast cells.
A most important organ connected with the alimentary system still
remains to be dealt with, viz. the atrial or peribranchial cavity. The
first rudiments of it appear at about the time of hatching, in the
form of a pair of dorsal epiblastic involutions (fig. 8 V. _kl_), at
the level of the junction between the brain and the spinal cord. These
involutions grow inwards, and meet corresponding outgrowths of the
branchial sack, with which they fuse. At the junction between them is
formed an elongated ciliated slit, leading from the branchial sack
into the atrial cavity of each side. The slits so formed are the first
pair of branchial clefts. Behind the first pair of branchial clefts a
second pair is formed during larval life by a second outgrowth of the
branchial sack meeting the epiblastic atrial involutions (fig. 8 VI.
_1ks_ and _2ks_). The intestine at first ends blindly close to the
left atrial involution, but the anus becomes eventually formed by an
opening being established between the left atrial involution and the
intestine.
During the above described processes the test remains quite intact,
and is not perforated at the oral or the atrial openings.
_The retrogressive metamorphosis of the larva._
The development of the adult from the larva is, as has already been
stated, in the main a retrogressive metamorphosis. The stages in this
metamorphosis are diagrammatically shewn in figs. 10 and 11. It
commences with the attachment of the larva (fig. 10 A) which takes
place by one of the three papillæ. Simultaneously with the attachment
the larval tail undergoes a complete atrophy (fig. 10 B), so that
nothing is left of it but a mass of fatty cells situated close to the
point of the previous insertion of the tail in the trunk.
FIG. 10. DIAGRAM SHEWING THE MODE OF ATTACHMENT AND SUBSEQUENT
RETROGRESSIVE METAMORPHOSIS OF A LARVAL ASCIDIAN. (From Lankester.)
The nervous system also undergoes a very rapid retrogressive
metamorphosis; and the only part of it which persists would seem to be
the dilated portion of the spinal cord in the trunk (Kupffer, No. 28).
The three papillæ, including that serving for attachment, early
disappear, and the larva becomes fixed by a growth of the test to
foreign objects.
An opening appears in the test some time after the larva is fixed,
leading into the mouth, which then becomes functional. The branchial
sack at the same time undergoes important changes. In the larva it is
provided with only two ciliated slits, which open into the, at this
stage, paired atrial cavity (fig. 10).
The openings of the atrial cavity at first are shut off from
communication with the exterior by the test, but not long after the
larva becomes fixed, two perforations are formed in the test, which
lead into the openings of the two atrial cavities. At the same time
the atrial cavities dilate so as gradually to embrace the whole
branchial sack to which their inner walls attach themselves. Shortly
after this the branchial clefts rapidly increase in number[9].
[9] The account of the multiplication of the branchial clefts is
taken from Krohn's paper on Phallusia mammillata (No. 24), but
there is every reason to think that it holds true in the main for
simple Ascidians.
The increase of the branchial clefts is somewhat complicated. Between
the two primitive clefts two new ones appear, and then a third appears
behind the last cleft. In the interval between each branchial cleft is
placed a vascular branchial vessel (fig. 8 VI. _bb_). Soon a great
number of clefts become added in a row on each side of the branchial
sack. These clefts are small ciliated openings placed transversely
with reference to the long axis of the branchial sack, but only
occupying a small part of the breadth of each side. The intervals
dorsal and ventral to them are soon filled by series of fresh rows of
slits, separated from each other by longitudinal bars. Each side of
the branchial sack becomes in this way perforated by a number of small
openings arranged in rows, and separated by transverse and
longitudinal bars. The whole structure forms the commencement of the
branchial basketwork of the adult; the arrangement of which differs
considerably in structure and origin from the simple system of
branchial clefts of normal vertebrate types. At the junction of the
transverse and longitudinal bars papillæ are formed projecting into
the lumen of the branchial sack.
[FIG. 11. DIAGRAM OF A VERY YOUNG ASCIDIAN. (From Lankester.)]
After the above changes are far advanced towards completion, the
openings of the two atrial sacks gradually approximate in the dorsal
line, and finally coalesce to form the single atrial opening of the
adult. The two atrial cavities at the same time coalesce dorsally to
form a single cavity, which is continuous round the branchial sack,
except along the ventral line where the endostyle is present. The
atrial cavity, from its mode of origin as a pair of epiblastic
involutions[10], is clearly a structure of the same nature as the
branchial or atrial cavity of Amphioxus; and has nothing whatever to
do with the true body cavity.
[10] In the asexually produced buds of Ascidians the atrial cavity
appears, with the exception of the external opening, to be formed
from the primitive branchial sack. In the buds of Pyrosoma however
it arises independently. These peculiarities in the buds cannot
weigh against the embryonic evidence that the atrial cavity arises
from involutions of the epiblast, and they may perhaps be
partially explained by the fact that in the formation of the
visceral clefts outgrowths of the branchial sack meet the atrial
involutions.
It has already been stated that the anus opens into the original left
atrial cavity; when the two cavities coalesce the anus opens into the
atrial cavity in the median dorsal line.
Two of the most obscure points in the development are the origin of
the mesoblast in the trunk, and of the body cavity. Of the former
subject we know next to nothing, though it seems that the cells
resulting from the atrophy of the tail are employed in the nutrition
of the mesoblastic structures of the trunk.
The body cavity in the adult is well developed in the region of the
intestine, where it forms a wide cavity lined by an epithelioid
mesoblastic layer. In the region of the branchial sack it is reduced
to the vascular channels in the walls of the sack.
Kowalevsky believes the body cavity to be the original segmentation
cavity, but this view can hardly be regarded as admissible in the
present state of our knowledge. In some other Ascidian types a few
more facts about the mesoblast will be alluded to.
With the above changes the retrogressive metamorphosis is completed;
and it only remains to notice the change in position undergone in the
attainment of the adult state. The region by which the larva is
attached grows into a long process (fig. 10 B), and at the same time
the part carrying the mouth is bent upwards so as to be removed nearly
as far as possible from the point of attachment. By this means the
condition in the adult (fig. 11) is gradually brought about; the
original dorsal surface with the oral and atrial openings becoming the
termination of the long axis of the body, and the nervous system being
placed between the two openings.
The genus Molgula presents a remarkable exception amongst the simple
Ascidians in that, in some if not all the species belonging to it,
development takes place (Lacaze Duthiers 29 and 30, Kupffer 28) quite
directly and without larval metamorphosis.
The ova are laid either singly or adhering together, and are very
opaque. The segmentation (Lacaze Duthiers) commences by the formation
of four equal spheres, after which a number of small clear spheres are
formed which envelope the large spheres. The latter give rise to a
closed enteric sack, and probably also to a mass of cells situated on
the ventral side, which appear to be mesoblastic. The epiblast is
constituted of a single layer of cells which completely envelopes the
enteric sack and the mesoblast.
While the ovum is still within the chorion five peculiar processes of
epiblast grow out; four of which usually lie in the same sectional
plane of the embryo. They are contractile and contain prolongations of
the body cavity. Their relative size is very variable.
The nervous system is formed on the dorsal side of the embryo before
the above projections make their appearance, but, though it seems
probable that it originates in the same manner as in the more normal
forms, its development has not been worked out. As soon as it is
formed it consists of a nervous ganglion similar to that usually found
in the adult. The history of the mass of mesoblast cells has been
inadequately followed, but it continuously disappears as the heart,
excretory organs, muscles, etc. become formed. So far as can be
determined from Kupffer's descriptions the body cavity is primitively
parenchymatous--an indication of an abbreviated development--and does
not arise as a definite split in the mesoblast.
The primitive enteric cavity becomes converted into the branchial
sack, and from its dorsal and posterior corner the oesophagus, stomach
and intestine grow out as in the normal forms. The mouth is formed by
the invagination of a disc-like thickening of the epidermis in front
of the nervous system on the dorsal side of the body; and the atrial
cavity arises behind the nervous system by a similar process at a
slightly later period. The gill clefts opening into the atrial cavity
are formed as in the type of simple Ascidians described by Krohn.
The embryo becomes hatched not long after the formation of the oral
and atrial openings, and the five epiblastic processes undergo
atrophy. They are not employed in the attachment of the adult.
The larva when hatched agrees in most important points with the adult;
and is without the characteristic provisional larval organs of
ordinary forms; neither organs of special sense nor a tail becoming
developed. It has been suggested by Kupffer that the ventrally
situated mesoblastic mass is the same structure as the mass of
elements which results in ordinary types from the degeneration of the
tail. If this suggestion is true it is difficult to believe that this
mass has any other than a nutritive function.
The larva of Ascidia ampulloides described by P. van Beneden is
regarded by Kupffer as intermediate between the Molgula larva and the
normal type, in that the larval tail and notochord and a pigment spot
are first developed, while after the atrophy of these organs peculiar
processes like those of Molgula make their appearance.
Sedentaria. The development of the fixed composite Ascidians is, so
far as we know, in the main similar to that of the simple Ascidians.
The larvæ of Botryllus sometimes attain, while still in the free
state, a higher stage of development with reference to the number of
gill slits, etc. than that reached by the simple Ascidians, and in
some instances (Botryllus auratus _Metschnikoff_) eight conical
processes are found springing in a ring-like fashion around the trunk.
The presence of these processes has led to somewhat remarkable views
about the morphology of the group; in that they were regarded by
Kölliker, Sars, etc. as separate individuals, and it was supposed that
the product of each ovum was not a single individual, but a whole
system of individuals with a common cloaca.
The researches of Metschnikoff (No. 32), Krohn (No. 25), and Giard
(No. 12), etc. demonstrate that this paradoxical view is untenable,
and that each ovum only gives rise to a single embryo, while the
stellate systems are subsequently formed by budding.
Natantia. Our knowledge of the development of Pyrosoma is mainly due
to Huxley (No. 16) and Kowalevsky (No. 22). In each individual of a
colony of Pyrosoma only a single egg comes to maturity at one time.
This egg is contained in a capsule formed of a structureless wall
lined by a flattened epithelioid layer. From this capsule a duct
passes to the atrial cavity, which, though called the oviduct,
functions as an afferent duct for the spermatozoa.
The segmentation is meroblastic, and the germinal disc adjoins the
opening of the oviduct. The segmentation is very similar to that which
occurs in Teleostei, and at its close the germinal disc has the form
of a cap of cells, without a trace of stratification or of a
segmentation cavity, resting upon the surface of the yolk, which forms
the main mass of the ovum.
After segmentation the blastoderm, as we may call the layer of cells
derived from the germinal disc, rapidly spreads over the surface of
the yolk, and becomes divided into two layers, the epiblast and the
hypoblast. At the same time it exhibits a distinction into a central
clearer and a peripheral more opaque region. At one end of the
blastoderm, which for convenience sake may be spoken of as the
posterior end, a disc of epiblast appears, which is the first rudiment
of the nervous system, and on each side of the middle of the
blastoderm there arises an epiblastic involution. The epiblastic
involutions give rise to the atrial cavity.
These involutions rapidly grow in length, and soon form longish tubes,
opening at the surface by pores situated not far from the posterior
end of the blastoderm.
The blastoderm at this stage, as seen on the surface of the yolk, is
shewn in fig. 12 A. It is somewhat broader than long. The nervous
system is shewn at _n_, and _at_ points to an atrial tube. A
transverse section, through about the middle of this blastoderm, is
represented in fig. 12 B. The epiblast is seen above. On each side is
the section of an atrial tube (_at_). Below is the hypoblast which is
separated from the yolk especially in the middle line; at each side it
is beginning to grow in below, on the surface of the yolk. The space
below the hypoblast is the alimentary cavity, the ventral wall of
which is formed by the cells growing in at the sides. Between the
epiblast and hypoblast are placed scattered mesoblast cells, the
origin of which has not been clearly made out.
[FIG. 12.
A. SURFACE VIEW OF THE OVUM OF PYROSOMA NOT FAR ADVANCED IN
DEVELOPMENT. The embryonic structures are developed from a disc-like
blastoderm.
B. TRANSVERSE SECTION THROUGH THE MIDDLE PART OF THE SAME
BLASTODERM.
_at._ atrial cavity; _hy._ hypoblast; _n._ nervous disc in the
region of the future Cyathozooid.]
In a later stage the openings of the two atrial tubes gradually travel
backwards, and at the same time approximate, till finally they meet
and coalesce at the posterior end of the blastoderm behind the nervous
disc (fig. 13, _cl_). The tubes themselves at the same time become
slightly constricted not far from their hinder extremities, and so
divided into a posterior region nearly coterminous with the nervous
system (fig. 13), and an anterior region. These two regions have very
different histories in the subsequent development.
The nervous disc has during these changes become marked by a median
furrow (fig. 13, _ng_), which is soon converted into a canal by the
same process as in the simple Ascidians. The closure of the groove
commences posteriorly and travels forwards. These processes are
clearly of the same nature as those which take place in Chordata
generally in the formation of the central nervous system.
In the region of the germinal disc which contains the anterior part of
the atrial tubes, the alimentary cavity becomes, by the growth of the
layer of cells described in the last stage, a complete canal, on the
outer wall of which the endostyle is formed as a median fold. The
whole anterior part of the blastoderm becomes at the same time
gradually constricted off from the yolk.
[FIG. 13. BLASTODERM OF PYROSOMA SHORTLY BEFORE ITS DIVISION INTO
CYATHOZOOID AND ASCIDIOZOOIDS. (After Kowalevsky.)
_cl._ cloacal (atrial) opening; _en._ endostyle; _at._ atrial
cavity; _ng._ nervous groove.
The heart and pericardial cavity are seen to the left.]
The fate of the anterior and posterior parts of the blastoderm is very
different. The anterior part becomes segmented into four zooids or
individuals, called by Huxley Ascidiozooids, which give rise to a
fresh colony of Pyrosoma. The posterior part forms a rudimentary
zooid, called by Huxley Cyathozooid, which eventually atrophies. These
five zooids are formed by a process of embryonic fission. This fission
commences by the appearance of four transverse constrictions in the
anterior part of the blastoderm; by which the whole blastoderm becomes
imperfectly divided into five regions, fig. 14 A.
The hindermost constriction (uppermost in my figure) lies just in
front of the pericardial cavity; and separates the Cyathozooid from
the four ascidiozooids. The three other constrictions mark off the
four Ascidiozooids. The Cyathozooid remains for its whole length
attached to the blastoderm, which has now nearly enveloped the yolk.
It contains the whole of the nervous system (_ng_), which is covered
behind by the opening of the atrial tubes (_cl_). The alimentary tract
in the Cyathozooid forms a tube with very delicate walls. The
pericardial cavity is completely contained within the Cyathozooid, and
the heart itself (_ht_) has become formed by an involution of the
walls of the cavity.
The Ascidiozooids are now completely separated from the yolk. They
have individually the same structure as the undivided rudiment from
which they originated; so that the organs they possess are simply two
atrial tubes, an alimentary tract with an endostyle, and
undifferentiated mesoblast cells.
In the following stages the Ascidiozooids grow with great rapidity.
They soon cease to lie in a straight line, and eventually form a ring
round the Cyathozooid and attached yolk sack.
While these changes are being accomplished in the external form of the
colony, both the Cyathozooids and the Ascidiozooids progress
considerably in development. In the Cyathozooid the atrial spaces
gradually atrophy, with the exception of the external opening, which
becomes larger and more conspicuous. The heart at the same time comes
into full activity and drives the blood through the whole colony. The
yolk becomes more and more enveloped by the Cyathozooid, and is
rapidly absorbed; while the nutriment derived from it is transported
to the Ascidiozooids by means of the vascular connection. The nervous
system retains its previous condition; and round the Cyathozooid is
formed the test into which cells migrate, and arrange themselves in
very conspicuous hexagonal areas. The delicate alimentary tract of the
Cyathozooid is still continuous with that of the first Ascidiozooid.
After the Cyathozooid has reached the development just described it
commences to atrophy.
[FIG. 14. TWO STAGES IN THE DEVELOPMENT OF PYROSOMA IN WHICH THE
CYATHOZOOID AND FOUR ASCIDIOZOOIDS ARE ALREADY DISTINCTLY FORMED.
(After Kowalevsky.)
_cy._ cyathozooid; _as._ ascidiozooid; _ng._ nervous groove; _ht._
heart of cyathozooid; _cl._ cloacal opening.]
The changes in the Ascidiozooids are even more considerable than those
in the Cyathozooid. A nervous system appears as a fresh formation
close to the end of each Ascidiozooid turned towards the Cyathozooid.
It forms a tube of which the open front end eventually develops into
the ciliated pit of the mouth, and the remainder into the actual
nervous ganglion. Between the nervous system and the endostyle an
involution appears, which gives rise to the mouth. On each side of the
primitive alimentary cavity of each Ascidiozooid branchial slits make
their appearance, leading into the atrial tubes; so that the primitive
alimentary tract becomes converted into the branchial sacks of the
Ascidiozooids. The remainder of the alimentary tract of each zooid is
formed as a bud from the hind end of the branchial sack in the usual
way. The alimentary tracts of the four Ascidiozooids are at first in
free communication by tubes opening from the hinder extremity of one
zooid into the dorsal side of the branchial sack of the next zooid. At
the hinder end of each Ascidiozooid is developed a mass of fatty cells
known as the elæoblast, which probably represents a rudiment of the
larval tail of simple Ascidians. (Cf. pp. 30-32.)
The further changes consist in the gradual atrophy of the Cyathozooid,
which becomes more and more enclosed within the four Ascidiozooids.
These latter become completely enveloped in a common test, and form a
ring round the remains of the yolk and of the Cyathozooid, the heart
of which continues however to beat vigorously. The cloacal opening of
the Cyathozooid persists through all these changes, and, after the
Cyathozooid itself has become completely enveloped in the
Ascidiozooids and finally absorbed, deepens to form the common cloacal
cavity of the Pyrosoma colony.
The main parts of the Ascidiozooids were already formed during the
last stage. The zooids long remain connected together, and united by a
vascular tube with the Cyathozooid, and these connections are not
severed till the latter completely atrophies. Finally, after the
absorption of the Cyathozooid, the Ascidiozooids form a rudimentary
colony of four individuals enveloped in a common test. The two atrial
tubes of each zooid remain separate in front but unite posteriorly. An
anus is formed leading from the rectum into the common posterior part
of the atrial cavity; and an opening is established between the
posterior end of the atrial cavity of each Ascidiozooid and the common
axial cloacal cavity of the whole colony. The atrial cavities in
Pyrosoma are clearly lined by epiblast, just as in simple Ascidians.
When the young colony is ready to become free, it escapes from the
atrial cavity of the parent, and increases in size by budding.
Doliolidæ. The sexually developed embryos of Doliolum have been
observed by Krohn (No. 23), Gegenbaur (No. 10), and Keferstein and
Ehlers (No. 17); but the details of the development have been very
imperfectly investigated.
The youngest embryo observed was enveloped in a large oval transparent
covering, the exact nature of which is not clear. It is perhaps a
larval rudiment of the test which would seem to be absent in the
adult. Within this covering is the larva, the main organs of which are
already developed; and which primarily differs from the adult in the
possession of a larval tail similar to that of simple Ascidians.
In the body both oral and atrial openings are present, the latter on
the dorsal surface; and the alimentary tract is fully established. The
endostyle is already formed on the ventral wall of the branchial sack,
but the branchial slits are not present. Nine muscular rings are
already visible. The tail, though not so developed as in the simple
Ascidians, contains an axial notochord of the usual structure, and
lateral muscles. It is inserted on the ventral side, and by its slow
movements the larva progresses.
In succeeding stages the tail gradually atrophies, and the gill slits,
four in number, develop; at the same time a process or stolon,
destined to give rise by budding to a second non-sexual generation,
makes its appearance on the dorsal side in the seventh intermuscular
space. This stolon is comparable with that which appears in the embryo
of Salpa. When the tail completely atrophies the larva leaves its
transparent covering, and becomes an asexual Doliolum with a dorsal
stolon.
Salpidæ. As is well known the chains of Salpa alone are sexual, and
from each individual of the chain only a single embryo is produced.
The ovum from which this embryo takes its origin is visible long
before the separate Salps of the chain have become completely
developed. It is enveloped in a capsule continuous with a duct, which
opens into the atrial cavity, and is usually spoken of as the oviduct.
The capsule with the ovum is enveloped in a maternal blood sinus.
Embryonic development commences after the chain has become broken up,
and the spermatozoa derived from another individual would seem to be
introduced to the ovum through the oviduct.
At the commencement of embryonic development the oviduct and
ovicapsule undergo peculiar changes; and in part at least give rise to
a structure subservient to the nutrition of the embryo, known as the
placenta. These changes commence with the shortening of the oviduct,
and the disappearance of a distinction between oviduct and ovicapsule.
The cells lining the innermost end of the capsule, _i.e._ that at the
side of the ovum turned away from the atrial cavity, become at the
same time very columnar. The part of the oviduct between the ovum and
the atrial cavity dilates into a sack, communicating on the one hand
with the atrial cavity, and on the other by a very narrow opening with
the chamber in which the egg is contained. This sack next becomes a
prominence in the atrial cavity, and eventually constitutes a
brood-pouch. The prominence it forms is covered by the lining of the
atrial cavity, immediately within which is the true wall of the sack.
The external opening of the sack becomes gradually narrowed, and
finally disappears. In the meantime the chamber in which the embryo is
at first placed acquires a larger and larger opening into the sack;
till finally the two chambers unite, and a single brood-pouch
containing the embryo is thus produced. The inner wall of the chamber
is formed by the columnar cells already spoken of. They form the
rudiment of the placenta. The double wall of the outer part of the
brood-pouch becomes stretched by the growth of the embryo; the inner
of its two layers then atrophies. The outer layer subsequently gives
way, and becomes rolled back so as to lie at the inner end of the
embryo, leaving the latter projecting freely into the atrial cavity.
While these changes are taking place the placenta becomes fully
developed. The first rudiment of it consists, according to Salensky,
of the thickened cells of the ovicapsule only, though this view is
dissented from by Brooks, Todaro, etc. Its cells soon divide to form a
largish mass, which becomes attached to a part of the epiblast of the
embryo.
On the formation of the body cavity of the embryo a central axial
portion of the placenta becomes separated from a peripheral layer; and
a channel is left between them which leads from a maternal blood sinus
into the embryonic body cavity. The peripheral layer of the placenta
is formed of cells continuous with the epiblast of the embryo; while
the axial portion is constituted of a disc of cells adjoining the
embryo, with a column of fibres attached to the maternal side. The
fibres of this column are believed by Salensky to be products of the
original rudiment of the placenta. The placenta now assumes a more
spherical form, and its cavity becomes shut off from the embryonic
body cavity. The fibrous column breaks up into a number of strands
perforating the lumen of the organ, and the cells of the wall become
stalked bodies projecting into the lumen.
When the larva is nearly ready to become free the placenta atrophies.
The placenta functions in the nutrition of the embryo in the following
way. It projects from its first formation into a maternal blood sinus,
and, on the appearance of a cavity in it continuous with the body
cavity of the embryo, the blood of the mother fully intermingles with
that of the embryo. At a later period the communication with the body
cavity of the embryo is shut off, but the cavity of the placenta is
supplied with a continuous stream of maternal blood, which is only
separated from the foetal blood by a thin partition.
It is now necessary to turn to the embryonic development about which
it is unfortunately not as yet possible to give a completely
satisfactory account. The statements of the different investigators
contradict each other on most fundamental points. I have followed in
the main Salensky (No. 34), but have also called attention to some
points where his observations diverge most from those of other
writers, or where they seem unsatisfactory.
The development commences at about the period when the brood-pouch is
becoming formed; and the ovum passes entirely into the brood-pouch
before the segmentation is completed. The segmentation is regular, and
the existence of a segmentation cavity is denied by Salensky, though
affirmed by Kowalevsky and Todaro[11].
[11] From Todaro's latest paper (No. 39) it would seem the
segmentation cavity has very peculiar relations.
At a certain stage in the segmentation the cells of the ovum become
divided into two layers, an epiblast investing the whole of the ovum
with the exception of a small area adjoining the placenta, where the
inner layer or hypoblast, which forms the main mass of the ovum,
projects at the surface. The epiblast soon covers the whole of the
hypoblast, so that there would seem (according to Salensky's
observations) to be a kind of epibolic invagination: a conclusion
supported by Todaro's figures.
At a later stage, on one side of the free apex of the embryo, a
mesoblastic layer makes its appearance between the epiblast and
hypoblast. This layer is derived by Salensky, as it appears to me on
insufficient grounds, from the epiblast. Nearly at the same time there
arises not far from the same point of the embryo, but on the opposite
side, a solid thickening of epiblast which forms the rudiment of the
nervous system. The nervous system is placed close to the front end of
the body; and nearly at the opposite pole, and therefore at the hind
end, there appears immediately below the epiblast a mass of cells
forming a provisional organ known as the elæoblast. Todaro regards
this organ as mesoblastic in origin, and Salensky as hypoblastic. The
organ is situated in the position which would be occupied by the
larval tail were it developed. It may probably be regarded (Salensky)
as a disappearing rudiment of the tail, and be compared in this
respect with the more or less similar mass of cells described by
Kupffer in Molgula, and with the elæoblast in Pyrosoma.
After the differentiation of these organs a cavity makes its
appearance between the epiblast and hypoblast, which is regarded by
Salensky as the body cavity. It appears to be equivalent to the
segmentation cavity of Todaro. According to Todaro's statements, it is
replaced by a second cavity, which appears between the splanchnic and
somatic layers of mesoblast, and constitutes the true body cavity. The
embryo now begins to elongate, and at the same time a cavity makes its
appearance in the centre of the hypoblast cells. This cavity is the
rudiment of the branchial and alimentary cavities: on its dorsal wall
is a median projection, the rudiment of the so-called gill of Salpa.
At two points this cavity comes into close contact with the external
skin. At one of these, situated immediately ventral to the nervous
system, the mouth becomes formed at a later period. At the other,
placed on the dorsal surface between the nervous system and the
elæoblast, is formed the cloacal aperture.
By the stage under consideration the more important systems of organs
are established, and the remaining embryonic history may be very
briefly narrated.
The embryo at this stage is no longer covered by the walls of the
brood-pouch but projects freely into the atrial cavity, and is only
attached to its parent by means of the placenta. The epiblast cells
soon give rise to a deposit which forms the mantle. The deposit
appears however to be formed not only on the outer side of the
epiblast but also on the inner side; so that the epiblast becomes
cemented to the subjacent parts, branchial sack, etc., by an
intercellular layer, which would seem to fill up the primitive body
cavity with the exception of the vascular channels (Salensky).
The nervous system, after its separation from the epiblast, acquires a
central cavity, and subsequently becomes divided into three lobes,
each with an internal protuberance. At its anterior extremity it opens
into the branchial sack; and from this part is developed the ciliated
pit of the adult. The nervous ganglion at a later period becomes
solid, and a median eye is subsequently formed as an outgrowth from
it.
According to Todaro there are further formed two small auditory (?
olfactory) sacks on the ventral surface of the brain, each of them
placed in communication with the branchial cavity by a narrow canal.
The mesoblast gives rise to the muscles of the branchial sack, to the
heart, and to the pericardium. The two latter are situated on the
ventral side of the posterior extremity of the branchial cavity.
_Branchial sack and alimentary tract._ The first development of the
enteric cavity has already been described. The true alimentary tract
is formed as a bud from the hinder end of the primitive cavity. The
remainder of the primitive cavity gives rise to the branchial sack.
The so-called gill has at first the form of a lamella attached
dorsally to the walls of the branchial sack; but its attachment
becomes severed except at the two ends, and it then forms a band
stretching obliquely across the branchial cavity, which subsequently
becomes hollow and filled with blood corpuscles. The whole structure
is probably homologous with the peculiar fold, usually prolonged into
numerous processes, which normally projects from the dorsal wall of
the Ascidian branchial sack.
On the completion of the gill the branchial sack becomes divided into
a region dorsal to the gill, and a region ventral to it. Into the
former the single atrial invagination opens. No gill slits are formed
comparable with those in simple Ascidians, and the only representative
of these structures is the simple communication which becomes
established between the dorsal division of the branchial sack and the
atrial opening. The whole branchial sack of Salpa, including both the
dorsal and ventral divisions, corresponds with the branchial sack of
simple Ascidians. On its ventral side the endostyle is formed in the
normal way. The mouth arises at the point already indicated near the
front end of the nervous system[12].
[12] Brooks takes a very different view of the nature of the
parts in Salpa. He says, No. 7, p. 322, "The atrium of Salpa,
when first observed, was composed of two broad lateral atria
within the body cavity, one on each side of the branchial sack,
and a very small mid-atrium.... The lateral atria do not however,
as in most Tunicata, remain connected with the mid-atrium, and
unite with the wall of the branchial sack to form the branchial
slits, but soon become entirely separated, and the two walls of
each unite so as to form a broad sheet of tissue, which soon
splits up to form the muscular bands of the branchial sack."
Again, p. 324, "During the changes which have been described as
taking place in the lateral atria, the mid-atrium has increased
in size.... The branchial and atrial tunics now unite upon each
side, so that the sinus is converted into a tube which
communicates, at its posterior end, with the heart and
perivisceral sinus, and at the anterior end with the neural
sinus. This tube is the gill.... The centres of the two regions
upon the sides of the gill, where these two tissues have become
united, are now absorbed, so that a single long and narrow
branchial slit is produced on each side of the gill. The
branchial cavity is thus thrown into communication with the
atrium, and the upper surface of the latter now unites with the
outer tunic, and the external atrial opening is formed by
absorption."
The above description would imply that the atrial cavity is a
space lined by mesoblast, a view which would upset the whole
morphology of the Ascidians. Salensky's account, which implies
only an immense reduction in the size of the atrial cavity as
compared with other types, appears to me far more probable. The
lateral atria of Brooks appear to be simply parts of the body
cavity, and have certainly no connection with the lateral atria
of simple Ascidians or Pyrosoma.
The observations of Todaro upon Salpa (No. 38) are very
remarkable, and illustrated by beautifully engraved plates. His
interpretations do not however appear quite satisfactory. The
following is a brief statement of some of his results.
During segmentation there arises a layer of small superficial
cells (epiblast) and a central layer of larger cells, which
becomes separated from the former by a segmentation cavity,
except at the pole adjoining the free end of the brood-pouch. At
this point the epiblast cells become invaginated into the central
cells and form the alimentary tract, while the primitive central
cells remain as the mesoblast. A fold arises from the epiblast
which Todaro compares to the vertebrate amnion, but the origin of
it is unfortunately not satisfactorily described. The folds of
the amnion project towards the placenta, and enclose a cavity
which, as the folds never completely meet, is permanently open to
the maternal blood sinus. This cavity corresponds with the cavity
of the true amnion of higher Vertebrates. It forms the cavity of
the placenta already described. Between the two folds of the
amnion is a cavity corresponding with the vertebrate false
amnion. A structure regarded by Todaro as the notochord is formed
on the neck, connecting the involution of the alimentary tract
with the exterior. It has only a very transitory existence.
In the later stages the segmentation cavity disappears and a true
body cavity is formed by a split in the mesoblast.
Todaro's interpretations, and in part his descriptions also, both
with reference to the notochord and amnion, appear to me quite
inadmissible. About some other parts of his descriptions it is
not possible to form a satisfactory judgment. He has recently
published a short paper on this subject (No. 39) preliminary to a
larger memoir, which is very difficult to understand in the
absence of plates. He finds however in the placenta various parts
which he regards as homologous with the decidua vera and reflexa
of Mammalia.
Development of the chain of sexual Salps. My description of the
embryonic development of Salpa would not be complete without some
reference to the development of the stolon of the Solitary generation
of Salps by the segmentation of which a chain of sexual Salps
originates.
The asexual Salp, the embryonic development of which has just been
described, may be compared to the Cyathozooid of Pyrosoma, from which
it mainly differs in being fully developed. While still in an
embryonic condition it gives rise to a process or stolon, which
becomes divided into a number of zooids by transverse constrictions,
in the same manner that part of the germ of the ovum of Pyrosoma is
divided by transverse constrictions into four Ascidiozooids.
The stolon arises as a projection on the right side of the body of the
embryo close to the heart. It is formed (Salensky, No. 35) of an
outgrowth of the body wall, into which there grow the following
structures:
(1) A central hollow process from the end of the respiratory sack.
(2) A right and left lateral prolongation of the pericardial cavity.
(3) A solid process of cells on the ventral side derived from the
same mass of the cells as the elæoblast.
(4) A ventral and a dorsal blood sinus.
Besides these parts there appears on the dorsal side a hollow tube,
the origin of which is unknown, which gives rise to the nervous
system.
The hollow process of the respiratory sack is purely provisional, and
disappears without giving rise to any permanent structure. The right
and left prolongations of the pericardial cavity become solid and
eventually give origin to the mesoblast. The ventral process of cells
is the most important structure in the stolon in that it gives rise
both to the alimentary and respiratory sacks, and to the generative
organs of the sexual Salps. The stolon containing the organs just
enumerated becomes divided by transverse constrictions into a number
of rings. These rings do not long remain complete, but become
interrupted dorsally and ventrally. The imperfect rings so formed soon
overlap, and each of them eventually gives rise to a sexual Salp.
Although the stolon arises while the asexual Salp is still in an
embryonic condition, it does not become fully developed till long
after the asexual Salp has attained maturity.
Appendicularia. Our only knowledge of the development of
Appendicularia is derived from Fol's memoir on the group (No. 8). He
simply states that it develops, as far as he was able to follow, like
other Ascidians; and that the extremely minute size of the egg
prevented him from pursuing the subject. He also states that the pair
of pores leading from the branchial cavity to the exterior is
developed from epiblastic involutions meeting outgrowths of the wall
of the branchial sack.
_Metagenesis._
One of the most remarkable phenomena in connection with the life
history of many Ascidians is the occurrence of an alternation of
sexual and gemmiparous generations. This alternation appears to have
originated from a complication of the process of reproduction by
budding, which is so common in this group. The mode in which this very
probably took place will be best understood by tracing a series of
transitional cases between simple budding and complete alternations of
generations.
In the simpler cases, which occur in some Composita Sedentaria, the
process of budding commences with an outgrowth of the body wall into
the common test, containing a prolongation of part of the alimentary
tract[13].
[13] It is not within the scope of this work to enter into
details with reference to the process of budding. The reader is
referred on this head more especially to the papers of Huxley
(No. 16) and Kowalevsky (No. 22) on Pyrosoma, of Salensky (No.
35) on Salpa, and Kowalevsky (No. 21) on Ascidians generally. It
is a question of very great interest how budding first arose, and
then became so prevalent in these degenerate types of Chordata.
It is possible to suppose that budding may have commenced by the
division of embryos at an early stage of development, and have
gradually been carried onwards by the help of natural selection
till late in life. There is perhaps little in the form of budding
of the Ascidians to support this view--the early budding of
Didemnum as described by Gegenbaur being the strongest evidence
for it--but it fits in very well with the division of the embryo
in Lumbricus trapezoides described by Kleinenberg, and with the
not unfrequent occurrence of double monsters in Vertebrata which
may be regarded as a phenomenon of a similar nature (Rauber). The
embryonic budding of Pyrosoma, which might perhaps be viewed as
supporting the hypothesis, appears to me not really in favour of
it; since the Cyathozooid of Pyrosoma is without doubt an
extremely modified form of zooid, which has obviously been
specially developed in connection with the peculiar reproduction
of the Pyrosomidæ.
Between the epiblastic and hypoblastic layers of the bud so formed, a
mesoblastic and sometimes a generative outgrowth of the parent also
appears.
The systems of organs of the bud are developed from the corresponding
layers to those in the embryo[14]. The bud eventually becomes
detached, and in its turn gives rise to fresh buds. Both the bud and
its parent reproduce sexually as well as by budding: the new colonies
being derived from sexually produced embryos.
[14] The atrial spaces form somewhat doubtful exceptions to the
rule.
The next stage of complication is that found in Botryllus (Krohn, Nos.
25 and 26). The larva produced sexually gives rise to a bud from the
right side of the body close to the heart. On the bud becoming
detached the parent dies away without developing sexual organs. The
bud of the second generation gives rise to two buds, a right one and a
left one, and like the larva dies without reaching sexual maturity.
The buds of the third generation each produce two buds and then suffer
the same fate as their parent.
The buds of the third generation arrange themselves with their cloacal
extremities in contact, and in the fourth generation a common cloaca
is formed, and so a true radial system of zooids is established; the
zooids of which are not however sexual.
The buds of the fourth generation in their turn produce two or three
buds and then die away.
Fresh systems become formed by a continuation of the process of
budding, but the zooids of the secondary systems so formed are sexual.
The ova come to maturity before the spermatozoa, so that cross
fertilization takes place.
In Botryllus we have clearly a rudimentary form of alternations of
generations, in that the sexually produced larva is asexual, and,
after a series of asexual generations, produced gemmiparously, there
appear sexual generations, which however continue to reproduce
themselves by budding.
The type of alternations of generations observable in Botryllus
becomes, as pointed out by Huxley, still more marked in Pyrosoma.
The true product of the ovum is here (_vide_ p. 25) a rudimentary
individual called by Huxley the Cyathozooid. This gives rise, while
still an embryo, by a process equivalent to budding to four fully
developed zooids (Ascidiozooids) similar to the parent form, and
itself dies away. The four Ascidiozooids form a fresh colony, and
reproduce (1) sexually, whereby fresh colonies are formed, and (2) by
ordinary budding, whereby the size of the colony is increased. All the
individuals of the colony are sexual.
The alternation of generations in Pyrosoma widely differs from that in
Botryllus in the fact of the Cyathozooid differing so markedly in its
anatomical characters from the ordinary zooids.
In Salpa the process is slightly different[15]. The sexual forms are
_now incapable of budding_, and, although at first a series of sexual
individuals are united together in the form of a chain, so as to form
a colony like Pyrosoma or Botryllus, yet they are so loosely connected
that they separate in the adult state. As in Botryllus, the ova are
ripe before the spermatozoa. Each sexual individual gives rise to a
single offspring, which, while still in the embryonic condition, buds
out a 'stolon' from its right ventral side. This stolon is divided
into a series of lateral buds after the solitary asexual Salp has
begun to lead an independent existence. The solitary asexual Salp
clearly corresponds with the Cyathozooid of Pyrosoma, though it has
not, like the Cyathozooid, undergone a retrogressive metamorphosis.
[15] _Vide_ p. 33.
By far the most complicated form of alternation of generations known
amongst the Ascidians is that in Doliolum. The discovery of this
metamorphosis was made by Gegenbaur (No. 10). The sexual form of
Doliolum is somewhat cask-shaped, with ring-like muscular bands, and
the oral and atrial apertures placed at opposite ends of the cask. The
number of gill slits varies according to the species. The ovum gives
rise, as already described, to a tailed embryo which subsequently
develops into a cask-shaped asexual form. On attaining its full size
it loses its branchial sack and alimentary tract. While still in the
embryonic condition, a stolon grows out from its dorsal side in the
seventh intermuscular space. The stolon, like that in Salpa, contains
a prolongation of the branchial sack[16].
[16] I draw this conclusion from Gegenbaur's fig. (No. 10), Pl.
XVI., fig. 15. The body (_x_) in the figure appears to me without
doubt the rudiment of the stolon, and not, as believed by
Gegenbaur, the larval tail.
On this stolon there develop two entirely different types of buds, (1)
lateral buds, (2) dorsal median buds.
The lateral buds are developed in regular order on the two sides of
the stolon, and the most advanced buds are those furthest removed from
the base. They give rise to forms with a very different organization
to that of the parent. They are compared by Gegenbaur to a spoon, the
bowl of which is formed by the branchial sack, and the handle by the
stalk attaching the bud to the stolon. The oral opening into the
branchial sack is directed upwards: _an atrial opening is remarkably
enough not present_. The branchial sack is perforated by numerous
openings. It leads into an alimentary tract which opens directly to
the exterior by an anus opposite the mouth.
The stalks attaching the more mature buds to the stolon are provided
with ventrally directed scales, which completely hide the stolon in a
view from the ventral surface.
These buds have, even after their detachment, no trace of generative
organs, and shew no signs of reproducing themselves by budding. Their
eventual fate is unknown.
The median dorsal buds have no such regular arrangement as the lateral
buds, but arise in irregular bunches, those furthest removed from the
base of the stolon being however the oldest. These buds are almost
exactly similar to the original sexual form; they do not acquire
sexual organs, but are provided with a stolon attached on the ventral
side, in the sixth intermuscular space.
This stolon is simply the stalk by which each median bud was
primitively attached to the stolon of the first asexual form.
From the stolon of the median buds of the second generation buds are
developed which grow into the sexual forms.
The generations of Doliolum may be tabulated in the following way.
Sexual generation,
|
1st asexual form with dorsal stolon,
_________________|_____________________
| |
spoon-like forms developed as 2nd asexual forms developed as
lateral buds (eventual history median buds with ventral stolon,
unknown). |
sexual generation.
BIBLIOGRAPHY.
(6) P. J. van Beneden. "Recherches s. l'Embryogénie, l'Anat. et la
Physiol. des Ascidies simples." _Mém. Acad. Roy. de Belgique_, Tom.
XX.
(7) W. K. Brooks. "On the development of Salpa." _Bull. of the Museum
of Comp. Anat. at Harvard College, Cambridge, Mass._
(8) H. Fol. _Etudes sur les Appendiculaires du détroit de Messine_.
Genève et Bâle, 1872.
(9) Ganin. "Neue Thatsachen a. d. Entwicklungsgeschichte d. Ascidien."
_Zeit. f. wiss. Zool._, Vol. XX. 1870.
(10) C. Gegenbaur. "Ueber den Entwicklungscyclus von Doliolum nebst
Bemerkungen über die Larven dieser Thiere." _Zeit. f. wiss. Zool._,
Bd. VII. 1856.
(11) A. Giard. "Etudes critiques des travaux d'embryogénie relatifs à
la parenté des Vertebrés et des Tuniciers." _Archiv Zool.
expériment._, Vol. I. 1872.
(12) A. Giard. "Recherches sur les Synascidies." _Archiv Zool.
expér._, Vol. I. 1872.
(13) O. Hertwig. "Untersuchungen üb. d. Bau u. d. Entwicklung des
Cellulose-Mantels d. Tunicaten." _Jenaische Zeitschrift_, Bd. VII.
1873.
(14) Th. H. Huxley. "Remarks upon Appendicularia and Doliolum." _Phil.
Trans._, 1851.
(15) Th. H. Huxley. "Observations on the anatomy and physiology of
Salpa and Pyrosoma." _Phil. Trans._, 1851.
(16) Th. H. Huxley. "Anatomy and development of Pyrosoma." _Linnean
Trans._, 1860, Vol. XXIII.
(17) Keferstein u. Ehlers. _Zoologische Beiträge_, 1861. Doliolum.
(18) A. Kowalevsky. "Entwicklungsgeschichte d. einfachen Ascidien."
_Mém. Acad. Pétersbourg_, VII. série, T. X. 1866.
(19) A. Kowalevsky. "Beitrag z. Entwick. d. Tunicaten." _Nachrichten
d. königl. Gesell. zu Göttingen._ 1868.
(20) A. Kowalevsky. "Weitere Studien üb. d. Entwicklung d. einfachen
Ascidien." _Archiv f. mikr. Anat._, Vol. VII. 1871.
(21) A. Kowalevsky. "Ueber Knospung d. Ascidien." _Archiv f. mikr.
Anat._, Vol. X. 1874.
(22) A. Kowalevsky. "Ueber die Entwicklungsgeschichte d. Pyrosoma."
_Archiv f. mikr. Anat._, Vol. XI. 1875.
(23) A. Krohn. "Ueber die Gattung Doliolum u. ihre Arten." _Archiv f.
Naturgeschichte_, Bd. XVIII. 1852.
(24) A. Krohn. "Ueber die Entwicklung d. Ascidien." _Müller's Archiv_,
1852.
(25) A. Krohn. "Ueber die Fortpflanzungsverhältnisse d. Botrylliden."
_Archiv f. Naturgeschichte_, Vol. XXXV. 1869.
(26) A. Krohn. "Ueber die früheste Bildung d. Botryllenstöcke."
_Archiv f. Naturgeschichte_, Vol. XXXV. 1869.
(27) C. Kupffer. "Die Stammverwandschaft zwischen Ascidien u.
Wirbelthieren." _Archiv f. mikr. Anat._, Vol. VI. 1870.
(28) C. Kupffer. "Zur Entwicklung d. einfachen Ascidien." _Archiv f.
mikr. Anat._, Vol. VIII. 1872.
(29) H. Lacaze Duthiers. "Recherches sur l'organisation et
l'Embryogénie des Ascidies (Molgula tubulosa)." _Comptes rendus_, May
30, 1870, p. 1154.
(30) H. Lacaze Duthiers. "Les Ascidies simples des Côtes de France"
(Development of Molgula). _Archiv Zool. expér._, Vol. III. 1874.
(31) R. Leuckart. "Salpa u. Verwandte." _Zoologische Untersuchungen_,
Heft II.
(32) E. Metschnikoff. "Observations sur le développement de quelques
animaux (Botryllus and Simple Ascidians)." _Bull. d. l'Acad.
Pétersbourg_, Vol. XIII. 1869.
(33) H. Milne-Edwards. "Observations s. l. Ascidies composées des
côtes de la Manche." _Mémoires d. l'Institut_, T. XVIII. 1842.
(34) W. Salensky. "Ueber d. embryonale Entwicklungsgeschichte der
Salpen." _Zeit. f. wiss. Zool._, B. XXVII. 1877.
(35) W. Salensky. "Ueber die Knospung d. Salpen." _Morphol. Jahrbuch_,
Bd. III. 1877.
(36) W. Salensky. "Ueber die Entwicklung d. Hoden u. über den
Generationswechsel d. Salpen." _Zeit. f. wiss. Zool._, Bd. XXX. Suppl.
1878.
(37) C. Semper. "Ueber die Entstehung d. geschichteten
Cellulose-Epidermis d. Ascidien." _Arbeit. a. d. zool.-zoot. Instit.
Würzburg_, Vol. II. 1875.
(38) Fr. Todaro. _Sopra lo sviluppo e l'anatomia delle Salpe._ Roma,
1875.
(39) Fr. Todaro. "Sui primi fenomeni dello sviluppo delle Salpe."
_Reale Accademia dei Lincei_, Vol. IV. 1880.
CHAPTER III.
ELASMOBRANCHII.
The impregnation of the ovum is effected in the oviduct. In most forms
the whole of the subsequent development, till the time when the embryo
is capable of leading a free existence, takes place in the uterus; but
in other cases the egg becomes enveloped, during its passage down the
oviduct, first in a layer of fluid albumen, and finally in a dense
horny layer, which usually takes the form of a quadrilateral capsule
with characters varying according to the species. After the formation
of this capsule the egg is laid, and the whole of the development,
with the exception of the very first stages, takes place externally.
In many of the viviparous forms (Mustelus, Galeus, Carcharias,
Sphyrna) the egg is enclosed, during the early stages of development
at any rate, in a very delicate shell homologous with that of the
oviparous forms; there is usually also a scanty albuminous layer. Both
of these are stated by Gerbe (No. 42) to be absent in Squalus spinax.
The following are examples of viviparous genera: Hexanchus, Notidanus,
Acanthias, Scymnus, Galeus, Squalus, Mustelus, Carcharias, Sphyrna,
Squatina, Torpedo; and the following of oviparous genera: Scyllium,
Pristiurus, Cestracion, Raja[17].
[17] For further details, _vide_ Müller (No. 48).
The ovum at the time of impregnation has the form of a large spherical
mass, similar to the yolk of a bird's egg, but without a vitelline
membrane[18]. The greater part of it is formed of peculiar oval
spherules of food-yolk, held together by a protoplasmic network. The
protoplasm is especially concentrated in a small lens-shaped area,
known as the germinal disc, which is not separated by a sharp line
from the remainder of the ovum. Yolk spherules are present in this
disc as elsewhere, but are much smaller and of a different character.
The segmentation has the normal meroblastic character (fig. 15) and is
confined to the germinal disc. Before it commences the germinal disc
exhibits amoeboid movements. During the segmentation nuclei make their
appearance spontaneously (?) in the yolk adjoining the germinal disc
(fig. 15, _nx´_), and around them portions of the yolk with its
protoplasmic network become segmented off. Cells are thus formed which
are added to those resulting from the segmentation proper. Even after
the segmentation numerous nuclei are present in the granular matter
below the blastoderm (fig. 16 A, _n´_); and around these cells are
being continually formed, which enter the blastoderm, and are more
especially destined to give rise to the hypoblast. The special
destination of many of these cells is spoken of in detail below.
[18] _Vide_ Vol. II., p. 62.
[FIG. 15. SECTION THROUGH GERMINAL DISC OF A PRISTIURUS EMBRYO
DURING THE SEGMENTATION.
_n._ nucleus; _nx._ nucleus modified prior to division; _nx´._
modified nucleus in the yolk; _f._ furrow appearing in the yolk
adjacent to the germinal disc.]
At the close of segmentation the blastoderm forms a somewhat
lens-shaped disc, thicker at one end than at the other; the thicker
end being the embryonic end. It is divided into two strata--an upper
one, the epiblast--formed of a single row of columnar cells; and a
lower one, the primitive hypoblast, consisting of the remaining cells
of the blastoderm, and forming a mass several strata deep. These cells
will be spoken of as the lower layer cells, to distinguish them from
the true hypoblast which is one of their products.
[FIG. 16. TWO LONGITUDINAL SECTIONS OF THE BLASTODERM OF A
PRISTIURUS EMBRYO DURING STAGES PRIOR TO THE FORMATION OF THE
MEDULLARY GROOVE.
_ep._ epiblast; _ll._ lower layer cells or primitive hypoblast; _m._
mesoblast; _hy._ hypoblast; _sc._ segmentation cavity; _es._ embryo
swelling; _n´._ nuclei of yolk; _er._ embryonic rim. _c._ lower
layer cells at the non-embryonic end of the blastoderm.]
A cavity very soon appears in the lower layer cells, near the
non-embryonic end of the blastoderm, but the cells afterwards
disappear from the floor of this cavity, which then lies between the
yolk and the lower layer cells (fig. 16 A, _sc_). This cavity is the
segmentation cavity equivalent to that present in Amphioxus, Amphibia,
etc. The chief peculiarity about it is the relatively late period at
which it makes its appearance, and the fact that its roof is formed
both by the epiblast and by the lower layer cells. Owing to the large
size of the segmentation cavity the blastoderm forms a thin layer
above the cavity and a thickened ridge round its edge.
[FIG. 17. LONGITUDINAL SECTION THROUGH THE BLASTODERM OF A
PRISTIURUS EMBRYO OF THE SAME AGE AS FIG. 28 B.
_ep._ epiblast; _er._ embryonic rim; _m._ mesoblast; _al._
mesenteron.]
The epiblast in the next stage is inflected for a small arc at the
embryonic end of the blastoderm, where it becomes continuous with the
lower layer cells; at the same time some of the lower layer cells of
the embryonic end of the blastoderm assume a columnar form, and
constitute the true hypoblast. The portion of the blastoderm, where
epiblast and hypoblast are continuous, forms a projecting structure
which will be called the embryonic rim (fig. 16 B, _er_).
This rim is a very important structure, since it represents the dorsal
portion of the lip of the blastopore of Amphioxus. The space between
it and the yolk represents the commencing mesenteron, of which the
hypoblast on the under side of the lip is the dorsal wall. The ventral
wall of the mesenteron is at first formed solely of yolk held together
by a protoplasmic network with numerous nuclei. The cavity under the
lip becomes rapidly larger (fig. 17, _al_), owing to the continuous
conversion of lower layer cells into columnar hypoblast along an axial
line passing from the middle of the embryonic rim towards the centre
of the blastoderm. The continuous differentiation of the hypoblast
towards the centre of the blastoderm corresponds with the invagination
in Amphioxus. During the formation of the embryonic rim the blastoderm
grows considerably larger, but, with the exception of the formation of
the embryonic rim, retains its primitive constitution.
The segmentation cavity undergoes however important changes. There is
formed below it a floor of lower layer cells, derived partly from an
ingrowth from the two sides, but mainly from the formation of cells
around the nuclei of the yolk (fig. 16). Shortly after the floor of
cells has appeared, the whole segmentation cavity becomes obliterated
(fig. 17).
The disappearance of the segmentation cavity corresponds in point of
time with the formation of the hypoblast by the pseudo-invagination
above described; and is probably due to this pseudo-invagination, in
the same way that the disappearance of the segmentation cavity in
Amphioxus is due to the true invagination of the hypoblast.
When the embryonic rim first appears there are no external indications
of the embryo as distinguished from the blastoderm, but when it has
attained to some importance the position of the embryo becomes marked
out by the appearance of a shield-like area extending inwards from the
edge of the embryonic rim, and formed of two folds with a groove
between them (fig. 28 B, _mg_), which is deepest at the edge of the
blastoderm, and shallows out as it extends inwards. This groove is the
medullary groove; and its termination at the edge of the blastoderm is
placed at the hind end of the embryo.
At about the time of its appearance the mesoblast becomes first
definitely established.
[FIG. 18. TWO TRANSVERSE SECTIONS OF AN EMBRYO OF THE SAME AGE AS
FIG. 17.
A. Anterior section.
B. Posterior section.
_mg._ medullary groove; _ep._ epiblast; _hy._ hypoblast; _n.al._
cells formed round the nuclei of the yolk which have entered the
hypoblast; _m._ mesoblast.
The sections shew the origin of the mesoblast.]
At the edge of the embryonic rim the epiblast and lower layer cells
are continuous. Immediately underneath the medullary groove, as is
best seen in transverse section (fig. 18), the whole of the lower
layer cells become converted into hypoblast, and along this line the
columnar hypoblast is in contact with the epiblast above. At the sides
however this is not the case; but at the junction of the epiblast and
lower layer cells the latter remain undifferentiated. A short way from
the edge the lower layer cells become divided into two distinct
layers, a lower one continuous with the hypoblast in the middle line,
and an upper one between this and the epiblast (fig. 18 B). The upper
layer is the commencement of the mesoblast (_m_). The mesoblast thus
arises as two independent lateral plates, one on each side of the
medullary groove, which are continuous behind with the undifferentiated
lower layer cells at the edge of the embryonic rim. The mesoblast
plates are at first very short, and do not extend to the front end of
the embryo. They soon however grow forwards as two lateral ridges,
attached to the hypoblast, one on each side of the medullary groove
(fig. 18 A, _m_). These ridges become separate from the hypoblast, and
form two plates, thinner in front than behind; but still continuous at
the edge of the blastoderm with the undifferentiated cells of the lip
of the blastopore, and laterally with the lower layer cells of the
non-embryonic part of the blastoderm. It results from the above mode
of development of the mesoblast, that it may be described as arising
in the form of a pair of solid outgrowths of the wall of the
alimentary tract; which differ from the mesoblastic outgrowths of the
wall of the archenteron in Amphioxus in not containing a prolongation
of the alimentary cavity.
[FIG. 19. DIAGRAMMATIC LONGITUDINAL SECTIONS OF AN ELASMOBRANCH
EMBRYO.
_Epiblast_ without shading. _Mesoblast_ black with clear outlines to
the cells. _Lower layer cells_ and _hypoblast_ with simple shading.
_ep._ epiblast; _m._ mesoblast; _al._ alimentary cavity; _sg._
segmentation cavity; _nc._ neural canal; _ch._ notochord; _x._ point
where epiblast and hypoblast become continuous at the posterior end
of the embryo; _n._ nuclei of yolk.
A. Section of young blastoderm, with segmentation cavity enclosed in
the lower layer cells.
B. Older blastoderm with embryo in which hypoblast and mesoblast are
distinctly formed, and in which the alimentary slit has appeared.
The segmentation cavity is still represented as being present,
though by this stage it has in reality disappeared.
C. Older blastoderm with embryo in which the neural canal has become
formed, and is continuous posteriorly with the alimentary canal. The
notochord, though shaded like mesoblast, belongs properly to the
hypoblast.]
A general idea of the structure of the blastoderm at this stage may be
gathered from the diagram representing a longitudinal section through
the embryo (fig. 19 B). In this figure the epiblast is represented in
white and is seen to be continuous at the lip of the blastopore (_x_)
with the shaded hypoblast. Between the epiblast and hypoblast is seen
one of the lateral plates of mesoblast, represented by black cells
with clear outlines. The non-embryonic lower layer cells of the
blastoderm are represented in the same manner as the mesoblast of the
body. The alimentary cavity is shewn at _al_, and below it is seen the
yolk with nuclei (_n_). The segmentation cavity is represented as
still persisting, though by this stage it would have disappeared.
[FIG. 20. THREE SECTIONS THROUGH A PRISTIURUS EMBRYO SOMEWHAT
YOUNGER THAN FIG. 28 C.
A. Section through the cephalic plate.
B. Section through the posterior part of the cephalic plate.
C. Section through the trunk.
_ch._ notochord; _mg._ medullary groove; _al._ alimentary tract;
_lp._ lateral plate of mesoblast; _pp._ body cavity.]
As to the growth of the blastoderm it may be noted that it has greatly
extended itself over the yolk. Its edge in the meantime forms a marked
ridge, which is due not so much to a thickening as to an arching of
the epiblast. This ridge is continuous with the embryonic rim, which
gradually concentrates itself into two prominences, one on each side
of the tail of the embryo, mainly formed of masses of undifferentiated
lower layer cells. These prominences will be called the caudal
swellings.
By this stage the three layers of the body, the epiblast, mesoblast,
and hypoblast, have become definitely established. The further history
of these layers may now be briefly traced.
Epiblast. While the greater part of the epiblast becomes converted
into the external epidermis, from which involutions give rise to the
olfactory and auditory pits, the lens of the eye, the mouth cavity,
and anus, the part of it lining the medullary groove becomes converted
into the central nervous system and optic cup. The medullary groove is
at first continued to the front end of the medullary plate; but the
anterior part of this plate soon enlarges, and the whole plate assumes
a spatula form (fig. 28 C, _h_, and fig. 20 A and B). The enlarged
part becomes converted into the brain, and may be called the cephalic
plate.
The posterior part of the canal deepens much more rapidly than the
rest (fig. 20 C), and the medullary folds unite dorsally and convert
the posterior end of the medullary groove into a closed canal, while
the groove is still widely open elsewhere. The medullary canal does
not end blindly behind, but simply forms a tube not closed at either
extremity. The importance of this fact will appear later.
Shortly after the medullary folds have met behind the whole canal
becomes closed in. This occurs in the usual way by the junction and
coalescence of the medullary folds. In the course of the closing of
the medullary groove the edges of the cephalic plate, which have at
first a ventral curvature, become bent up in the normal manner, and
enclose the dilated cephalic portion of the medullary canal. The
closing of the medullary canal takes place earlier in the head and
neck than in the back.
An anterior pore at the front end of the canal, like that in Amphioxus
and the Ascidians, is not found. The further differentiation of the
central nervous system is described in a special chapter: it may
however here be stated that the walls of the medullary canal give rise
not only to the central nervous system but to the peripheral also.
Mesoblast. The mesoblast was left as two lateral plates continuous
behind with the undifferentiated cells of the caudal swellings.
The cells composing them become arranged in two layers (fig. 20 C,
_lp_), a splanchnic layer adjoining the hypoblast, and a somatic layer
adjoining the epiblast. Between these two layers there is soon
developed in the region of the head a well-marked cavity (fig. 20 A,
_pp_) which is subsequently continued into the region of the trunk,
and forms the primitive body cavity, equivalent to the cavity
originating as an outgrowth of the archenteron in Amphioxus. The body
cavities of the two sides are at first quite independent.
[FIG. 21. TRANSVERSE SECTION THROUGH THE TRUNK OF AN EMBRYO SLIGHTLY
OLDER THAN FIG. 28 E.
_nc._ neural canal; _pr._ posterior root of spinal nerve; _x._
subnotochordal rod; _ao._ aorta; _sc._ somatic mesoblast; _sp._
splanchnic mesoblast; _mp._ muscle-plate; _mp´._ portion of
muscle-plate converted into muscle; _Vv._ portion of the vertebral
plate which will give rise to the vertebral bodies; _al._ alimentary
tract.]
Coincidentally with the appearance of differentiation into somatic and
splanchnic layers the mesoblast plates become in the region of the
trunk partially split by a series of transverse lines of division into
mesoblastic somites. Only the dorsal parts of the plates become split
in this way, their ventral parts remaining quite intact. As a result
of this each plate becomes divided into a dorsal portion adjoining the
medullary canal, which is divided into somites, and may be called the
_vertebral plate_, and a ventral portion not so divided, which may be
called the _lateral plate_. These two parts are at this stage quite
continuous with each other; and the body cavity originally extends
uninterruptedly to the summit of the vertebral plates (fig. 21).
[FIG. 22. HORIZONTAL SECTION THROUGH THE TRUNK OF AN EMBRYO OF
SCYLLIUM CONSIDERABLY YOUNGER THAN 28 F.
The section is taken at the level of the notochord, and shews the
separation of the cells to form the vertebral bodies from the
muscle-plates.
_ch._ notochord; _ep._ epiblast; _Vr._ rudiment of vertebral body;
_mp._ muscle-plate; _mp´._ portion of muscle-plate already
differentiated into longitudinal muscles.]
The next change results in the complete separation of the vertebral
portion of the plate from the lateral portion; thereby the upper
segmented part of the body cavity becomes isolated, and separated from
the lower and unsegmented part. As a consequence of this change the
vertebral plate comes to consist of a series of rectangular bodies,
the mesoblastic somites, each composed of two layers, a somatic and a
splanchnic, between which is the cavity originally continuous with the
body cavity (fig. 23, _mp_). The splanchnic layer of the plates buds
off cells to form the rudiments of the vertebral bodies which are at
first segmented in the same planes as the mesoblastic somites (fig.
22, _Vr_). The plates themselves remain as the muscle-plates (_mp_),
and give rise to the whole of the voluntary muscular system of the
body. Between the vertebral and lateral plates there is left a
connecting isthmus, with a narrow prolongation of the body cavity
(fig. 23 B, _st_), which gives rise (as described in a special
chapter) to the segmental tubes and to other parts of the excretory
system.
In the meantime the lateral plates of the two sides unite ventrally
throughout the intestinal and cardiac regions of the body, and the two
primitively isolated cavities contained in them coalesce. In the tail
however the plates do not unite ventrally till somewhat later, and
their contained cavities remain distinct till eventually obliterated.
At first the pericardial cavity is quite continuous with the body
cavity; but it eventually becomes separated from the body cavity by
the attachment of the liver to the abdominal wall, and by a horizontal
septum in which run the two ductus Cuvieri (fig. 23 A, _sv_). Two
perforations in this septum (fig. 23 A) leave the cavities in
permanent communication.
The parts derived from the two layers of the mesoblast (not including
special organs or the vascular system) are as follows:--
From the somatic layer are formed
(1) A considerable part of the voluntary muscular system of the
body.
(2) The dermis.
(3) A large part of the intermuscular connective tissue.
(4) Part of the peritoneal epithelium.
From the splanchnic layer are formed
(1) A great part of the voluntary muscular system.
(2) Part of the intermuscular connective tissue.
(3) The axial skeleton and surrounding connective tissue.
(4) The muscular and connective-tissue wall of the alimentary tract.
(5) Part of the peritoneal epithelium.
[FIG. 23. SECTIONS THROUGH THE TRUNK OF A SCYLLIUM EMBRYO SLIGHTLY
YOUNGER THAN 28 F.
Figure A shews the separation of the body cavity from the
pericardial cavity by a horizontal septum in which runs the ductus
Cuvieri; on the left side is seen the narrow passage which remains
connecting the two cavities. Fig. B through a posterior part of the
trunk shews the origin of the segmental tubes and of the primitive
ova.
_sp.c._ spinal canal; _W._ white matter of spinal cord; _pr._
commissure connecting the posterior nerve-roots; _ch._ notochord;
_x._ subnotochordal rod; _ao._ aorta; _sv._ sinus venosus; _cav._
cardinal vein; _ht._ heart; _pp._ body cavity; _pc._ pericardial
cavity; _oes._ solid oesophagus; _l._ liver; _mp._ muscle-plate;
_mp´._ inner layer of muscle-plate; _Vr._ rudiment of vertebral
body; _st._ segmental tube; _sd._ segmental duct; _sp.v._ spiral
valve; _v._ subintestinal vein.]
In the region of the head the mesoblast does not at first become
divided into somites; but on the formation of the gill clefts a
division takes place, which is apparently equivalent to the
segmentation of the mesoblast in the trunk. This division causes the
body cavity of the head to be divided up into a series of separate
segments, one of which is shewn in fig. 24, _pp_. The walls of the
segments eventually give rise to the main muscles of the branchial
clefts, and probably also to the muscles of the mandibular arch, of
the eye, and of other parts. The cephalic sections of the body cavity
will be spoken of as head cavities.
[FIG. 24. HORIZONTAL SECTION THROUGH THE LAST VISCERAL ARCH BUT ONE
OF AN EMBRYO OF PRISTIURUS.
_ep._ epiblast; _vc._ pouch of hypoblast which will form the walls
of a visceral cleft; _pp._ segment of body-cavity in visceral arch;
_aa._ aortic arch.]
In addition to the parts already mentioned the mesoblast gives rise to
the whole of the vascular system, and to the generative system. The
heart is formed from part of the splanchnic mesoblast, and the
generative system from a portion of the mesoblast of the dorsal part
of the body cavity.
The hypoblast. Very shortly after the formation of the mesoblastic
plates as lateral differentiations of the lower layer cells, an axial
differentiation of the hypoblast appears, which gives rise to the
notochord very much in the same way as in Amphioxus.
At first the hypoblast along the axial line forms a single layer in
contact with the epiblast. Along this line a rod-like thickening of
the hypoblast very soon appears (fig. 25, B and C, _Ch´_) at the head
end of the embryo, and gradually extends backwards. This is the
rudiment of the notochord; it remains attached for some time to the
hypoblast, and becomes separated from it first at the head end of the
embryo (fig. 25 A, _ch_): the separation is then carried backwards.
A series of sections taken through an embryo shortly after the first
differentiation of the notochord presents the following characters.
In the hindermost sections the hypoblast retains a perfectly normal
structure and uniform thickness throughout. In the next few sections
(fig. 25 C, _Ch´_) a slight thickening is to be observed in it,
immediately below the medullary groove. The layer, which elsewhere is
composed of a single row of cells, here becomes two cells deep, but no
sign of a division into two layers is exhibited.
In the next few sections the thickening of the hypoblast becomes much
more pronounced; we have, in fact, a ridge projecting from the
hypoblast towards the epiblast (fig. 25 B, _Ch´_). This ridge is
pressed firmly against the epiblast, and causes in it a slight
indentation. The hypoblast in the region of the ridge is formed of two
layers of cells, the ridge being entirely due to the uppermost of the
two.
[FIG. 25. THREE SECTIONS OF A PRISTIURUS EMBRYO SLIGHTLY OLDER THAN
FIG. 28 B.
The sections shew the development of the notochord.
_Ch._ notochord; _Ch´._ developing notochord; _mg._ medullary
groove; _lp._ lateral plate of mesoblast; _ep._ epiblast; _hy._
hypoblast.]
In sections in front of this a cylindrical rod, which can at once be
recognized as the notochord, and is continuous with the ridge just
described, begins to be split off from the hypoblast (fig. 25 A,
_Ch_). It is difficult to say at what point the separation of this rod
from the hypoblast is completed, since all intermediate gradations
between complete separation and complete attachment are to be seen.
Shortly after the separation takes place, a fairly thick bridge is
found connecting the two lateral halves of the hypoblast, but this
bridge is anteriorly excessively delicate and thin, and in some cases
is barely visible except with high powers. In some sections I have
observed possible indications of the process like that described by
Calberla for Petronyzon, by which the lateral parts of the hypoblast
grow in underneath the axial part, and so isolate it bodily as the
notochord.
It is not absolutely clear whether the notochord is to be regarded as
an axial differentiation of the hypoblast, or as an axial
differentiation of the lower layer cells.
The facts of development both in Amphioxus and Elasmobranchii tend
towards the former view; but the nearly simultaneous differentiation
of the notochord and the mesoblastic plates lends some support to the
supposition that the notochord may be merely a median plate of
mesoblast developed slightly later than the two lateral plates.
The alimentary canal or mesenteron was left as a space between the
hypoblast and the yolk, ending blindly in front, but opening behind by
a widish aperture, the blastopore or anus of Rusconi (_vide_ fig. 19
B).
[FIG. 26. SECTION THROUGH THE ANTERIOR PART OF A PRISTIURUS EMBRYO
TO SHEW THE FORMATION OF THE ALIMENTARY TRACT.
_Ch._ notochord; _hy._ hypoblast; _al._ alimentary tract; _na._
cells passing in from the yolk to form the ventral wall of the
alimentary tract.]
The conversion of this irregular cavity into a closed canal commences
first of all at the anterior extremity. In this conversion two
distinct processes are concerned. One of these is a process of folding
off of the embryo from the blastoderm. The other is a simple growth of
cells independent of any fold. To the first of these processes the
depth and narrowness of the alimentary cavity is due; the second is
concerned in forming its ventral wall. The process of the folding off
of the embryo from the blastoderm resembles exactly the similar
process in the embryo bird. The fold is a perfectly continuous one
round the front end of the embryo, but may be conveniently spoken of
as composed of a head-fold and two lateral folds.
Of far greater interest than the nature of these folds is the
formation of the ventral wall of the alimentary canal. This originates
in a growth of cells from the two sides to the middle line (fig. 26).
The cells for it are not however mainly derived from pre-existing
hypoblast cells, but are formed _de novo_ around the nuclei of the
yolk which have already been spoken of (fig. 26, _na_). The ventral
wall of the mesenteron is in fact, to a large extent at any rate,
formed as a differentiation of the primitive yolk floor.
[FIG. 27. LONGITUDINAL VERTICAL SECTION OF AN EMBRYO SLIGHTLY
YOUNGER THAN THAT IN FIG. 26 D.
The section shews the communication which exists between the neural
and alimentary canals.
_nc._ neural canal; _al._ alimentary tract; _Ch._ notochord; _Ts._
tail swelling.]
The folding off and closing of the alimentary canal in the anterior
part of the body proceeds rapidly, and not only is a considerable
tract of the alimentary canal formed, but a great part of the head is
completely folded off from the yolk before the medullary groove is
closed.
The posterior part of the alimentary canal retains for a longer time
its primitive condition. Finally however it also becomes closed in, by
the lips of the blastopore at the hind end of the embryo meeting and
uniting. The peculiarity of the closing in of the posterior part of
the alimentary canal consists in the fact that a similar continuity to
that in Amphioxus obtains between the neural and alimentary canals.
This is due to the medullary folds being continuous at the end of the
tail with the lips of the blastopore, which close in the hind end of
the alimentary canal; so that, when the medullary folds unite to form
a canal, this canal becomes continuous with the alimentary canal,
which is closed in at the same time. In other words, the medullary
folds assist in enveloping the blastopore which does not therefore
become absolutely closed, but opens into the floor of the neural
canal. It will afterwards be shewn that it is only the posterior part
of the blastopore that becomes closed during the above process, and
that the anterior and ventral part long remains open. The general
arrangement of the parts, at the time when the hind end of the
mesenteron is first closed, is shewn in fig. 27. The same points may
be seen in the diagrammatic longitudinal section fig. 19 C.
The middle portion of the alimentary tract is the last to be closed in
since it remains till late in embryonic life as the umbilical or
vitelline canal, connecting the yolk-sack with the alimentary cavity.
The umbilical canal falls into the alimentary tract immediately behind
the entrance of the hepatic duct.
[FIG. 27*. TRANSVERSE SECTION THROUGH THE TAIL REGION OF A
PRISTIURUS EMBRYO OF THE SAME AGE AS FIG. 28 E.
_df_. dorsal fin; _sp.c_. spinal cord; _pp_. body cavity; _sp_.
splanchnic layer of mesoblast; so. somatic layer of mesoblast; _mp_.
commencing differentiation of muscles; _ch_. notochord; _x_.
subnotochordal rod arising as an outgrowth of the dorsal wall of the
alimentary tract; _al_. alimentary tract.]
At a fairly early stage of development a rod is constricted off from
the dorsal wall of the alimentary canal (figs. 27* and 23 _x_), which
is known as the subnotochordal rod. It is placed immediately below the
notochord, and disappears during embryonic life.
_General features of the Elasmobranch embryo at successive stages._
Shortly after the three germinal layers become definitely established,
the rudiment of the embryo, as visible from the surface, consists of
an oblong plate, which extends inwards from the periphery of the
blastoderm, and is bounded on its inner side by a head-fold and two
lateral folds (fig. 28 B). This plate is the medullary plate; along
its axial line is a shallow groove--the medullary groove (_mg_). The
rudiment of the embryo rapidly increases in length, and takes a
spatula-like form (fig. 28 C). The front part of it, turned away from
the edge of the blastoderm, soon becomes dilated into a broad
plate,--the cephalic plate (_h_)--while the tail end at the edge of
the blastoderm is also enlarged, being formed of a pair of
swellings--the tail swellings (_ts_)--derived from the lateral parts
of the original embryonic rim. By this stage a certain number of
mesoblastic somites have become formed but are not shewn in my figure.
They are the foremost somites of the trunk, and those behind them
continue to be added, like the segments in Chætopods, between the last
formed somite and the end of the body. The increase in length of the
body mainly takes place by growth in the region between the last
mesoblastic somite and the end of the tail. The anterior part of the
body is now completely folded off from the blastoderm, and the
medullary groove of the earlier stage has become converted into a
closed canal.
By the next stage (fig. 28 D) the embryo has become so much folded off
from the yolk both in front and behind that the separate parts of it
begin to be easily recognizable.
The embryo is attached to the yolk by a distinct stalk or cord, which
in the succeeding stages gradually narrows and elongates, and is known
as the umbilical cord (_so. s_.). The medullary canal has now become
completely closed. The anterior region constitutes the brain; and in
this part slight constrictions, not perceptible in views of the embryo
as a transparent object, mark off three vesicles. These vesicles are
known as the fore, mid, and hind brain. From the fore-brain there is
an outgrowth on each side, the first rudiment of the optic vesicles
(_op_). The tail swellings are still conspicuous.
[FIG. 28. VIEWS OF ELASMOBRANCH EMBRYOS.
A-F. PRISTIURUS. G. and H. SCYLLIUM.
A. A blastoderm before the formation of the medullary plate. _sc._
segmentation cavity; _es._ embryonic swelling.
B. A somewhat older blastoderm in which the medullary groove has
been established. _mg._ medullary groove.
C. An embryo from the dorsal surface, as an opaque object, after the
medullary groove has become posteriorly converted into a tube. _mg._
medullary groove: the reference line points very nearly to the
junction between the open medullary groove with the medullary tube;
_h._ cephalic plate; _ts._ tail swelling.
D. Side view of a somewhat older embryo as a transparent object.
_ch._ notochord; _op._ optic vesicle; _1.v.c._ 1st visceral cleft;
_al._ alimentary tract; _so.s._ stalk connecting the yolk-sack with
the embryo.
E. Side view of an older embryo as a transparent object. _mp._
muscle-plates; _au.v._ auditory vesicle; _vc._ visceral cleft; _ht._
heart; _m._ mouth invagination; _an._ anal diverticulum; _al.v._
posterior vesicle of postanal gut.
F. G. H. Older embryos as opaque objects.]
The tissues of the body have now become fairly transparent, and there
may be seen at the sides of the body seventeen mesoblastic somites.
The notochord, which was formed long before the stage represented in
figure 28 D, is now also distinctly visible. It extends from almost
the extreme posterior to the anterior end of the embryo, and lies
between the ventral wall of the spinal canal and the dorsal wall of
the intestine. Round its posterior end the neural and alimentary
tracts become continuous with each other. Anteriorly the termination
of the notochord cannot be seen, it can only be traced into a mass of
mesoblast at the base of the brain, which there separates the epiblast
from the hypoblast. The alimentary canal (_al_) is completely closed
anteriorly and posteriorly, though still widely open to the yolk-sack
in the middle part of its course. In the region of the head it
exhibits on each side a slight bulging outwards, the rudiment of the
first visceral cleft. This is represented in the figure by two lines
(1. _v.c._).
The embryo represented in fig. 28 E is far larger than the one just
described, but it has not been convenient to represent this increase
of size in the figure. Accompanying this increase in size, the folding
off from the yolk has considerably progressed, and the stalk which
unites the embryo with the yolk is proportionately narrower and longer
than before.
The brain is now very distinctly divided into the three lobes, the
rudiments of which appeared during the last stage. From the foremost
of these the optic vesicles now present themselves as well-marked
lateral outgrowths, towards which there has appeared an involution
from the external skin (_op_) to form the lens.
A fresh organ of sense, the auditory sack, now for the first time
becomes visible as a shallow pit in the external skin on each side of
the hind-brain (_au.v_). The epiblast which is involuted to form this
pit becomes much thickened, and thereby the opacity, indicated in the
figure, is produced.
The mesoblastic somites have greatly increased in number by the
formation of fresh somites in the tail. Thirty-eight of them were
present in the embryo figured. The mesoblast at the base of the brain
is more bulky, and there is still a mass of unsegmented mesoblast
which forms the tail swellings. The first rudiment of the heart (_ht_)
becomes visible during this stage as a cavity between the mesoblast of
the splanchnopleure and the hypoblast.
The fore and hind guts are now longer than they were. An invagination
from the exterior to form the mouth has appeared (_m_) on the ventral
side of the head close to the base of the thalamencephalon. The upper
end of this eventually becomes constricted off as the pituitary body,
and an indication of the future position of the anus is afforded by a
slight diverticulum of the hind gut towards the exterior, some little
distance from the posterior end of the embryo (_an_). The portion of
the alimentary canal behind this point, though at this stage large,
and even dilated into a vesicle at its posterior end (_al.v_), becomes
eventually completely atrophied. It is known as the postanal gut. In
the region of the throat the rudiment of a second visceral cleft has
appeared behind the first; neither of them is as yet open to the
exterior.
In a somewhat older embryo the first spontaneous movements take place,
and consist in somewhat rapid excursions of the embryo from side to
side, produced by a serpentine motion of the body.
[FIG. 28*. FOUR SECTIONS THROUGH THE POSTANAL PART OF THE TAIL OF AN
EMBRYO OF THE SAME AGE AS FIG. 28 F.
A is the posterior section.
_nc._ neural canal; _al._ postanal gut; _alv._ caudal vesicle of
postanal gut; _x._ subnotochord rod; _mp._ muscle-plate; _ch._
notochord; _cl.al._ cloaca; _ao._ aorta; _v.cau._ caudal vein.]
A ventral flexure of the præoral part of the head, known as the
cranial flexure, which commenced in earlier stages (fig. 28 D and E),
has now become very evident, and the mid-brain[19] begins to project
in the same manner as in the embryo fowl on the third day, and will
soon form the anterior termination of the long axis of the embryo. The
fore-brain has increased in size and distinctness, and the anterior
part of it may now be looked on as the unpaired rudiment of the
cerebral hemispheres.
[19] The part of the brain which I have here called mid-brain,
and which unquestionably corresponds to the part called mid-brain
in the embryos of higher vertebrates, becomes in the adult what
Miklucho-Maclay and Gegenbaur called the vesicle of the third
ventricle or thalamencephalon.
Further changes have taken place in the organs of sense, especially in
the eye, in which the involution for the lens has made considerable
progress. The number of the muscle-plates has again increased, but
there is still a region of unsegmented mesoblast in the tail. The
thickened portions of mesoblast, which caused the tail swellings, are
still to be seen, and would seem to act as the reserve from which is
drawn the matter for the rapid growth of the tail, which occurs soon
after this. The mass of the mesoblast at the base of the brain has
again increased. No fresh features of interest are to be seen in the
notochord. The heart is very much more conspicuous than before, and
its commencing flexure is very apparent. It now beats actively. The
postanal gut is much longer than during the last stage; and the point
where the anus will appear is very easily detected by a bulging out of
the gut towards the external skin. The alimentary vesicle at the end
of the postanal gut, first observable during the last stage, is now a
more conspicuous organ. There are three visceral clefts, none of which
are as yet open to the exterior.
Figure 28 F represents a considerably older embryo viewed as an opaque
object, and fig. 29 A is a view of the head as a transparent object.
The stalk connecting it with the yolk is now, comparatively speaking,
quite narrow, and is of sufficient length to permit the embryo to
execute considerable movements.
The tail has grown immensely, but is still dilated terminally. The
terminal dilatation is mainly due to the alimentary vesicle (fig. 28*
_alv_), but the postanal section of the alimentary tract in front of
this is now a solid cord of cells. Both the alimentary vesicle and
this cord very soon disappear. Their relations are shewn in section in
fig. 28*.
The two pairs of limbs have appeared as differentiations of a
continuous but not very conspicuous epiblastic thickening, which is
probably the rudiment of a lateral fin. The anterior pair is situated
just at the front end of the umbilical stalk; and the posterior pair,
which is the later developed and less conspicuous of the two, is
situated some little distance behind the stalk.
[FIG. 29. VIEWS OF THE HEAD OF ELASMOBRANCH EMBRYOS AT TWO STAGES AS
TRANSPARENT OBJECTS.
A. Pristiurus embryo of the same stage as fig. 28 F.
B. Somewhat older Scyllium embryo.
_III._ third nerve; _V._ fifth nerve; _VII._ seventh nerve; _au.n._
auditory nerve; _gl._ glossopharyngeal nerve; _Vg._ vagus nerve;
_fb._ fore-brain; _pn._ pineal gland; _mb._ mid-brain; _hb._
hind-brain; _iv.v._ fourth ventricle; _cb._ cerebellum; _ol._
olfactory pit; _op._ eye; _au.V._ auditory vesicle; _m._ mesoblast
at base of brain; _ch._ notochord; _ht._ heart; _Vc._ visceral
clefts; _eg._ external gills; _pp._ sections of body cavity in the
head.]
The cranial flexure has greatly increased, and the angle between the
long axis of the front part of the head and of the body is less than a
right angle. The conspicuous mid-brain (29 A, _mb_) forms the anterior
termination of the long axis of the body. The thin roof of the fourth
ventricle (_hb_) may be noticed in the figure behind the mid-brain.
The auditory sack (_au.V_) is nearly closed, and its opening is not
shewn in the figure. In the eye (_op_) the lens is completely formed.
The olfactory pit (_ol_) is seen a little in front of the eye.
Owing to the opacity of the embryo, the muscle-plates are only
indistinctly indicated in fig. 28 F, and no other features of the
mesoblast are to be seen.
The mouth is now a deep pit, the hind borders of which are almost
completely formed by a thickening in front of the first branchial or
visceral cleft, which may be called the first branchial arch or
mandibular arch.
Four branchial clefts are now visible, all of which are open to the
exterior, but in the embryo, viewed as a transparent object, two more,
not open to the exterior, are visible behind the last of these.
Between each of these and behind the last one there is a thickening of
the mesoblast which gives rise to a branchial arch. The arch between
the first and second cleft is known as the hyoid arch.
Fig. 29 B is a representation of the head of a slightly older embryo
in which papillæ may be seen in the front wall of the second, third,
and fourth branchial clefts; these papillæ are the commencements of
filiform processes which grow out from the gill-clefts and form
external gills. The peculiar ventral curvature of the anterior end of
the notochord (_ch_) both in this and in the preceding figure deserves
notice.
A peculiar feature in the anatomy makes its appearance at this period,
viz. the replacement of the original hollow oesophagus by a solid cord
of cells (fig. 23 A, _oes_) in which a lumen does not reappear till
very much later. I have found that in some Teleostei (the Salmon) long
after they are hatched a similar solidity in the oesophagus is
present. It appears not impossible that this feature in the oesophagus
may be connected with the fact that in the ancestors of the present
types the oesophagus was perforated by gill slits; and that in the
process of embryonic abbreviation the stage with the perforated
oesophagus became replaced by a stage with a cord of indifferent cells
(the oesophagus being in the embryo quite functionless) out of which
the non-perforated oesophagus was directly formed. In the higher types
the process of development appears to have become quite direct.
By this stage all the parts of the embryo have become established, and
in the succeeding stages the features characteristic of the genus and
species are gradually acquired.
Two embryos of Scyllium are represented in fig. 28 G and H, the head
and anterior part of the trunk being represented in fig. G, and the
whole embryo at a much later stage in fig. H.
In both of these, and especially in the second, an apparent diminution
of the cranial flexure is very marked. This diminution is due to the
increase in the size of the cerebral hemispheres, which grow upwards
and forwards, and press the original fore-brain against the mid-brain
behind.
In fig. G the rudiments of the nasal sacks are clearly visible as
small open pits.
The first cleft is no longer similar to the rest, but by the closure
of the lower part has commenced to be metamorphosed into the spiracle.
Accompanying the change in position of the first cleft, the mandibular
arch has begun to bend round so as to enclose the front as well as the
sides of the mouth. By this change in the mandibular arch the mouth
becomes narrowed in an antero-posterior direction.
In fig. H are seen the long filiform external gills which now project
out from all the visceral clefts, including the spiracle. They are
attached to the front wall of the spiracle, to both walls of the next
four clefts, and to the front wall of the last cleft. They have very
possibly become specially developed to facilitate respiration within
the egg; and they disappear before the close of larval life.
When the young of Scyllium and other Sharks are hatched they have all
the external characters of the adult. In Raja and Torpedo the early
stages, up to the acquirement of a shark-like form, are similar to
those in the Selachoidei, but during the later embryonic stages the
body gradually flattens out, and assumes the adult form, which is thus
clearly shewn to be a secondary acquirement.
An embryonic gill cleft behind the last present in the adult is found
(Wyman, No. 54) in the embryo of Raja batis.
The unpaired fins are developed in Elasmobranchs as a fold of skin on
the dorsal side, which is continued round the end of the tail along
the ventral side to the anus. Local developments of this give rise to
the dorsal and anal fins. The caudal fin is at first symmetrical, but
a special lower lobe grows out and gives to it a heterocercal
character.
_Enclosure of the yolk-sack and its relation to the embryo._
The blastoderm at the stage represented in fig. 28 A and B forms a
small and nearly circular patch on the surface of the yolk, composed
of epiblast and lower layer cells. While the body of the embryo is
gradually being moulded this patch grows till it envelopes the yolk;
the growth is not uniform, but is less rapid in the immediate
neighbourhood of the embryonic part of the blastoderm than elsewhere.
As a consequence of this, that part of the edge, to which the embryo
is attached, forms a bay in the otherwise regular outline of the edge
of the blastoderm, and by the time that about two-thirds of the yolk
is enclosed this bay is very conspicuous. It is shewn in fig. 30 A,
where _bl_ points to the blastoderm, and _yk_ to the part of the yolk
not yet covered by the blastoderm. The embryo at this time is only
connected with the yolk-sack by a narrow umbilical cord; but, as shewn
in the figure, is still attached to the edge of the blastoderm.
[FIG. 30. THREE VIEWS OF THE VITELLUS OF AN ELASMOBRANCH, SHEWING
THE EMBRYO, THE BLASTODERM, AND THE VESSELS OF THE YOLK-SACK.
The shaded part (_bl_) is the blastoderm; the white part the
uncovered yolk.
A. Young stage with the embryo still attached at the edge of the
blastoderm.
B. Older stage with the yolk not quite enclosed by the blastoderm.
C. Stage after the complete enclosure of the yolk.
_yk._ yolk; _bl._ blastoderm; _v._ venous trunks of yolk-sack; _a._
arterial trunks of yolk-sack; _y._ point of closure of the yolk
blastopore; _x._ portion of the blastoderm outside the arterial
sinus terminalis.]
Shortly subsequent to this the bay in the blastoderm, at the head of
which the embryo is attached, becomes obliterated by its two sides
coming together and coalescing. The embryo then ceases to be attached
at the edge of the blastoderm. But a linear streak formed by the
coalesced edges of the blastoderm is left connecting the embryo with
the edge of the blastoderm. This streak is probably analogous to
(though not genetically related with) the primitive streak in the
Amniota.
This stage is represented in fig. 30 B. In this figure there is only a
small patch of yolk (_yk_) not yet enclosed, which is situated at some
little distance behind the embryo. Throughout all this period the edge
of the blastoderm has remained thickened: a feature which persists
till the complete investment of the yolk, which takes place shortly
after the stage last described. In this thickened edge a circular vein
arises which brings back the blood from the yolk-sack to the embryo.
The opening in the blastoderm, exposing the portion of the yolk not
yet covered, may be conveniently called the yolk blastopore. It is
interesting to notice that, owing to the large size of the yolk in
Elasmobranchs, the posterior part of the primitive blastopore becomes
encircled by the medullary folds and tail swellings, and is so closed
long before the anterior and more ventral part, which is represented
by the uncovered portion of the yolk. It is also worth remarking that,
owing to the embryo becoming removed from the edge of the blastoderm,
the final closure of the yolk blastopore takes place _at some little
distance from the embryo_.
The blastoderm enclosing the yolk is formed of an external layer of
epiblast, a layer of mesoblast below in which the blood-vessels are
developed, and within this a layer of hypoblast, which is especially
well marked and ciliated (Leydig, No. 46) in the umbilical stalk,
where it lines the canal leading from the yolk-sack to the intestine.
In the region of the yolk-sack proper the blastoderm is so thin that
it is not easy to be quite sure that a layer of hypoblast is
throughout distinct. Both the hypoblast and mesoblast of the yolk-sack
are formed by a differentiation of the primitive lower layer cells.
Nutriment from the yolk-sack is brought to the embryo partly through
the umbilical canal and so into the intestine, and partly by means of
blood-vessels in the mesoblast of the sack. The blood-vessels arise
before the blastoderm has completely covered the yolk.
Fig. 30 A represents the earliest stage of the circulation of the
yolk-sack. At this stage there is visible a single arterial trunk
(_a_) passing forwards from the embryo and dividing into two branches.
No venous trunk could be detected with the simple microscope, but
probably venous channels were present in the thickened edge of the
blastoderm.
In fig. 30 B the circulation is greatly advanced. The blastoderm has
now nearly completely enveloped the yolk, and there remains only a
small circular space (_yk_) not enclosed by it. The arterial trunk is
present as before, and divides in front of the embryo into two
branches which turn backwards and form a nearly complete ring round
the embryo. In general appearance this ring resembles the sinus
terminalis of the area vasculosa of the Bird, but in reality bears
quite a different relation to the circulation. It gives off branches
on its inner side only.
A venous system of returning vessels is now fully developed, and its
relations are very remarkable. There is a main venous ring in the
thickened edge of the blastoderm, which is connected with the embryo
by a single stem running along the seam where the edges of the
blastoderm have coalesced. Since the venous trunks are only developed
behind the embryo, it is only the posterior part of the arterial ring
that gives off branches.
The succeeding stage (fig. 30 C) is also one of considerable interest.
The arterial ring has greatly extended, and now embraces nearly half
the yolk, and sends off trunks on its inner side along its whole
circumference. More important changes have taken place in the venous
system. The blastoderm has now completely enveloped the yolk, and the
venous ring is therefore reduced to a point. The small veins which
originally started from it may be observed diverging in a brush-like
fashion from the termination of the unpaired trunk, which originally
connected the venous ring with the heart.
At a still later stage the arterial ring embraces the whole yolk, and,
as a result of this, vanishes in its turn, as did the venous ring
before it. There is then present a single arterial and a single venous
trunk. The arterial trunk is a branch of the dorsal aorta, and the
venous trunk originally falls into the heart together with the
subintestinal or splanchnic vein. On the formation of the liver the
proximal end of the subintestinal vein becomes the portal vein, and it
is joined just as it enters the liver by the venous trunk from the
yolk-sack. The venous trunk leaves the body on the right side, and the
arterial on the left.
The yolk-sack persists during the whole of embryonic life, and in the
majority of Elasmobranch embryos there arises within the body walls an
outgrowth from the umbilical canal into which a large amount of the
yolk passes. This outgrowth forms an internal yolk-sack. In Mustelus
vulgaris the internal yolk-sack is very small, and in Mustelus lævis
it is absent. The latter species, which is one of those in which
development takes place within the uterus, presents a remarkable
peculiarity in that the vascular surface of the yolk-sack becomes
raised into a number of folds, which fit into corresponding
depressions in the vascular walls of the uterus. The yolk-sack becomes
in this way firmly attached to the walls of the uterus, and the two
together constitute a kind of placenta. A similar placenta is found in
Carcharias.
After the embryo is hatched or born, as the case may be, the yolk-sack
becomes rapidly absorbed.
BIBLIOGRAPHY.
(40) F. M. Balfour. "A preliminary account of the development of the
Elasmobranch Fishes." _Quart. J. of Micr. Science_, Vol. XIV. 1876.
(41) F. M. Balfour. "A Monograph on the development of Elasmobranch
Fishes." London, 1878. Reprinted from the _Journal of Anat. and
Physiol._ for 1876, 1877, and 1878.
(42) Z. Gerbe. "_Recherches sur la segmentation de la cicatrule et la
formation des produits adventifs de l'oeuf des Plagiostomes et
particulièrement des Raies._" Vide also _Journal de l'Anatomie et de
la Physiologie_, 1872.
(43) W. His. "Ueb. d. Bildung v. Haifischenembryonen." _Zeit. für
Anat. u. Entwick._, Vol. II. 1877.
(44) A. Kowalevsky. "Development of Acanthias vulgaris and Mustelus
lævis." (_Russian._) _Transactions of the Kiew Society of
Naturalists_, Vol. I. 1870.
(45) R. Leuckart. "Ueber die allmählige Bildung d. Körpergestalt bei
d. Rochen." _Zeit. f. wiss. Zool._, Bd. II., p. 258.
(46) Fr. Leydig. _Rochen u. Haie._ Leipzig, 1852.
(47) A. W. Malm. "Bidrag till kännedom om utvecklingen af Rajæ."
_Kongl. vetenskaps akademiens förhandlingar._ Stockholm, 1876.
(48) Joh. Müller. _Glatter Haie des Aristoteles und über die
Verschiedenheiten unter den Haifischen und Rochen in der Entwicklung
des Eies._ Berlin, 1840.
(49) S. L. Schenk. "Die Eier von Raja quadrimaculata innerhalb der
Eileiter." _Sitz. der k. Akad. Wien_, Vol. LXXIII. 1873.
(50) Alex. Schultz. "Zur Entwicklungsgeschichte des Selachiereies."
_Archiv für micro. Anat._, Vol. XI. 1875.
(51) Alex. Schultz. "Beitrag zur Entwicklungsgeschichte d.
Knorpelfische." _Archiv für micro. Anat._, Vol. XIII. 1877.
(52) C. Semper. "Die Stammesverwandschaft d. Wirbelthiere u.
Wirbellosen." _Arbeit. a. d. zool.-zoot. Instit. Würzburg_, Vol. II.
1875.
(53) C. Semper. "Das Urogenitalsystem d. Plagiostomen, etc." _Arbeit.
a. d. zool.-zoot. Instit. Würzburg_, Vol. II. 1875.
(54) Wyman. "Observations on the Development of Raja batis." _Memoirs
of the American Academy of Arts and Sciences_, Vol. IX. 1864.
CHAPTER IV.
TELEOSTEI.
The majority of the Teleostei deposit their eggs before impregnation,
but some forms are viviparous, _e.g._ Blennius viviparus. Not a few
carry their eggs about; but this operation is with a few exceptions
performed by the male. In Syngnathus the eggs are carried in a
brood-pouch of the male situated behind the anus. Amongst the
Siluroids the male sometimes carries the eggs in the throat above the
gill clefts. Ostegeniosus militaris, Arius falcarius, and Arius fissus
have this peculiar habit.
The ovum when laid is usually invested in the zona radiata only,
though a vitelline membrane is sometimes present in addition, _e.g._
in the Herring. It is in most cases formed of a central yolk mass,
which may either be composed of a single large vitelline sphere, or of
distinct yolk spherules. The yolk mass is usually invested by a
granular protoplasmic layer, which is especially thickened at one pole
to form the germinal disc.
In the Herring's ovum the germinal disc is formed, as in many
Crustacea, at impregnation; the protoplasm which was previously
diffused through the egg becoming aggregated at the germinal pole and
round the periphery.
Impregnation is external, and on its occurrence a contraction of the
vitellus takes place, so that a space is formed between the vitellus
and the zona radiata, which becomes filled with fluid.
The peculiarities in the development of the Teleostean ovum can best
be understood by regarding it as an Elasmobranch ovum very much
reduced in size. It seems in fact very probable that the Teleostei are
in reality derived from a type of Fish with a much larger ovum. The
occurrence of a meroblastic segmentation, in spite of the ovum being
usually smaller than that of Amphibia and Acipenser, etc., in which
the segmentation is complete, as well as the solid origin of many of
the organs, receives its most plausible explanation on this
hypothesis.
The proportion of the germinal disc to the whole ovum varies
considerably. In very small eggs, such as those of the Herring, the
disc may form as much as a fifth of the whole.
The segmentation, which is preceded by active movements of the
germinal disc, is meroblastic. There is nothing very special to note
with reference to its general features, but while in large ova like
those of the Salmon the first furrows only penetrate for a certain
depth through the germinal disc, in small ova like those of the
Herring they extend through the whole thickness of the disc. During
the segmentation a great increase in the bulk of the blastoderm takes
place.
In hardened specimens a small cavity amongst the segmentation spheres
may be present at any early stage; but it is probably an artificial
product, and in any case has nothing to do with the true segmentation
cavity, which does not appear till near the close of segmentation. The
peripheral layer of granular matter, continuous with the germinal
disc, does not undergo division, but it becomes during the
segmentation specially thickened and then spreads itself under the
edge of the blastoderm; and, while remaining thicker in this region,
gradually grows inwards so as to form a continuous sub-blastodermic
layer. In this layer nuclei appear, which are equivalent to those in
the Elasmobranch ovum. A considerable number of these nuclei often
become visible simultaneously (van Beneden, No. 60) and they are
usually believed to arise spontaneously, though this is still
doubtful[20]. Around these nuclei portions of protoplasm are segmented
off, and cells are thus formed, which enter the blastoderm, and have
nearly the same destination as the homologous cells of the
Elasmobranch ovum.
[20] _Vide_ Vol. II. p. 108.
During the later stages of segmentation one end of the blastoderm
becomes thickened and forms the embryonic swelling; and a cavity
appears between the blastoderm and the yolk which is excentrically
situated near the non-embryonic part of the blastoderm. This cavity is
the true segmentation cavity. Both the cavity and the embryonic
swelling are seen in section in fig. 31 A and B.
In Leuciscus rutilus Bambeke describes a cavity as appearing in the
middle of the blastoderm during the later stages of segmentation. From
his figures it might be supposed that this cavity was equivalent to
the segmentation cavity of Elasmobranchs in its earliest condition,
but Bambeke states that it disappears and that it has no connection
with the true segmentation cavity. Bambeke and other investigators
have failed to recognize the homology of the segmentation cavity in
Teleostei with that in Elasmobranchii, Amphibia, etc.
With the appearance of the segmentation cavity the portion of the
blastoderm which forms its roof becomes thinned out, so that the whole
blastoderm consists of (1) a thickened edge especially prominent at
one point where it forms the embryonic swelling, and (2) a thinner
central portion. The changes which now take place result in the
differentiation of the embryonic layers, and in the rapid extension of
the blastoderm round the yolk, accompanied by a diminution in its
thickness.
[FIG. 31. LONGITUDINAL SECTIONS THROUGH THE BLASTODERM OF THE TROUT
AT AN EARLY STAGE OF DEVELOPMENT.
A. at the close of the segmentation; B. after the differentiation of
the germinal layers.
_ep´._ epidermic layer of the epiblast; _sc._ segmentation cavity.]
The first differentiation of the layers consists in a single row of
cells on the surface of the blastoderm becoming distinctly marked off
as a special layer (fig. 31 A); which however does not constitute the
whole epiblast but only a small part of it, which will be spoken of as
the epidermic layer. The complete differentiation of the epiblast is
effected by the cells of the thickened edge of the blastoderm becoming
divided into two strata (fig. 31 B). The upper stratum constitutes the
epiblast. It is divided into two layers, viz., the external epidermic
layer already mentioned, and an internal layer known as the nervous
layer, formed of several rows of vertically arranged cells. According
to the unanimous testimony of investigators the roof of the
segmentation cavity is formed of epiblast cells only. The lower
stratum in the thickened rim of the blastoderm is several rows of
cells deep, and corresponds with the lower layer cells or primitive
hypoblast in Elasmobranchii. It is continuous at the edge of the
blastoderm with the nervous layer of the epiblast.
In smaller Teleostean eggs there is formed, before the blastoderm
becomes differentiated into epiblast and lower layer cells, a complete
stratum of cells around the nuclei in the granular layer underneath
the blastoderm. This layer is the hypoblast; and in these forms the
lower layer cells of the blastoderm are stated to become converted
into mesoblast only. In the larger Teleostean eggs, such as those of
the Salmonidæ, the hypoblast, as in Elasmobranchs, appears to be only
partially formed from the nuclei of the granular layer. In these forms
however, as in the smaller Teleostean ova and in Elasmobranchii, the
cells derived from the granular stratum give rise to a more or less
complete cellular floor for the segmentation cavity. The segmentation
cavity thus becomes enclosed between an hypoblastic floor and an
epiblastic roof several cells deep. It becomes obliterated shortly
after the appearance of the medullary plate.
At about the time when the three layers become established the
embryonic swelling takes a somewhat shield-like form (fig. 33 A).
Posteriorly it terminates in a caudal prominence (_ts_) homologous
with the pair of caudal swellings in Elasmobranchs. The homologue of
the medullary groove very soon appears as a shallow groove along the
axial line of the shield. After these changes there takes place in the
embryonic layers a series of differentiations leading to the
establishment of the definite organs. These changes are much more
difficult to follow in the Teleostei than in the Elasmobranchii, owing
partly to the similarity of the cells of the various layers, and
partly to the primitive solidity of all the organs.
The first changes in the epiblast give rise to the central nervous
system. The epiblast, consisting of the nervous and epidermic strata
already indicated, becomes thickened along the axis of the embryo and
forms a keel projecting towards the yolk below: so great is the size
of this keel in the front part of the embryo that it influences the
form of the whole body and causes the outline of the surface adjoining
the yolk to form a strong ridge moulded on the keel of the epiblast
(fig. 32 A and B). Along the dorsal line of the epiblast keel is
placed the shallow medullary groove; and according to Calberla (No.
61) the keel is formed by the folding together of the two sides of the
primitively uniform epiblastic layer. The keel becomes gradually
constricted off from the external epiblast and then forms a _solid
cord_ below it. Subsequently there appears in this cord a median
slit-like canal, which forms the permanent central canal of the
cerebrospinal cord. The peculiarity in the formation of the central
nervous system of Teleostei consists in the fact that it is not formed
by the folding over of the sides of the medullary groove into a canal,
but by the separation, below the medullary groove, of a solid cord of
epiblast in which the central canal is subsequently formed. Various
views have been put forward to explain the apparently startling
difference between Teleostei, with which Lepidosteus and Petromyzon
agree, and other vertebrate forms. The explanations of Götte and
Calberla appear to me to contain between them the truth in this
matter. The groove above in part represents the medullary groove; but
the closure of the groove is represented by the folding together of
the lateral parts of the epiblast plate to form the medullary keel.
According to Götte this is the whole explanation, but Calberla states
for Syngnathus and Salmo that the epidermic layer of the epiblast is
carried down into the keel as a double layer just as if it had been
really folded in. This ingrowth of the epidermic layer is shewn in
fig. 32 A where it is just commencing to pass into the keel; and at a
later stage in fig. 32 B where the keel has reached its greatest
depth.
Götte maintains that Calberla's statements are not to be trusted, and
I have myself been unable to confirm them for Teleostei or
Lepidosteus; but if they could be accepted the difference in the
formation of the medullary canal in Teleostei and in other Vertebrata
would become altogether unimportant and consist simply in the fact
that the ordinary open medullary groove is in Teleostei obliterated in
its inner part by the two sides of the groove coming together. Both
layers of epiblast would thus have a share in the formation of the
central nervous system; the epidermic layer giving rise to the lining
epithelial cells of the central canal, and the nervous layer to the
true nervous tissue.
The separation of the solid nervous system from the epiblast takes
place relatively very late; and, before it has been completed, the
first traces of the auditory pits, of the optic vesicles, and of the
olfactory pits are visible. The auditory pit arises as a solid
thickening of the nervous layer of the epiblast at its point of
junction with the medullary keel; and the optic vesicles spring as
solid outgrowths from part of the keel itself. The olfactory pits are
barely indicated as thickenings of the nervous layer of the epiblast.
[FIG. 32. TWO TRANSVERSE SECTIONS OF SYNGNATHUS. (After Calberla.)
A. Younger stage before the definite establishment of the notochord.
B. Older stage.
The epidermic layer of the epiblast is represented in black.
_ep._ epidermic layer of epiblast; _mc._ neural cord; _hy._
hypoblast; _me._ mesoblast; _ch._ notochord.]
At this early stage all the organs of special sense are attached to a
layer continuous with or forming part of the central nervous system;
and this fact has led Götte (No. 63) to speak of a special-sense
plate, belonging to the central nervous system and not to the skin,
from which all the organs of special sense are developed; and to
conclude that a serial homology exists between these organs in their
development. A comparison between Teleostei and other forms shews that
this view cannot be upheld; even in Teleostei the auditory and
olfactory rudiments arise rather from the epiblast at the sides of the
brain than from the brain itself, while the optic vesicles spring from
the first directly from the medullary keel, and are therefore
connected with the central nervous system rather than with the
external epiblast. In a slightly later stage the different connections
of the two sets of sense organs is conclusively shewn by the fact
that, on the separation of the central nervous system from the
epiblast, the optic vesicles remain attached to the former, while the
auditory and olfactory vesicles are continuous with the latter.
After its separation from the central nervous system the remainder of
the epiblast gives rise to the skin, etc., and most probably the
epidermic stratum develops into the outer layer of the epidermis and
the nervous stratum into the mucous layer. The parts of the organs of
special sense, which arise from the epiblast, are developed from the
nervous layer. In the Trout (Oellacher, No. 72) both layers are
continued over the yolk-sack; but in Clupeus and Gasterosteus only the
epidermic has this extension. According to Götte the distinction
between the two layers becomes lost in the later embryonic stages.
Although it is thoroughly established that the mesoblast originates
from the lower of the two layers of the thickened embryonic rim, it is
nevertheless not quite certain whether it is a continuous layer
between the epiblast and hypoblast, or whether it forms two lateral
masses as in Elasmobranchs. The majority of observers take the former
view, while Calberla is inclined to adopt the latter. In the median
line of the embryo underneath the medullary groove there are
undoubtedly from the first certain cells which eventually give rise to
the notochord; and it is these cells the nature of which is in doubt.
They are certainly at first very indistinctly separated from the
mesoblast on the two sides, and Calberla also finds that there is no
sharp line separating them from the secondary hypoblast (fig. 32 A).
Whatever may be the origin of the notochord the mesoblast very soon
forms two lateral plates, one on each side of the body, and between
them is placed the notochord (fig. 32 B). The general fate of the two
mesoblast plates is the same as in Elasmobranchs. They are at first
quite solid and exhibit relatively late a division into splanchnic and
somatic layers, between which is placed the primitive body cavity. The
dorsal part of the plates becomes transversely segmented in the region
of the trunk; and thus gives rise to the mesoblastic somites, from
which the muscle plates and the perichordal parts of the vertebral
column are developed. The ventral or outer part remains unsegmented.
The cavity of the ventral section becomes the permanent body cavity.
It is continued forward into the head (Oellacher), and part of it
becomes separated off from the remainder as the pericardial cavity.
The hypoblast forms a continuous layer below the mesoblast, and, in
harmony with the generally confined character of the development of
the organs in Teleostei, there is no space left between it and the
yolk to represent the primitive alimentary cavity. The details of the
formation of the true alimentary tube have not been made out; it is
not however formed by a folding in of the lateral parts of the
hypoblast, but arises as a solid or nearly solid cord in the axial
line, between the notochord and the yolk, in which a lumen is
gradually established.
In the just hatched larva of an undetermined freshwater fish with a
very small yolk-sack I found that the yolk extended along the ventral
side of the embryo from almost the mouth to the end of the gut. The
gut had, except in the hinder part, the form of a solid cord resting
in a concavity of the yolk. In the hinder part of the gut a lumen was
present, and below this part the amount of yolk was small and the yolk
nuclei numerous. Near the limit of its posterior extension the yolk
broke up into a mass of cells, and the gut ended behind by falling
into this mass. These incomplete observations appear to shew that the
solid gut owes its origin in a large measure to nuclei derived from
the yolk.
When the yolk has become completely enveloped a postanal section of
gut undoubtedly becomes formed; and although, owing to the solid
condition of the central nervous system, a communication between the
neural and alimentary canals cannot at first take place, yet the
terminal vesicle of the postanal gut of Elasmobranchii is represented
by a large vesicle, originally discovered by Kupffer (No. 68), which
can easily be seen in the embryos of most Teleostei, but the relations
of which have not been satisfactorily worked out (_vide_ fig. 34,
_hyv_). As the tail end of the embryo becomes separated off from the
yolk the postanal vesicle atrophies.
General development of the Embryo. Attention has already been called
to the fact that the embryo first appears as a thickening of the edge
of the blastoderm which soon assumes a somewhat shield-like form (fig.
33 A). The hinder end of the embryo, which is placed at the edge of
the blastoderm, is somewhat prominent, and forms the caudal swelling
(_ts_). The axis of the embryo is marked by a shallow groove.
[FIG. 33. THREE STAGES IN THE DEVELOPMENT OF THE SALMON. (After
His.)
_ts._ tail swelling; _au.v._ auditory vesicle; _oc._ optic vesicle;
_ce._ cerebral rudiment; _m.b._ mid-brain; _cb._ cerebellum; _md._
medulla oblongata; _m.so._ mesoblastic somite.]
The body now rapidly elongates, and at the same time becomes
considerably narrower, while the groove along the axis becomes
shallower and disappears. The anterior, and at first proportionately a
very large part, soon becomes distinguished as the cephalic region
(fig. 33 B). The medullary cord in this region becomes very early
divided into three indistinctly separated lobes, representing the
fore, the mid, and the hind brains: of these the anterior is the
smallest. With it are connected the optic vesicles (_oc_)--solid at
first--which are pushed back into the region of the mid-brain.
The trunk grows in the usual way by the addition of fresh somites
behind.
After the yolk has become completely enveloped by the blastoderm the
tail becomes folded off, and the same process takes place at the front
end of the embryo. The free tail end of the embryo continues to grow,
remaining however closely applied to the yolk-sack, round which it
curls itself to an extent varying with the species (_vide_ fig. 34).
The general growth of the embryo during the later stages presents a
few special features of interest. The head is remarkable for the small
apparent amount of the cranial flexure. This is probably due to the
late development of the cerebral hemispheres. The flexure of the floor
of the brain is however quite as considerable in the Teleostei as in
other types. The gill clefts develop from before backwards. The first
cleft is the hyomandibular, and behind this there are the hyobranchial
and four branchial clefts. Simultaneously with the clefts there are
developed the branchial arches. The postoral arches formed are the
mandibular, hyoid and five branchial arches. In the case of the Salmon
all of these appear before hatching.
[FIG. 34. VIEW OF AN ADVANCED EMBRYO OF A HERRING IN THE EGG. (After
Kupffer.)
_oc._ eye; _ht._ heart; _hyv._ postanal vesicle; _ch._ notochord.]
The first cleft closes up very early (about the time of hatching in
the Salmon); and about the same time there springs a membranous fold
from the hyoid arch, which gradually grows backwards over the arches
following, and gives rise to the operculum. There appear in the Salmon
shortly before hatching double rows of papillæ on the four anterior
arches behind the hyoid. They are the rudiments of the branchiæ. They
reach a considerable length before they are covered in by the
opercular membrane. In Cobitis (Götte, No. 64) they appear in young
larvæ as filiform processes equivalent to the external gills of
Elasmobranchs. The extremities of these processes atrophy; while the
basal portions became the permanent gill lamellæ. The general relation
of the clefts, after the closure of the hyomandibular, is shewn in
fig. 35.
The air-bladder is formed as a dorsal outgrowth of the alimentary
tract very slightly in front of the liver. It grows in between the two
limbs of the mesentery, in which it extends itself backwards. It
appears in the Salmon, Carp, and other types to originate rather on
the right side of the median dorsal line, but whether this fact has
any special significance is rather doubtful. In the Salmon and Trout
it is formed considerably later than the liver, but the two are stated
by Von Baer to arise in the Carp nearly at the same time. The absence
of a pneumatic duct in the Physoclisti is due to a post-larval
atrophy. The region of the stomach is reduced almost to nothing in the
larva.
The oesophagus becomes solid, like that of Elasmobranchs, and remains
so for a considerable period after hatching.
The liver, in the earliest stage in which I have met with it in the
Trout (27 days after impregnation), is a solid ventral diverticulum of
the intestine, which in the region of the liver is itself without a
lumen.
[FIG. 35. DIAGRAMMATIC VIEW OF THE HEAD OF AN EMBRYO TELEOSTEAN,
WITH THE PRIMITIVE VASCULAR TRUNKS. (From Gegenbaur.)
_a._ auricle; _v._ ventricle; _abr._ branchial artery; _c´._
carotid; _ad._ aorta; _s._ branchial clefts; _sv._ sinus venosus;
_dc._ ductus Cuvieri; _n._ nasal pit.]
The excretory system commences with the formation of a segmental duct,
formed by a constriction of the parietal wall of the peritoneal
cavity. The anterior end remains open to the body cavity, and forms a
pronephros (head kidney). On the inner side of and opposite this
opening a glomerulus is developed, and the part of the body cavity
containing both the glomerulus and the opening of the pronephros
becomes shut off from the remainder of the body cavity, and forms a
completely closed Malpighian capsule.
The mesonephros (Wolffian body) is late in developing.
The unpaired fins arise as simple folds of the skin along the dorsal
and ventral edges, continuous with each other round the end of the
tail. The ventral fold ends anteriorly at the anus.
The dorsal and anal fins are developed from this fold by local
hypertrophy. The caudal fin[21], however, undergoes a more complicated
metamorphosis. It is at first symmetrical or nearly so on the dorsal
and ventral sides of the hinder end of the notochord. This symmetry is
not long retained, but very soon the ventral part of the fin with its
fin rays becomes much more developed than the dorsal part, and at the
same time the posterior part of the notochord bends up towards the
dorsal side.
[21] In addition to the paper by Alex. Agassiz (No. 55) _vide_
papers by Huxley, Kölliker, Vogt, etc.
In some few cases, _e.g._ Gadus, Salmo, owing to the simultaneous
appearance of a number of fin rays on the dorsal and ventral side of
the notochord the external symmetry of the tail is not interfered with
in the above processes. In most instances this is far from being the
case.
[FIG. 36. THREE STAGES IN THE DEVELOPMENT OF THE TAIL OF THE
FLOUNDER (PLEURONECTES). (After Agassiz.)
A. Stage in which the permanent caudal fin has commenced to be
visible as an enlargement of the ventral side of the embryonic
caudal fin.
B. Ganoid-like stage in which there is a true external heterocercal
tail.
C. Stage in which the embryonic caudal fin has almost completely
atrophied.
_c._ embryonic caudal fin; _f._ permanent caudal fin; _n._
notochord; _u._ urostyle.]
In the Flounder, which may serve as a type, the primitive symmetry is
very soon destroyed by the appearance of fin rays on the ventral side.
The region where they are present soon forms a lobe; and an externally
heterocercal tail is produced (fig. 36 A). The ventral lobe with its
rays continues to grow more prominent and causes the tail fin to
become bilobed (fig. 36 B); there being a dorsal embryonic lobe
without fin rays (_c_), which contains the notochord, and a ventral
lobe with fin rays, which will form the permanent caudal fin. In this
condition the tail fin resembles the usual Elasmobranch form or still
more that of some Ganoids, _e.g._ the Sturgeon. The ventral lobe
continues to develop; and soon projects beyond the dorsal, which
gradually atrophies together with the notochord contained in it, and
finally disappears, leaving hardly a trace on the dorsal side of the
tail (fig. 36 C, _c_). In the meantime the fin rays of the ventral
lobe gradually become parallel to the axis of the body; and this lobe,
together with a few accessory dorsal and ventral fin rays supported by
neural and hæmal processes, forms the permanent tail fin, which though
internally unsymmetrical, assumes an externally symmetrical form. The
upturned end of the notochord which was originally continued into the
primitive dorsal lobe becomes ensheathed in a bone without a division
into separate vertebræ. This bone forms the urostyle (_u_). The hæmal
processes belonging to it are represented by two cartilaginous masses,
which subsequently ossify, forming the hypural bones, and supporting
the primary fin rays of the tail (fig. 36 C). The ultimate changes of
the notochord and urostyle vary very considerably in the different
types of Teleostei. Teleostei may fairly be described as passing
through an Elasmobranch stage or a stage like that of most
pre-jurassic Ganoids or the Sturgeon as far as concerns their caudal
fin.
The anterior paired fins arise before the posterior; and there do not
appear to be any such indications as in Elasmobranchii of the paired
fins arising as parts of a continuous lateral fin.
Most osseous fishes pass through more or less considerable
post-embryonic changes, the most remarkable of which are those
undergone by the Pleuronectidæ[22]. These fishes, which in the adult
state have the eyes unsymmetrically placed on one side of the head,
leave the egg like normal Teleostei. In the majority of cases as they
become older the eye on the side, which in the adult is without an
eye, travels a little forward and then gradually rotates over the
dorsal side of the head, till finally it comes to lie on the same side
as the other eye. During this process the rotating eye always remains
at the surface and continues functional; and on the two eyes coming to
the same side of the head the side of the body without an organ of
vision loses its pigment cells, and becomes colourless.
[22] _Vide_ Agassiz (No. 56) and Steenstrup, Malm.
The dorsal fin, after the rotation of the eye, grows forward beyond
the level of the eyes. In the genus Plagusia (Steenstrup, Agassiz, No.
56) the dorsal fin grows forward before the rotation of the eye (the
right eye in this form), and causes some modifications in the process.
The eye in travelling round gradually sinks into the tissues of the
head, at the base of the fin above the frontal bone; and in this
process the original large opening of the orbit becomes much reduced.
Soon a fresh opening on the opposite and left side of the dorsal fin
is formed; so that the orbit has two external openings, one on the
left and one on the right side. The original one on the right soon
atrophies, and the eye passes through the tissues at the base of the
dorsal fin completely to the left side.
The rotating eye may be either the right or the left according to the
species.
The most remarkable feature in which the young of a large number of
Teleostei differ from the adults is the possession of provisional
spines, very often formed as osseous spinous projections the spaces
between which become filled up in the adult. These processes are
probably, as suggested by Günther, secondary developments acquired,
like the Zooea spines of larval Crustaceans, for purposes of defence.
The yolk-sack varies greatly in size in the different types of
Teleostei.
According as it is enclosed within the body-wall, or forms a distinct
ventral appendage, it is spoken of by Von Baer as an internal or
external yolk-sack. By Von Baer the yolk-sack is stated to remain in
communication with the intestine immediately behind the liver, while
Lereboullet states that there is a vitelline pedicle opening between
the stomach and the liver which persists till the absorption of the
yolk-sack. My own observations do not fully confirm either of these
statements for the Salmon and Trout. So far as I have been able to
make out, all communication between the yolk-sack and the alimentary
tract is completely obliterated very early. In the Trout the
communication between the two is shut off before hatching, and in the
just-hatched Salmon I can find no trace of any vitelline pedicle. The
absorption of the yolk would seem therefore to be effected entirely by
blood-vessels.
The yolk-sack persists long after hatching, and is gradually absorbed.
There is during the stages either just before hatching or shortly
subsequent to hatching (Cyprinus) a rich vascular development in the
mesoblast of the yolk-sack. The blood is at first contained in lacunar
spaces, but subsequently it becomes confined to definite channels. As
to its exact relations to the vascular system of the embryo more
observations seem to be required.
The following account is given by Rathke (No. 72*) and Lereboullet
(No. 71). At first a subintestinal vein (_vide_ chapter on
Circulation) falls into the lacunæ of the yolk-sack, and the blood
from these is brought back direct to the heart. At a later period,
when the liver is developed, the subintestinal vessel breaks up into
capillaries in the liver, thence passes into the yolk-sack, and from
this to the heart. An artery arising from the aorta penetrates the
liver, and there breaks up into capillaries continuous with those of
the yolk-sack. This vessel is perhaps the equivalent of the artery
which supplies the yolk-sack in Elasmobranchii, but it seems possible
that there is some error in the above description.
BIBLIOGRAPHY.
(55) Al. Agassiz. "On the young Stages of some Osseous Fishes. I.
Development of the Tail." _Proceedings of the American Academy of Arts
and Sciences_, Vol. XIII. Presented Oct. 11, 1877.
(56) Al. Agassiz. "II. Development of the Flounders." _Proceedings of
the American Acad. of Arts and Sciences_, Vol. XIV. Presented June,
1878.
(57) K. E. v. Baer. _Untersuchungen über die Entwicklungsgeschichte
der Fische._ Leipzig, 1835.
(58) Ch. van Bambeke. "Premiers effets de la fécondation sur les oeufs
de Poissons: sur l'origine et la signification du feuillet muqueux ou
glandulaire chez les Poissons Osseux." _Comptes Rendus des Séances de
l'Académie des Sciences_, Tome LXXIV. 1872.
(59) Ch. van Bambeke. "Recherches sur l'Embryologie des Poissons
Osseux." _Mém. couronnés et Mém. de savants étrangers de l'Académie
roy. Belgique_, Vol. XL. 1875.
(60) E. v. Beneden. "A contribution to the history of the Embryonic
development of the Teleosteans." _Quart. J. of Micr. Sci._, Vol.
XVIII. 1878.
(61) E. Calberla. "Zur Entwicklung des Medullarrohres u. d. Chorda
dorsalis d. Teleostier u. d. Petromyzonten." _Morphologisches
Jahrbuch_, Vol. III. 1877.
(62) A. Götte. "Beiträge zur Entwicklungsgeschichte der Wirbelthiere."
_Archiv f. mikr. Anat._, Vol. IX. 1873.
(63) A. Götte. "Ueber d. Entwicklung d. Central-Nervensystems der
Teleostier." _Archiv f. mikr. Anat._, Vol. XV. 1878.
(64) A. Götte. "Entwick. d. Teleostierkeime." _Zoologischer Anzeiger_,
No. 3. 1878.
(65) W. His. "Untersuchungen über die Entwicklung von Knochenfischen,
etc." _Zeit. f. Anat. u. Entwicklungsgeschichte_, Vol. I. 1876.
(66) W. His. "Untersuchungen über die Bildung des Knochenfischembryo
(Salmen)." _Archiv f. Anat. u. Physiol._, 1878.
(67) E. Klein. "Observations on the early Development of the Common
Trout." _Quart. J. of Micr. Science_, Vol. XVI. 1876.
(68) C. Kupffer. "Beobachtungen über die Entwicklung der
Knochenfische." _Archiv f. mikr. Anat._, Bd. IV. 1868.
(69) C. Kupffer. _Ueber Laichen u. Entwicklung des Ostsee-Herings._
Berlin, 1878.
(70) M. Lereboullet. "Recherches sur le développement du brochet de la
perche et de l'écrevisse." _Annales des Sciences Nat._, Vol. I.,
Series IV. 1854.
(71) M. Lereboullet. "Recherches d'Embryologie comparée sur le
développement de la Truite." _An. Sci. Nat._, quatrième série, Vol.
XVI. 1861.
(72) T. Oellacher. "Beiträge zur Entwicklungsgeschichte der
Knochenfische nach Beobachtungen am Bachforellenei." _Zeit. f. wiss.
Zool._, Vol. XXII., 1872, and Vol. XXIII., 1873.
(72*) H. Rathke. _Abh. z. Bildung u. Entwick. d. Menschen u. Thiere._
Leipzig, 1832-3. Part II. Blennius.
(73) Reineck. "Ueber die Schichtung des Forellenkeims." _Archiv f.
mikr. Anat._, Bd. V. 1869.
(74) S. Stricker. "Untersuchungen über die Entwicklung der
Bachforelle." _Sitzungsberichte der Wiener k. Akad. d. Wiss._, 1865.
Vol. LI. Abth. 2.
(75) Carl Vogt. "Embryologie des Salmones." _Histoire Naturelle des
Poissons de l'Europe Centrale._ L. Agassiz. 1842.
(76) C. Weil. "Beiträge zur Kenntniss der Knochenfische."
_Sitzungsber. der Wiener kais. Akad. der Wiss._, Bd. LXVI. 1872.
CHAPTER V.
CYCLOSTOMATA[23].
[23] The following classification of the Cyclostomata is employed
in the present chapter:
I. Hyperoartia ex. Petromyzon.
II. Hyperotreta ex. Myxine, Bdellostoma.
Petromyzon is the only type of this degenerated but primitive group of
Fishes the development of which has been as yet studied[24].
[24] The present chapter is in the main founded upon observations
which I was able to make in the spring of 1880 upon the
development of Petromyzon Planeri. Mr Scott very kindly looked
over my proof-sheets and made a number of valuable suggestions,
and also sent me an early copy of his preliminary note (No. 87),
which I have been able to make use of in correcting my
proof-sheets.
The development does not however throw any light on the relationships
of the group. The similarity of the mouth and other parts of
Petromyzon to those of the Tadpole probably indicates that there
existed a common ancestral form for the Cyclostomata and Amphibia.
Embryology does not however add anything to the anatomical evidence on
this subject. The fact of the segmentation being complete was at one
time supposed to indicate an affinity between the two groups; but the
discovery that the segmentation is also complete in the Ganoids
deprives this feature in the development of any special weight. In the
formation of the layers and in most other developmental characters
there is nothing to imply a special relationship with the Amphibia,
and in the mode of formation of the nervous system Petromyzon exhibits
a peculiar modification, otherwise only known to occur in Teleostei
and Lepidosteus.
Dohrn[25] was the first to bring into prominence the degenerate
character of the Cyclostomata. I cannot however assent to his view
that they are descended from a relatively highly-organized type of
Fish. It appears to me almost certain that they belong to a group of
fishes in which a true skeleton of branchial bars had not become
developed, the branchial skeleton they possess being simply an
extra-branchial system; while I see no reason to suppose that a true
branchial skeleton has disappeared. If the primitive Cyclostomata had
not true branchial bars, they could not have had jaws, because jaws
are essentially developed from the mandibular branchial bar. These
considerations, which are supported by numerous other features of
their anatomy, such as the character of the axial skeleton, the
straightness of the intestinal tube, the presence of a subintestinal
vein etc., all tend to prove that these fishes are remnants of a
primitive and prægnathostomatous group. The few surviving members of
the group have probably owed their preservation to their parasitic or
semiparasitic habits, while the group as a whole probably disappeared
on the appearance of gnathostomatous Vertebrata.
[25] _Der Ursprung d. Wirbelthiere_, etc. Leipzig, 1875.
The ripe ovum of Petromyzon Planeri is a slightly oval body of about 1
mm. in diameter. It is mainly formed of an opaque nearly white yolk,
invested by a membrane composed of an inner perforated layer, and an
outer structureless layer. There appears to be a pore perforating the
inner layer at the formative pole, which may be called a micropyle
(Kupffer and Benecke, No. 79). Enclosing the egg-membranes there is
present a mucous envelope, which causes the egg, when laid, to adhere
to stones or other objects.
[FIG. 37. LONGITUDINAL VERTICAL SECTION THROUGH AN EMBRYO OF
PETROMYZON PLANERI OF 136 HOURS.
_me._ mesoblast; _yk._ yolk-cells; _al._ alimentary tract; _bl._
blastopore; _s.c._ segmentation cavity.]
Impregnation is effected by the male attaching itself by its suctorial
mouth to the female. The attached couple then shake together; and, as
they do so, they respectively emit from their abdominal pores ova and
spermatozoa which pass into a hole previously made[26].
[26] Artificial impregnation may be effected without difficulty
by squeezing out into the same vessel the ova and spermatozoa of
a ripe female and male. The fertilized eggs are easily reared.
Petromyzon Planeri breeds during the second half of April.
The segmentation is total and unequal, and closely resembles that in
the Frog's egg (Vol. II. p. 96). The upper pole is very slightly
whiter than the lower. A segmentation cavity is formed very early, and
is placed between the small cells of the upper pole and the large
cells of the lower pole. It is proportionately larger than in the
Frog; and the roof eventually thins out so as to be formed of a single
row of small cells. At the sides of the segmentation cavity there are
always several rows of small cells, which gradually merge into the
larger cells of the lower pole of the egg. The segmentation is
completed in about fifty hours.
[FIG. 38. TRANSVERSE SECTION THROUGH A PETROMYZON EMBRYO 160 HOURS
AFTER IMPREGNATION.
_ep._ epiblast; _al._ mesenteron; _yk._ yolk-cells; _ms._
mesoblast.]
The segmentation is followed by an asymmetrical invagination (fig. 37)
which leads to a mode of formation of the hypoblast fundamentally
similar to that in the Frog. The process has been in the main
correctly described by M. Schultze (No. 81).
On the border between the large and small cells of the embryo, at a
point slightly below the segmentation cavity, a small circular pit
appears; the roof of which is formed by an infolding of the small
cells, while the floor is formed of the large cells. This pit is the
commencing mesenteron. It soon grows deeper (fig. 37, _al_) and
extends as a well-defined tube (shewn in transverse section in fig.
38, _al_) in the direction of the segmentation cavity. In the course
of the formation of the mesenteron the segmentation cavity gradually
becomes smaller, and is finally (about the 200th hour) obliterated.
The roof of the mesenteron is formed by the continued invagination of
small cells, and its floor is composed of large yolk-cells. The wide
external opening is arched over dorsally by a somewhat prominent
lip--the homologue of the embryonic rim. The opening persists till
nearly the time of hatching; but eventually becomes closed, and is not
converted into the permanent anus. On the formation of the mesenteron
the hypoblast is composed of two groups of cells, (1) the yolk-cells,
and (2) the cells forming the roof of the mesenteron.
While the above changes are taking place, the small cells, or as they
may now be called the epiblast cells, gradually spread over the large
yolk-cells, as in normal types of epibolic invagination. The growth
over the yolk-cells is not symmetrical, but is most rapid in the
meridian opposite the opening of the alimentary cavity, so that the
latter is left in a bay (cf. Elasmobranchii, p. 63). The epibolic
invagination takes place as in Molluscs and many other forms, not
simply by the division of pre-existing epiblast cells, but by the
formation of fresh epiblast cells from the yolk-cells (fig. 37); and
till after the complete enclosure of the yolk-cells there is never
present a sharp line of demarcation between the two groups of cells.
By the time that the segmentation cavity is obliterated the whole yolk
is enclosed by the epiblast. The yolk-cells adjoining the opening of
the mesenteron are the latest to be covered in, and on their enclosure
this opening constitutes the whole of the blastopore. The epiblast is
composed of a single row of columnar cells.
Mesoblast and notochord. During the above changes the mesoblast
becomes established. It arises, as in Elasmobranchs, in the form of
two plates derived from the primitive hypoblast. During the
invagination to form the mesenteron some of the hypoblast cells on
each side of the invaginated layer become smaller, and marked off as
two imperfect plates (fig. 38, _ms_). It is difficult to say whether
these plates are entirely derived from invaginated cells, or are _in
part_ directly formed from the pre-existing yolk-cells, but I am
inclined to adopt the latter view; the ventral extension of the
mesoblast plates undoubtedly takes place at the expense of the
yolk-cells. The mesoblast plates soon become more definite, and form
(fig. 39, _ms_) well-defined structures, triangular in section, on the
two sides of the middle line.
[FIG. 39. TRANSVERSE SECTION THROUGH AN EMBRYO OF PETROMYZON PLANERI
OF 208 HOURS.
The figure illustrates the formation of the neural cord and of the
notochord.
_ms._ mesoblast; _nc._ neural cord; _ch._ notochord; _yk._
yolk-cells; _al._ alimentary canal.]
At the time the mesoblast is first formed the hypoblast cells, which
roof the mesenteron, are often imperfectly two layers thick (fig. 38).
They soon however become constituted of a single layer only. When the
mesoblast is fairly established, the lateral parts of the hypoblast
grow inwards underneath the axial part, so that the latter (fig. 39,
_ch_) first becomes isolated as an axial cord, and is next inclosed
between the medullary cord (_nc_) (which has by this time been formed)
and a continuous sheet of hypoblast below (fig. 40). Here its cells
divide and it becomes the notochord. The notochord is thus bodily
formed out of the axial portion of the primitive hypoblast. Its mode
of origin may be compared with that in Amphioxus, in which an axial
fold of the archenteric wall is constricted off as the notochord. The
above features in the development of the notochord were first
established by Calberla[27] (No. 78).
[27] In Calberla's figure, shewing the development of the
notochord, the limits of mesoblast and hypoblast are wrongly
indicated.
[FIG. 40. TRANSVERSE SECTION THROUGH PART OF AN EMBRYO OF PETROMYZON
PLANERI OF 256 HOURS.
_m.c_. medullary cord; _ch_. notochord; _al_. alimentary canal;
_ms_. mesoblastic plate.]
_General history of the development._ Up to about the time when the
enclosure of the hypoblast by the epiblast is completed, no external
traces are visible of any of the organs of the embryo; but about this
time, _i.e._ about 180 hours after impregnation, the rudiment of the
medullary plate becomes established, as a linear streak extending
forwards from the blastopore over fully one half the circumference of
the embryo. The medullary plate first contains a shallow median
groove, but it is converted into the medullary cord, not in the usual
vertebrate fashion, but, as first shewn by Calberla, in a manner much
more closely resembling the formation of the medullary cord in
Teleostei. Along the line of the median groove the epiblast becomes
thickened and forms a kind of keel projecting inwards towards the
hypoblast (fig. 39, _nc_). This keel is the rudiment of the medullary
cord. It soon becomes more prominent, the median groove in it
disappears, and it becomes separated from the epiblast as a solid cord
(fig. 40, _mc_).
By this time the whole embryo has become more elongated, and on the
dorsal surface is placed a ridge formed by the projection of the
medullary cord. At the lip of the blastopore the medullary cord is
continuous with the hypoblast, thus forming the rudiment of a
neurenteric canal.
Calberla gives a similar account of the formation of the neural canal
to that which he gives for the Teleostei (_vide_ p. 72).
He states that the epiblast becomes divided into two layers, of which
the outer is involuted into the neural cord, a median slit in the
involution representing the neural groove. The eventual neural canal
is stated to be lined by the involuted cells. Scott (No. 87) fully
confirms Calberla on this point, and, although my own sections do not
clearly shew an involution of the outer layer of epiblast cells, the
testimony of these two observers must no doubt be accepted on this
point.
Shortly after the complete establishment of the neural cord the
elongation of the embryo proceeds with great rapidity. The processes
in this growth are shewn in fig. 41, A, B, and C. The cephalic portion
(A, _c_) first becomes distinct, forming an anterior protuberance free
from yolk. About the time it is formed the mesoblastic plates begin to
be divided into somites, but the embryo is so opaque that this process
can only be studied in sections. Shortly afterwards an axial lumen
appears in the centre of the neural cord, in the same manner as in
Teleostei.
The general elongation of the embryo continues rapidly, and, as shewn
in my figures, the anterior end is applied to the ventral surface of
the yolk (B). With the growth of the embryo the yolk becomes entirely
confined to the posterior part. This part is accordingly greatly
dilated, and might easily be mistaken for the head. The position of
the yolk gives to the embryo a very peculiar appearance. The apparent
difference between it and the embryos of other Fishes in the position
of the yolk is due in the main to the fact that the postanal portion
of the tail is late in developing, and always small. As the embryo
grows longer it becomes spirally coiled within the egg-shell. Before
hatching the mesoblastic somites become distinctly marked (C).
The hatching takes place at between 13-21 days after impregnation; the
period varying according to the temperature.
[FIG. 41. FOUR STAGES IN THE DEVELOPMENT OF PETROMYZON. (After
Owsjannikoff.)
_c._ cephalic extremity; _bl._ blastopore; _op._ optic vesicle;
_au.v._ auditory vesicle; _br.c._ branchial clefts.]
During the above changes in the external form of the embryo, the
development of the various organs makes great progress. This is
especially the case in the head. The brain becomes distinct from the
spinal cord, and the auditory sacks and the optic vesicles of the eye
become formed. The branchial region of the mesenteron becomes
established, and causes a dilatation of the anterior part of the body,
and the branchial pouches grow out from the throat. The anus becomes
formed, and a neurenteric canal is also established (Scott). The
nature of these and other changes will best be understood by a
description of the structure of the just-hatched larva. The general
appearance of the larva immediately after hatching is shewn in fig.
41, D. The body is somewhat curved; the posterior extremity being much
dilated with yolk, while the anterior is very thin. All the cells
still contain yolk particles, which render the embryo very opaque. The
larva only exhibits slow movements, and is not capable of swimming
about.
The structure of the head is shewn in figs. 42 and 43. Fig. 42 is a
section through a very young larva, while fig. 43 is taken from a
larva three days after hatching, and shews the parts with considerably
greater detail.
[FIG. 42. DIAGRAMMATIC VERTICAL SECTION OF A JUST-HATCHED LARVA OF
PETROMYZON. (From Gegenbaur; after Calberla.)
_o._ mouth; _o´._ olfactory pit; _v._ septum between stomodæum and
mesenteron; _h._ thyroid involution; _n._ spinal cord; _ch._
notochord; _c._ heart; _a._ auditory vesicle.]
On the ventral side of the head is placed the oral opening (fig. 43,
_m_) leading into a large stomodæum which is still without a
communication with the mesenteron. Ventrally the stomodæum is
prolonged for a considerable distance under the anterior part of the
mesenteron. Immediately behind the stomodæum is placed the branchial
region of the mesenteron. Laterally it is produced on each side into
seven or perhaps eight branchial pouches (fig. 43, _br.c_), which
extend outwards nearly to the skin but are not yet open. Between the
successive pouches are placed mesoblastic segments, of the same nature
and structure as the walls of the head cavities in the embryos of
Elasmobranchs, and like them enclosing a central cavity. A similar
structure is placed behind the last, and two similar structures in
front of the first persistent pouch. This pouch is situated in the
same vertical line as the auditory sack (_au.v_), and would appear
therefore to be the hyobranchial cleft; and this identification is
confirmed by the fact of two head cavities being present in front of
it. At the front end of the branchial region of the mesenteron is
placed a thickened ridge of tissue, which, on the opening of the
passage between the stomodæum and the mesenteron, forms a partial
septum between the two, and is known as the velum (fig. 43, _tv_).
[FIG. 43. DIAGRAMMATIC VERTICAL SECTION THROUGH THE HEAD OF A LARVA
OF PETROMYZON.
The larva had been hatched three days, and was 4.8 mm. in length.
The optic and auditory vesicles are supposed to be seen through the
tissues. The letter _tv_ pointing to the base of the velum is where
Scott believes the hyomandibular cleft to be situated.
_c.h._ cerebral hemisphere; _th._ optic thalamus; _in._
infundibulum; _pn._ pineal gland; _mb._ mid-brain; _cb._ cerebellum;
_md._ medulla oblongata; _au.v._ auditory vesicle; _op._ optic
vesicle; _ol._ olfactory pit; _m._ mouth; _br.c._ branchial pouches;
_th._ thyroid involution; _v.ao._ ventral aorta; _ht._ ventricle of
heart; _ch._ notochord.]
According to Scott (No. 87) a hyomandibular pouch forming the eighth
pouch is formed in front of the pouch already defined as the
hyobranchial. It disappears early and does not acquire gill folds[28].
The tissue forming the line of insertion of the velum appears to me to
represent the mandibular arch. The grounds for this view are the
following:
(1) The structure in question has _exactly_ the position usually
occupied by the mandibular arch.
(2) There is present in late larvæ (about 20 days after hatching) an
arterial vessel, continued from the ventral prolongation of the bulbus
arteriosus along the insertion of the velum towards the dorsal aorta,
which has the relations of a true branchial artery.
[28] Scott informs me that he has been unable to find the
hyomandibular pouch in larvæ larger than 4.8 mm. My material of
the stages when it should be present is somewhat scanty, but I
have as yet, very likely owing to the imperfection of my
material, been unable to find Scott's hyomandibular pouch either
in my sections or surface-views. Huxley describes this pouch as
present in the form of a cleft in later stages; I have failed to
find his cleft also. The vessel interpreted below as the
branchial artery of the mandibular arch was only imperfectly
investigated by me, and I was not sure of my interpretations
about it. Scott however informs me by letter that it is
undoubtedly present.
On the ventral aspect of the branchial region is placed a sack (figs.
42, _h_, and 43, _th_), which extends from the front end of the
branchial region to the fourth cleft. At first it constitutes a groove
opening into the throat above (fig. 44), but soon the opening becomes
narrowed to a pore placed between the second and third of the
_permanent_ branchial pouches (fig. 43, _th_). In Ammocoetes[29] the
simple tube becomes divided, and assumes a very complicated form,
though still retaining its opening into the branchial region of the
throat. In the adult it forms a glandular mass underneath the
branchial region of the throat equivalent to the thyroid gland of
higher Vertebrates.
[29] Schneider (No. 85) states that in the full-grown
Ammocoetes the opening is situated between the third and fourth
pouches. This is certainly not true for the young larva.
On the ventral aspect of the head, and immediately in front of the
mouth, is placed the olfactory pit (fig. 43, _ol_). It is from the
first _unpaired_, and in just-hatched larvæ simply forms a shallow
groove of thickened epiblast at the base of the front of the brain. By
the stage represented in fig. 43 the ventral part of the original
groove is prolonged into a pit, extending backwards beneath the brain
nearly up to the infundibulum.
[FIG. 44. DIAGRAMMATIC TRANSVERSE SECTIONS THROUGH THE BRANCHIAL
REGION OF A YOUNG LARVA OF PETROMYZON. (From Gegenbaur; after
Calberla.)
_d._ branchial region of throat.]
On the side of the head, nearly on a level with the front end of the
notochord, is placed the eye (fig. 43, _op_). It is constituted (figs.
45 and 46) of a very shallow optic cup with a thick outer (retinal)
layer, and a thin inner choroid layer. In contact with the retinal
layer is placed the lens. The latter is formed as an invagination of
the skin; to which it is still attached in the just-hatched larva
(fig. 45). The eye only differs at this stage from that of other
Vertebrata in its extraordinarily small size, and the rudimentary
character of its constituent parts.
The auditory sack is a large vesicle (fig. 43, _au.v._), placed at the
side of the brain opposite the first persistent branchial pouch.
The brain is formed of the usual vertebrate parts[30], but is
characterized by the very slight cranial flexure. The fore-brain
consists (fig. 43) of a thalamencephalon (_th_) and an undivided
cerebral rudiment (_ch_). To the roof of the thalamencephalon is
attached a flattened sack (_pn_) which is probably the pineal gland.
The floor is prolonged into an infundibulum (_in_) which contains a
prolongation of the third ventricle. The lateral walls of the cerebral
rudiment are much thickened.
[30] Max Schultze's statements as to the structure and histology
of the brain are very inadequate in the present state of our
knowledge.
Behind the thalamencephalon follows the mid-brain (_mb_), the sides of
which form the optic lobes, and behind this again the hind-brain
(_md_); the front border of the roof of which is thickened to form the
cerebellum (_cb_). The medulla passes without any marked line of
demarcation into the spinal cord.
[FIG. 45. HORIZONTAL SECTION THROUGH THE HEAD OF A JUST-HATCHED
LARVA OF PETROMYZON SHEWING THE DEVELOPMENT OF THE LENS OF THE EYE.
_th.c._ thalamencephalon; _op.v._ optic vesicle; _l._ lens of eye;
_h.c._ head cavity.]
The histological differentiation of the brain has already proceeded to
some extent; and it has in the main the same character as the spinal
cord. Before the larva has been hatched very long a lateral investment
of white matter is present throughout. The notochord (_ch_) is
continued forwards in the head to the hinder border of the
infundibulum. It is slightly flexed anteriorly.
From the hinder border of the auditory region to the end of the
branchial region the mesoblast is dorsally divided into myotomes,
which nearly, though not quite, correspond in number with the
branchial pouches.
The growth of the myotomes would seem, as might be anticipated from
their independent innervation, not to be related to that of the
branchial pouches, so that there is a want of correspondence between
these parts, the extent of which varies at different periods of life.
The relation between the two in an old larva is shewn in fig. 47.
[FIG. 46. EYE OF A LARVA OF PETROMYZON NINE DAYS AFTER HATCHING.
_l._ lens; _r._ retina.
The section passes through one side of the lens.]
The head of the larva of Petromyzon differs very strikingly in general
appearance from that of the normal Vertebrata. This is at once shewn
by a comparison of fig. 43 with fig. 29. The most important difference
between the two is due to the absence of a pronounced cranial flexure
in Petromyzon; an absence which is in its turn probably caused by the
small development of the fore-brain.
The stomodæum of Petromyzon is surprisingly large, and its size and
structure in this type militate against the view of some embryologists
that the stomodæum originated from the coalescence of a pair of
branchial pouches.
In the region of the trunk there is present an uninterrupted dorsal
fin continuous with a ventral fin round the end of the tail.
There is a well-developed body cavity, which is especially dilated in
front, in the part which afterwards becomes the pericardium. In this
region is placed the nearly straight heart, divided into an auricle
and ventricle (figs. 42 and 43), the latter continued forwards into a
bulbus arteriosus.
The myotomes are now very numerous (about 57, including those of the
head, in a three days' larva). They are separated by septa, but do not
fill up the whole space between the septa, and have a peculiar wavy
outline. The notochord is provided with a distinct sheath, and below
it is placed a subnotochordal rod.
The alimentary canal consists of a narrow anterior section free from
yolk, and a posterior region, the walls of which are largely swollen
with yolk. The anterior section corresponds to the region of the
oesophagus and stomach, but exhibits no distinction of parts.
Immediately behind this point the alimentary canal dilates
considerably, and on the ventral side is placed the opening of a
single large sack, which forms the commencement of the liver. The
walls of the hepatic sack are posteriorly united to the yolk-cells. At
the region where the hepatic sack opens into the alimentary tract the
latter dilates considerably.
The posterior part of the alimentary tract still constitutes a kind of
yolk-sack, the ventral wall being enormously thick and formed of
several layers of yolk-cells. The dorsal wall is very thin.
The excretory system is composed of two segmental ducts, each
connected in front with a well-developed pronephros (head-kidney),
with about five ciliated funnels opening into the pericardial region
of the body cavity. The segmental ducts in the larvæ open behind into
the cloacal section of the alimentary tract.
[FIG. 47. HEAD OF A LARVA OF PETROMYZON SIX WEEKS OLD.
(Altered from Max Schultze.)
_au.v._ auditory vesicle; _op._ optic vesicle; _ol._ olfactory pit;
_ul._ upper lip; _ll._ lower lip; _or.p._ papillæ at side of mouth;
_v._ velum; _br.s._ extra branchial skeleton; 1-7. branchial clefts.]
The development of the larva takes place with considerable rapidity.
The yolk becomes absorbed and the larva becomes accordingly more
transparent. It generally lies upon its side, and resembles in general
appearance and habit a minute Amphioxus. It is soon able to swim with
vigour, but usually, unless disturbed, is during the day quite
quiescent, and chooses by preference the darkest situations. It soon
straightens out, and, with the disappearance of the yolk, the tail
becomes narrower than the head. A large caudal fin becomes developed.
When the larva is about twenty days old, it bears in most anatomical
features a close resemblance to an Ammocoetes; though the histological
differences between my oldest larva (29 days) and even very young
Ammocoetes are considerable.
The mouth undergoes important changes. The upper lip becomes much more
prominent, forming of itself the anterior end of the body (fig. 47,
_ul_). The opening of the nasal pit is in this way relatively thrown
back, and at the same time is caused to assume _a dorsal position_.
This will be at once understood by a comparison of fig. 43 with fig.
47. On the inner side of the oral cavity a ring of papillæ is formed
(fig. 47, _or.p_). Dorsally these papillæ are continued forward as a
linear streak on the under side of the upper lip. A communication
between the oral cavity and the branchial sack is very soon
established.
The gill pouches gradually become enlarged; but it is some time before
their small external openings are established. Their walls, which are
entirely lined by hypoblast, become raised in folds, forming the
branchial lamellæ. The walls of the head cavities between them become
resolved into the contractors and dilators of the branchial sacks. The
extra-branchial basketwork becomes established very early (it is
present in the larva of 6 millimetres, about 9 days after hatching)
and is shewn in an older larva in fig. 47, _br.s_. It is not so
complicated in these young larvæ as in the Ammocoetes, but in Max
Schultze's figure, which I have reproduced, the dorsal elements of the
system are omitted. On the dorsal wall of the branchial region a
ciliated ridge is formed, which may be homologous with the ridge on
the dorsal wall of the branchial sack of Ascidians. It has been
described by Schneider in Ammocoetes.
With reference to the remainder of the alimentary canal there is but
little to notice. The primitive hepatic diverticulum rapidly sprouts
out and forms a tubular gland. The opening into the duodenum changes
from a ventral to a lateral or even dorsal position. The duct leads
into a gall-bladder imbedded in the substance of the liver. Ventrally
the liver is united with the abdominal wall, but laterally passages
are left by which the pericardial and body cavities continue to
communicate.
The greater part of the yolk becomes employed in the formation of the
intestinal wall. This part of the intestine in a nine days' larva (67
mm.) has the form of a cylindrical tube with very thick columnar cells
entirely filled with yolk particles. The dorsal wall is no longer
appreciably thinner than the ventral. In the later stages the cells of
this part of the intestine become gradually less columnar as the yolk
is absorbed.
The fate of the yolk-cells in the Lamprey is different from that in
most other Vertebrata with an equally large amount of yolk. They no
doubt supply nutriment for the growth of the embryo, and although in
the anterior part of the intestine they become to some extent enclosed
in the alimentary tract and break up, yet in the posterior part they
become wholly transformed into the regular epithelium of the
intestine.
On the ninth day a slight fold filled with mesoblastic tissue is
visible on the dorsal wall of the intestine. This fold appears to
travel towards the ventral side; at any rate a similar but
better-marked fold is visible in a ventro-lateral position at a
slightly later period. This fold is the commencement of the fold which
in the adult makes a half spiral, and is no doubt equivalent to the
spiral valve of Elasmobranchs and Ganoids. It contains a prolongation
of the coeliac artery, which constitutes at first the vitelline
artery.
The nervous system does not undergo during the early larval period
changes which require a description.
The opening of the olfactory sack becomes narrowed and ciliated (fig.
47, _ol_). It is carried by the process already mentioned to the
dorsal surface of the head. The lumen of the sack is well developed;
and lies in contact with the base of the fore part of the brain.
The vascular system presents no very remarkable features. The heart is
two-chambered and straight. The ventricle is continued forwards as a
bulbus arteriosus, which divides into two arteries at the thyroid
body. From the bulbus and its continuations eight branches are given
off to the gills; and, as mentioned above, a vessel, probably of the
same nature, is given off in the region of the velum. The blood from
the branchial sacks is collected into the dorsal aorta. Some of it is
transmitted to the head, but the greater part flows backwards under
the notochord.
The venous system consists of the usual anterior and posterior
cardinal veins which unite on each side into a ductus Cuvieri, and of
a great subintestinal vessel of the same nature as that in embryo
Elasmobranchs, which persists however in the adult. It breaks up into
capillaries in the liver, and constitutes therefore the portal vein.
From the liver the blood is brought by the hepatic vein into the sinus
venosus. In addition to these vessels there is a remarkable unpaired
sub-branchial vein, which brings back the blood directly to the heart
from the ventral part of the branchial region.
Metamorphosis. The larva just described does not grow directly into
the adult, but first becomes a larval form, known as Ammocoetes, which
was supposed to be a distinct species till Aug. Müller (No. 80) made
the brilliant discovery of its nature.
The Ammocoetes does not differ to any marked extent from the larva
just described. The histological elements become more differentiated,
and a few organs reach a fuller development.
The branchial skeleton becomes more developed, and capsules for the
olfactory sack and auditory sacks are established.
The olfactory sack is nearly divided into two by a ventral septum. The
eye (fig. 48) is much more fully developed, but lies a long way below
the surface. The optic cup forms a deep pit, in the mouth of which is
placed the lens. The retinal layers are well developed (cf.
Langerhans), and the outer layer of the optic cup or layer of retinal
pigment (_rp_) contains numerous pigment granules, especially on its
dorsal side. At the edge of the optic cup the two layers fall into
each other. They constitute the commencement of the pigment layer of
the iris; but at this stage they are not pigmented. The mesoblast of
the iris is hardly differentiated. The lens (_l_) has the normal
structure of the embryonic lens of Vertebrata. The inner wall is thick
and doubly convex, while the outer wall, which will form the anterior
epithelium, is very thin. There is a large space between the lens and
the retina containing the vitreous humour (_v.h_). There is no aqueous
humour, and the tissues in front of the lens bear but little
resemblance to those in higher Vertebrata. The cornea is represented
by (1) the epidermis (_ep_); (2) the dermis (_d.c_); (3) the subdermal
connective tissue (_s.d.c_) which passes without any sharp line of
demarcation into the dermis; (4) a thick membrane continuous with the
choroid which represents Descemet's membrane. The subdermal connective
tissue is continued as an investment round the whole eye. There is no
specially differentiated sclerotic, and a choroid is only imperfectly
indicated[31]. The peculiar features of the eye of the young larva of
the Ammocoetes are probably due to degeneration.
[31] Langerhans _loc. cit._ describes the eye of the
Ammocoetes in some respects very differently from the above.
Very probably his description applies to an older Ammocoetes.
The most important points of difference appear to be (1) that the
vitreous humour is all but obliterated; (2) that the iris is much
better developed.
[FIG. 48. EYE OF AN AMMOCOETES LYING BENEATH THE SKIN.
_ep._ epidermis; _d.c._ dermal connective tissue continuous with the
subdermal connective tissue (_s.d.c_), which is also shaded. There
is no definite boundary to this tissue where it surrounds the eye.
_m._ muscles; _dm._ membrane of Descemet; _l._ lens; _v.h._ vitreous
humour; _r._ retina; _rp._ retinal pigment.]
In the brain the two cerebral hemispheres lie one on each side of the
anterior end of the thalamencephalon. There are well-defined olfactory
lobes, and two distinct olfactory nerves are present.
The excretory system has undergone great changes. A series of
segmental tubes, which first appear in a larva of about 9 mm., becomes
established behind the pronephros, and in an Ammocoetes of 65 mm. the
pronephros has begun to atrophy. The generative organs are formed in a
larva of about 35 mm. Shortly before the metamorphosis the portion of
the cloaca into which the segmental tubes open becomes separated off
as a distinct urinogenital sinus, the walls of which become perforated
by the two abdominal pores.
The Ammocoetes of Petromyzon Planeri lives in the mud in streams.
Without undergoing any marked changes in structure it gradually grows
larger, and after three or four years undergoes a metamorphosis. The
full-grown larva may be as large or even larger than the adult. The
metamorphosis takes place from August till January. The breeding
season sets in during the second half of April; and shortly after
depositing its generative products the Lamprey dies. The changes which
take place in the metamorphosis are of a most striking kind.
The dome-shaped mouth of the larva is replaced (fig. 47) by a more
definitely suctorial mouth with horny cuticular teeth (fig. 49). The
eyes appear on the surface; and the dorsal fin becomes more prominent,
and is divided into two parts.
[FIG. 49. MOUTH OF PETROMYZON MARINUS WITH ITS HORNY TEETH. (From
Gegenbaur; after Heckel and Kner.)]
Besides these obvious external changes very great modifications are
effected in almost all the organs, which may be very briefly
enumerated.
1. Very profound changes take place in the skeleton. An elaborate
system of cartilages is developed in connection with the mouth; the
cranium itself undergoes important modifications; and neural arches
become formed.
2. Considerable changes are effected in the gill pouches, and,
according to Schneider, whose statements must however be received with
some caution, the branchial sack becomes detached posteriorly from the
oesophagus, the oesophagus then sends forwards a prolongation above
the branchial sack which is at first solid. This prolongation forms
the anterior part of the oesophagus of the adult, and joins the
primitive oral cavity at the velum. The so-called bronchus of the
adult is thus the whole branchial region of the Ammocoetes, and the
anterior part of the oesophagus of the adult is an entirely new
formation.
3. The posterior part of the alimentary tract of the Ammocoetes
undergoes partial atrophy. The gall-bladder of the liver is absorbed;
and the liver itself ceases to communicate with the intestine.
4. The eye undergoes important changes in that it travels to the
surface, and acquires all the characters of the normal vertebrate eye.
5. The brain becomes relatively larger but more compact, and the optic
lobes (corpora bigemina) become more distinct.
6. The pericardial cavity becomes completely separated from the body
cavity, and a distinct pericardium is formed.
7. The mesonephros of the larva disappears, and a fresh posterior part
is formed.
Myxine. The ovum of Myxine when ready to be laid is inclosed, as shewn
by Allen Thomson[32], in an oval horny shell in many respects similar
to that of Elasmobranchii; from its ends there project a number of
trumpet-shaped tubular processes, which no doubt serve to attach it to
marine objects. No observations have been made on the development.
[32] _Cyclopædia of Anat. and Phys._ Article 'Ovum.'
BIBLIOGRAPHY.
(77) E. Calberla. "Der Befruchtungsvorgang beim Petromyzon Planeri."
_Zeit. f. wiss. Zool._, Vol. XXX. 1877.
(78) E. Calberla. "Ueb. d. Entwicklung d. Medullarrohres u. d. Chorda
dorsalis d. Teleostier u. d. Petromyzonten." _Morpholog. Jahrbuch_,
Vol. III. 1877.
(79) C. Kupffer u. B. Benecke. _Der Vorgang d. Befruchtung am Ei d.
Neunaugen._ Königsberg, 1878.
(80) Aug. Müller. "Ueber die Entwicklung d. Neunaugen." Müller's
_Archiv_, 1856.
(81) Aug. Müller. _Beobachtungen üb. d. Befruchtungserscheinungen im
Ei d. Neunaugen._ Königsberg, 1864.
(82) W. Müller. "Das Urogenitalsystem d. Amphioxus u. d. Cyclostomen."
_Jenaische Zeitschrift_, Vol. IX. 1875.
(83) Ph. Owsjannikoff. "Die Entwick. von d. Flussneunaugen." Vorläuf.
Mittheilung. _Mélanges Biologiques tirés du Bulletin de l'Acad. Imp.
St Pétersbourg_, Vol. VII. 1870.
(84) Ph. Owsjannikoff. _On the development of Petromyzon fluviatilis_
(Russian).
(85) Anton Schneider. _Beiträge z. vergleich. Anat. u. Entwick. d.
Wirbelthiere._ Quarto. Berlin, 1879.
(86) M. S. Schultze. "Die Entwickl. v. Petromyzon Planeri." Gekrönte
Preisschrift. Haarlem, 1856.
(87) W. B. Scott. "Vorläufige Mittheilung üb. d.
Entwicklungsgeschichte d. Petromyzonten." _Zoologischer Anzeiger_,
Nos. 63 and 64. III. Jahrg. 1880.
CHAPTER VI.
GANOIDEI[33].
[33] The following classification of the Ganoidei is employed in
the present chapter:
I. Selachoidei. {Acipenseridæ.
{Polyodontidæ.
{Polypteridæ.
II. Teleostoidei. {Amiidæ.
{Lepidosteidæ.
It is only within quite recent times that any investigations have been
made on the embryology of this heterogeneous, but primitive group of
fishes. Much still remains to be done, but we now know the main
outlines of the development of Acipenser and Lepidosteus, which are
representatives of the two important subdivisions of the Ganoids. Both
types have a complete segmentation, but Lepidosteus presents in its
development some striking approximations to the Teleostei. I have
placed at the end of the chapter a few remarks with reference to the
affinities indicated by the embryology.
ACIPENSER[34].
[34] Our knowledge of the development of Acipenser is in the main
derived from Salensky's valuable observations. His full memoir is
unfortunately published in Russian, and I have been obliged to
satisfy myself with the abstract (No. 90), and with what could be
gathered from his plates. Prof. Salensky very kindly supplied me
with some embryos; and I have therefore been able to some extent
to work over the subject myself. This is more especially true for
the stages after hatching. The embryos of the earlier stages were
not sufficiently well preserved for me to observe more than the
external features and a few points with reference to the
formation of the layers.
The freshly laid ovum is 2 mm. in diameter and is invested by a
two-layered shell, covered by a cellular layer derived from the
follicle[35]. The segmentation, though complete, approaches the
meroblastic type more nearly than the segmentation of the frog's egg.
The first furrow appears at the formative pole, at which the germinal
vesicle was situated. The earlier phases of the segmentation are like
those of meroblastic ova, in that the furrows only penetrate for a
certain distance into the egg. Eight vertical furrows appear before
the first equatorial furrow; which is somewhat irregular, and situated
close to the formative pole.
[35] Seven micropylar apertures, six of which form a circle round
the seventh, are stated by Kowalevsky, Wagner, and Owsjannikoff
(No. 89) to be present at one of the poles of the inner egg
membrane. They are stated by Salensky to vary in number from five
to thirteen.
In the later stages the vertical furrows extend through the whole egg,
and a segmentation cavity appears between the small and the large
spheres. The segmentation is thus in the main similar to that of a
frog, from which it diverges in the fact that there is a greater
difference in size between the small and the large segments.
[FIG. 50. EMBRYOS OF ACIPENSER VIEWED FROM THE DORSAL SURFACE.
(After Salensky.)
A. Stage before the appearance of the mesoblastic somites.
B. Stage with five somites.
_Mg._ medullary groove; _bl.p._ blastopore; _s.d._ segmental duct;
_Fb._ fore-brain; _Hb._ hind-brain; _m.s._ mesoblastic somite.]
In the final stages of the segmentation the cells become distinctly
divided into two layers. A layer of small cells is placed at the
formative pole, and constitutes the epiblast. The cells composing it
are divided, like those of Teleostei, etc., into a superficial
epidermic and a deeper nervous layer. The remaining cells constitute
the primitive hypoblast (the eventual hypoblast and mesoblast); they
form a great mass of yolk-cells at the lower pole, and also spread
along the roof of the segmentation cavity, on the inner side of the
epiblast.
A process of unsymmetrical invagination now takes place, which is in
its essential features exactly similar to that in the frog or the
lamprey, and I must refer the reader for the details of the process to
the chapter on the Amphibia. The edge of the cap of epiblast forms an
equatorial line. For the greater extent of this line the epiblast
cells grow over the hypoblast, as in an epibolic gastrula, but for a
small arc they are inflected. At the inflected edge an invagination of
cells takes place, underneath the epiblast, towards the segmentation
cavity, and gives rise to the dorsal wall of the mesenteron and the
main part of the dorsal mesoblast. The slit below the invaginated
layer gradually dilates to form the alimentary cavity; the ventral
wall of which is at first formed of yolk-cells. The epiblast along the
line of the invaginated cells soon becomes thickened, and forms a
medullary plate, which is not very distinct in surface views. The
cephalic extremity of this plate, which is furthest removed from the
edge, dilates, and the medullary plate then assumes a spatula form
(fig. 50 A, _Mg_).
By the continued extension of the epiblast the uncovered part of the
hypoblast has in the meantime become reduced to a small circular
pore--the blastopore--and in surface views of the embryo has the form
represented in fig. 50 A, _bl.p_. The invagination of the mesenteron
has in the meantime extended very far forwards, and the segmentation
cavity has become obliterated. The lip of the blastopore has moreover
become inflected for its whole circumference.
The invaginated cells forming the dorsal wall of the mesenteron soon
become divided into a pigmented hypoblastic epithelium adjoining the
lumen of the mesenteron (fig. 51, _En_) and a mesoblastic layer
(_Sgp_), between the hypoblast and the epiblast. The mesoblast is
divided into two plates, between which is placed the notochord[36]
(_Ch_).
[36] Salensky believes that the notochord is derived from the
mesoblast. I could not satisfy myself on this point.
With the completion of the medullary plate and the germinal layers,
the first embryonic period may be considered to come to a close. The
second period ends with the hatching of the embryo. During it the
rudiments of the greater number of organs make their appearance. The
general form of the embryo during this period is shewn in figs. 50 B
and 52 A and B.
One of the first changes to take place is the conversion of the
medullary plate into the medullary canal. This, as shewn in fig. 51,
is effected in the usual vertebrate fashion, by the establishment of a
medullary groove which is then converted into a closed canal by the
folding over of the sides.
The uncovered patch of yolk in the blastoporic area soon becomes
closed over; and on the formation of the medullary canal the usual
neurenteric canal becomes established.
[FIG. 51. TRANSVERSE SECTION THROUGH THE ANTERIOR PART OF AN
ACIPENSER EMBRYO. (After Salensky.)
_Rf._ medullary groove; _Mp._ medullary plate; _Wg._ segmental duct;
_Ch._ notochord; _En._ hypoblast; _Sgp._ mesoblastic somite; _Sp._
parietal part of mesoblastic plate.]
The further changes which take place are in the main similar to those
in other Ichthyopsida, but in some ways the appearance of the embryo
is, as may be gathered from fig. 52, rather strange. This is mainly
due to the fact that the embryo does not become folded off from the
yolk in the manner usual in Vertebrates; and as will be shewn in the
sequel, the relation of the yolk to the embryo is unlike that in any
other known Vertebrate. The appearance of the embryo is something like
that of an ordinary embryo slit open along the ventral side and then
flattened out. Organs which properly belong to the ventral side appear
on the lateral parts of the dorsal surface. Owing to the great forward
extension of the yolk the heart (fig. 52 B) appears to be placed
directly in front of the head.
Even before the formation of the medullary canal the cephalic portion
of the nervous system becomes marked out. This part, after the closure
of the medullary groove, becomes divided into two (fig. 50 B), and
then three lobes--the fore-, the mid-, and the hind-brain (fig. 52, A
and B). From the lateral parts of the at first undivided fore-brain
the optic vesicles (fig. 52 B, _Op_) soon sprout out; and in the
hind-brain a dilatation to form the fourth ventricle appears in the
usual fashion.
[FIG. 52. EMBRYOS OF ACIPENSER BELONGING TO TWO STAGES VIEWED FROM
THE DORSAL SURFACE. (After Salensky.)
_Fb._ fore-brain; _Mb._ mid-brain; _Hb._ hind-brain; _cp._ cephalic
plate; _Op._ optic vesicle; _Auv._ auditory vesicle; _Olp._
olfactory pit; _Ht._ heart; _Md._ mandibular arch; _Ha._ hyoid arch;
_Br´._ first branchial arch; _Sd._ segmental duct.]
The epiblast at the sides of the brain constitutes a more or less
well-defined structure, which may be spoken of as a cephalic plate
(fig. 52 A, _cp_). From this plate are formed the essential parts of
the organs of special sense. Anteriorly the olfactory pits arise (fig.
52 B, _Olp_) as invaginations of both layers of the epiblast. The lens
of the eye is formed as an ingrowth of the nervous layer only, and
opposite the hind-brain the auditory sack (fig. 52 A and B, _Auv_) is
similarly formed from the nervous layer of the epiblast. At the sides
of the cephalic plate the visceral arches make their appearance; and
in fig. 52 A and B there are shewn the mandibular (_Md_), hyoid (_Ha_)
and first branchial (_Br´_) arches, with the hyomandibular (spiracle)
and hyobranchial clefts between them. They constitute peculiar
concentric circles round the cephalic plate; their shape being due to
the flattened form of the embryo, already alluded to.
While the above structures are being formed in the head the changes in
the trunk have also been considerable. The mesoblastic plates at the
junction of the head and trunk become very early segmented, the
segments being formed from before backwards (fig. 50 B). With their
formation the trunk rapidly increases in length. At their outer border
the segmental duct (fig. 50 B, and fig. 52 A, _Sd_) is very early
established. It is formed, as in Elasmobranchs, as a solid outgrowth
of the mesoblast (fig. 51, _Wg_); but its anterior extremity becomes
converted into a pronephros (fig. 57, _pr.n_).
Before hatching, the embryo has to a small extent become folded off
from the yolk both anteriorly and posteriorly; and has also become to
some extent vertically compressed. As a result of these changes, the
general form of its body becomes much more like that of an ordinary
Teleostean embryo.
The general features of the larva after hatching are illustrated by
figs. 53, 54 and 55. Fig. 53 represents a larva of about 7 mm. and
fig. 54 a lateral and fig. 55 a ventral view of the head of a larva of
about 11 mm.
[FIG. 53. LARVA OF ACIPENSER OF 7 MM., SHORTLY AFTER HATCHING.
_ol._ olfactory pit; _op._ optic vesicle; _sp._ spiracle; _br.c._
branchial clefts; _an._ anus.]
There are only a few points which call for special attention in the
general form of the body. In the youngest larva figured the ventral
part of the hyomandibular cleft is already closed: the dorsal part of
the cleft is destined to form the spiracle (_sp_). The arch behind is
the hyoid: on its posterior border is a membranous outgrowth, which
will develop into the operculum. In older larvæ, a very rudimentary
gill appears to be developed on the front walls of the spiracular
cleft (Parker), but I have not succeeded in satisfying myself about
its presence; and rows of gill papillæ appear on the hyoid and the
true branchial arches (figs. 54 and 55, _g_). The biserially-arranged
gill papillæ of the true branchial arches are of considerable length,
and are not at first covered by the operculum; but they do not form
elongated thread-like external gills similar to those of the
Elasmobranchii.
The oral cavity is placed on the ventral side of the head; it has at
first a more or less rhomboidal form. It soon however (fig. 55)
becomes narrowed to a slit with projecting lips, and eventually
becomes converted into the suctorial mouth of the adult. The most
remarkable feature connected with the mouth is the development of
provisional teeth (fig. 55) on both jaws.
These teeth were first discovered by Knock (No. 88). They do not
appear to be calcified, and might be supposed to be of the same nature
as the horny teeth of the Lamprey. They are however developed like
true teeth, as a deposit between a papilla of subepidermic tissue and
an epidermic cap. The substance of which they are formed corresponds
morphologically to the enamel of ordinary teeth. As they grow they
pierce the epidermis, and form hollow spine-like structures with a
central axis filled with subepidermic (mesoblastic) cells. They
disappear after the third month of larval life.
In front of the mouth two pairs of papillæ grow out, which appear to
be of the same nature as the papillæ on the suctorial disc in the
embryo of Lepidosteus (_vide_ p. 115). They are very short in the
embryo represented in fig. 53; soon however they grow in length (figs.
54 and 55, _st_); and it is probable that they become the barbels,
since these occupy a precisely similar position[37].
[37] If these identifications are correct the barbels of fishes
must be phylogenetically derived from the papillæ of a suctorial
disc adjoining the mouth.
[FIG. 54. SIDE VIEW OF A LARVA OF ACIPENSER OF 11 MILLIMETRES.
_op._ eye; _ol._ olfactory pit; _st._ suctorial (?) processes; _m._
mouth; _sp._ spiracle; _g._ gills.]
The openings of the nasal pits are at first single; but the opening of
each becomes gradually divided into two by the growth of a flap on the
outer side (fig. 54, _ol_). It is probable that this flap is
equivalent to the fold of the superior maxillary process of the
Amniota, which by its growth roofs over the open groove which
originally leads from the external to the internal nares; so that the
two openings of each nasal sack, so established in these and in other
fishes, correspond to the external and internal nares of higher
Vertebrata.
[FIG. 55. VENTRAL VIEW OF A LARVA OF ACIPENSER OF 11 MILLIMETRES.
_m._ mouth; _st._ suctorial (?) processes; _op._ eye; _g._ gills.]
At the time of hatching there is a continuous dorso-ventral fin,
which, by atrophy in some parts, and hypertrophy in other parts, gives
rise to all the unpaired fins of the adult, except the first dorsal
and the abdominal. The caudal part of the fin is at first symmetrical,
and the heterocercal tail is produced by the special growth of the
ventral part of the fin.
[FIG. 56. DIAGRAMMATIC LONGITUDINAL SECTION THROUGH THE ANTERIOR
PART OF THE TRUNK OF A LARVA OF ACIPENSER TO SHEW THE POSITION
OCCUPIED BY THE YOLK.
_in._ intestine; _st._ stomach filled with yolk; _oes._ oesophagus;
_l._ liver; _ht._ heart; _ch._ notochord; _sp.c._ spinal cord.]
Of the internal features of development in the Sturgeon the most
important concern the relation of the yolk to the alimentary tract. In
most Vertebrata the yolk-cells form a protuberance of the part of the
alimentary canal, immediately behind the duodenum. The yolk may
either, as in the lamprey or frog, form a simple thickening of the
alimentary wall in this region, or it may constitute a well-developed
yolk-sack as in Elasmobranchii and the Amniota. In either case the
liver is placed in front of the yolk. In the Sturgeon on the contrary
the yolk is placed almost entirely in front of the liver, and the
Sturgeon appears to be also peculiar in that the yolk, instead of
constituting an appendage of the alimentary tract, is completely
enclosed in a dilated portion of the tract which becomes the stomach
(figs. 56 and 57). It dilates this portion to such extent that it
might be supposed to form a true external yolk-sack. In the stages
before hatching the glandular hypoblast, which was established on the
dorsal side of the primitive mesenteron, envelops the yolk-cells,
which fuse together into a yolk-mass, and lose all trace of their
original cellular structure.
The peculiar flattening out of the embryo over the yolk (_vide_ p.
105) is no doubt connected with the mode in which the yolk becomes
enveloped by the hypoblast.
[FIG. 57. TRANSVERSE SECTION THROUGH THE REGION OF THE STOMACH OF A
LARVA OF ACIPENSER 5 MM. IN LENGTH.
_st._ epithelium of stomach; _yk._ yolk; _ch._ notochord, below
which is a subnotochordal rod; _pr.n._ pronephros; _ao._ aorta;
_mp._ muscle-plate formed of large cells, the outer parts of which
are differentiated into contractile fibres; _sp.c._ spinal cord;
_b.c._ body cavity.]
As the posterior part of the trunk, containing the intestine, becomes
formed, the yolk is gradually confined to the anterior part of the
alimentary tract, which, as before stated, becomes the stomach. The
epithelial cells of the stomach, as well as those of the intestine,
are enormously dilated with food-yolk (fig. 57, _st_). Behind the
stomach is formed the liver. The subintestinal vein bringing back the
blood to the liver appears to have the same course as in Teleostei, in
that the blood, after passing through the liver, is distributed to the
walls of the stomach and is again collected into a venous trunk which
falls into the sinus venosus. As the yolk becomes absorbed, the liver
grows forwards underneath the stomach till it comes in close contact
with the heart. The relative position of the parts at this stage is
shewn diagrammatically in fig. 56. At the commencement of the
intestine there arises in the larva of about 14 mm. a great number of
diverticula, which are destined to form the compact glandular organ,
which opens at this spot in the adult. At this stage there is also a
fairly well developed pancreas opening into the duodenum at the same
level as the liver.
No trace of the air-bladder was present at the stage in question.
The spiral valve is formed, as in Elasmobranchii, as a simple fold in
the wall of the intestine.
There is a well developed subnotochordal rod (fig. 57) which,
according to Salensky, becomes the subvertebral ligament of the adult;
a statement which confirms an earlier suggestion of Bridge. The
pronephros (head-kidney) resembles in the main that of Teleostei (fig.
57); while the front end of the mesonephros, which is developed
considerably later than the pronephros, is placed some way behind it.
In my oldest larva (14 mm.) the mesonephros did not extend backwards
into the posterior part of the abdominal cavity.
BIBLIOGRAPHY.
(88) Knock. "Die Beschr. d. Reise z. Wolga Behufs d.
Sterlettbefruchtung." _Bull. Soc. Nat._ Moscow, 1871.
(89) A. Kowalevsky, Ph. Owsjannikoff, and N. Wagner. "Die Entwick. d.
Störe." Vorläuf. Mittheilung. _Mélanges Biologiques tirés du Bulletin
d. l'Acad. Imp. St Pétersbourg_, Vol. VII. 1870.
(90) W. Salensky. "Development of the Sterlet (Acipenser ruthenus)." 2
Parts. _Proceedings of the Society of Naturalists in the imperial
University of Kasan._ 1878 and 9 (Russian). Part I., abstracted in
Hoffmann and Schwalbe's _Jahresbericht_ for 1878.
(91) W. Salensky. "Zur Embryologie d. Ganoiden (Acipenser)."
_Zoologischer Anzeiger_, Vol. I., Nos. 11, 12, 13.
LEPIDOSTEUS[38].
[38] Alexander Agassiz was fortunate enough to succeed in
procuring and rearing a batch of eggs of this interesting form.
He has given an adequate account of the external characters of
the post-embryonic stages, and very liberally placed his
preserved material of the stages both before and after hatching
at Prof. W. K. Parker's and my disposal. The account of the
stages prior to hatching is the result of investigations carried
on by Professor Parker's son, Mr W. N. Parker, and myself on the
material supplied to us by Agassiz. This material was not very
satisfactorily preserved, but I trust that our results are not
without some interest.
The ova of Lepidosteus are spherical bodies of about 3 mm. in
diameter. They are invested by a tough double membrane, composed of
(1) an outer layer of somewhat pyriform bodies, radiately arranged,
which appear to be the remains of the follicular cells; and (2) of an
inner zona radiata, the outer part of which is radiately striated,
while the inner part is homogeneous.
[FIG. 58. SURFACE VIEW OF THE OVUM OF LEPIDOSTEUS WITH THE MEMBRANES
REMOVED ON THE THIRD DAY AFTER IMPREGNATION.]
The segmentation, as in the Sturgeon, is complete, but approaches
closely the meroblastic type. It commences with a vertical furrow at
the animal pole, extending through about one-fifth of the
circumference. Before this furrow has proceeded further a second
furrow is formed at right angles to it. The next stages have not been
observed, but on the third day after impregnation (fig. 58), the
animal pole is completely divided into small segments, which form a
disc similar to the blastoderm of meroblastic ova; while the
vegetative pole, which subsequently forms a large yolk-sack, is
divided by a few vertical furrows, four of which nearly meet at the
pole opposite the blastoderm. The majority of the vertical furrows
extend only a short way from the edge of the small spheres, and are
partially intercepted by imperfect equatorial furrows.
The stages immediately following the segmentation are still unknown,
and in the next stage satisfactorily observed, on the fifth day after
impregnation, the body of the embryo is distinctly differentiated. The
lower pole of the ovum is then formed of a mass in which no traces of
segments or segmentation furrows can be detected.
The embryo (fig. 59) has a dumbbell-shaped outline, and is composed of
(1) an outer area, with some resemblance to the area pellucida of an
avian embryo, forming the lateral part of the body; and (2) a central
portion consisting of the vertebral plates and medullary plate. The
medullary plate is dilated in front to form the brain (_br_). Two
lateral swellings in the brain are the commencing optic vesicles. The
caudal extremity of the embryo is somewhat swollen.
[FIG. 59. SURFACE VIEW OF A LEPIDOSTEUS EMBRYO ON THE FIFTH DAY
AFTER IMPREGNATION.
_br._ dilated extremity of medullary plate which forms the rudiment
of the brain.]
Sections of this stage (fig. 60) are interesting as shewing a
remarkable resemblance between Lepidosteus and Teleostei.
The three layers are fully established. The epiblast (_ep_) is formed
of a thicker inner nervous stratum, and an outer flattened epidermic
stratum. Along the axial line there is a solid keel-like thickening of
the nervous layer of the epidermis, which projects towards the
hypoblast. This thickening (_MC_) is the medullary cord; and there is
no evidence of the epidermic layer being at this or any subsequent
period concerned in its formation (_vide_ chapter on Teleostei, p.
72). In the region of the brain the medullary cord is so thick that it
gives rise, as in Teleostei, to a projection of the whole body of the
embryo towards the yolk. Posteriorly it is flatter. The mesoblast
(_Me_) in the trunk has the form of two plates, which thin out
laterally. The hypoblast (_hy_) is a single layer of cells, and is
nowhere folded in to form a closed alimentary canal. The hypoblast is
separated from the neural cord by the notochord (_Ch_), which
throughout the greater part of the embryo is a distinct structure.
[FIG. 60. SECTION THROUGH AN EMBRYO OF LEPIDOSTEUS ON THE FIFTH DAY
AFTER IMPREGNATION.
_MC._ medullary cord; _Ep._ epiblast; _Me._ mesoblast; _hy._
hypoblast; _Ch._ notochord.]
In the region of the tail, the axial part of the hypoblast, the
notochord, and the neural cord fuse together, the fused part so formed
is the homologue of the neurenteric canal of other types. Quite at the
hinder end of the embryo the mesoblastic plates cease to be separable
from the axial structures between them.
In a somewhat later stage the embryo is considerably more elongated,
embracing half the circumference of the ovum. The brain is divided
into three distinct vesicles.
Anteriorly the neural cord has now become separated from the
epidermis. The whole of the thickened nervous layer of the epiblast
appears to remain united with the cerebrospinal cord, so that the
latter organ is covered dorsally by the epidermic layer of the
epiblast only. The nervous layer soon however grows in again from the
two sides.
Where the neural cord is separated from the epidermis, it is already
provided with a well-developed lumen. Posteriorly it remains in its
earlier condition.
In the region of the hind-brain traces of the auditory vesicles are
present in the form of slightly involuted thickenings of the nervous
layer of the epidermis.
[FIG. 61. EMBRYO OF LEPIDOSTEUS ON THE SIXTH DAY AFTER IMPREGNATION.
_op._ optic vesicles; _br.c._ branchial clefts (?); _s.d._ segmental
duct.
N.B. The branchial clefts and segmental duct are somewhat too
prominent.]
The mesoblast of the trunk is divided anteriorly into splanchnic and
somatic layers.
In the next stage, on the sixth day after impregnation (fig. 61),
there is a great advance in development. The embryo is considerably
longer, and a great number of mesoblastic somites are visible. The
body is now laterally compressed and raised from the yolk.
The region of the head is more distinct, and laterally two streaks are
visible (_br.c_), which, by comparison with the Sturgeon, would seem
to be the two first visceral clefts[39]: they are not yet perforated.
In the lateral regions of the trunk the two segmental ducts are
visible in surface views (fig. 61, _sd_) occupying the same situation
as in the Sturgeon. Their position in section is shewn in fig. 62,
_sg_.
[39] I have as yet been unable to make out these structures in
section.
[FIG. 62. SECTION THROUGH THE TRUNK OF A LEPIDOSTEUS EMBRYO ON THE
SIXTH DAY AFTER IMPREGNATION.
_mc._ medullary cord; _ms._ mesoblast; _sg._ segmental duct; _ch._
notochord; _x._ subnotochordal rod; _hy._ hypoblast.]
With reference to the features in development, visible in sections, a
few points may be alluded to.
The optic vesicles are very prominent outgrowths of the brain, but are
still solid, though the anterior cerebral vesicle has a well-developed
lumen. The auditory vesicles are now deep pits of the nervous layer of
the epiblast, the openings of which are covered by the epidermic
layer. They are shewn for a slightly later stage in fig. 63 (_au.v_).
There is now present a subnotochordal rod, which develops as in other
types from a thickening of the hypoblast (fig. 62, _x_).
[FIG. 63. SECTION THROUGH THE HEAD OF A LEPIDOSTEUS EMBRYO ON THE
SIXTH DAY AFTER IMPREGNATION.
_au.v._ auditory vesicle; _au.n._ auditory nerve; _ch._ notochord;
_hy._ hypoblast.]
In an embryo of the seventh day after impregnation, the features of
the preceding stage become generally more pronounced.
The optic vesicles are now provided with a lumen (fig. 64), and have
approached close to the epidermis. Adjoining them a thickening (_l_)
of _the nervous layer_ of the epidermis has appeared, which will form
the lens. The cephalic extremity of the segmental duct, which, as
shewn in fig. 61, is bent inwards towards the middle line, has now
become slightly convoluted, and forms the rudiment of a pronephros
(head-kidney).
[FIG. 64. SECTION THROUGH THE FRONT PART OF THE HEAD OF A
LEPIDOSTEUS EMBRYO ON THE SEVENTH DAY AFTER IMPREGNATION.
_al._ alimentary tract; _fb._ thalamencephalon; _l._ lens of eye;
_op.v._ optic vesicle. The mesoblast is not represented.]
During the next few days the folding off of the embryo from the yolk
commences, and proceeds till the embryo acquires the form represented
in fig. 65.
Both the head and tail are quite free from the yolk; and the embryo
presents a general resemblance to that of a Teleostean.
On the ventral surface of the front of the head there is a disc (figs.
65, 66, _sd_), which is beset with a number of processes, formed as
thickenings of the epiblast. As shewn by Agassiz, these eventually
become short suctorial papillæ[40]. Immediately behind this disc is
placed a narrow depression which forms the rudiment of the mouth.
[40] These papillæ are very probably sensitive structures; but I
have not yet investigated their histological characters.
The olfactory pits are now developed, and are placed near the front of
the head.
A great advance has taken place in the development of the visceral
clefts and arches. The oral region is bounded behind by a well-marked
mandibular arch, which is separated by a shallow depression from a
still more prominent hyoid arch (fig. 65, _hy_). Between the hyoid and
mandibular arches a double lamella of hypoblast, which represents the
hyomandibular cleft, is continued from the throat to the external
skin, but does not, at this stage at any rate, contain a lumen.
The hyoid arch is prolonged backwards into a considerable opercular
fold, which to a great extent overshadows the branchial clefts behind.
The hyobranchial cleft is widely open.
Behind the hyobranchial cleft are four pouches of the throat on each
side, not yet open to the exterior. They are the rudiments of the four
branchial clefts of the adult.
The trunk has the usual compressed piscine form, and there is a
well-developed dorsal fin continuous round the end of the tail, with a
ventral fin. There is no trace of the paired fins.
The anterior and posterior portions of the alimentary tract are closed
in, but the middle region is still open to the yolk. The circulation
is now fully established, and the vessels present the usual vertebrate
arrangement. There is a large subintestinal vein.
[FIG. 65. EMBRYO OF LEPIDOSTEUS SHORTLY BEFORE HATCHING.
_ol._ olfactory pit; _sd._ suctorial disc; _hy._ hyoid arch.]
The first of Agassiz' embryos was hatched about ten days after
impregnation. The young fish on hatching immediately used its
suctorial disc to attach itself to the sides of the vessel in which it
was placed.
[FIG. 66. VENTRAL VIEW OF THE HEAD OF A LEPIDOSTEUS EMBRYO SHORTLY
BEFORE HATCHING, TO SHEW THE LARGE SUCTORIAL DISC.
_m._ mouth; _op._ eye; _s.d._ suctorial disc.]
The general form of Lepidosteus shortly after hatching is shewn in
fig. 67. On the ventral part of the front of the head is placed the
large suctorial disc. At the side of the head are seen the olfactory
pit, the eye and the auditory vesicle; while the projecting vesicle of
the mid-brain is very prominent above. Behind the mouth follow the
visceral arches. The mandibular arch (_md_) is placed on the hinder
border of the mouth, and is separated by a deep groove from the hyoid
arch (_hy_). This groove is connected with the hyomandibular cleft,
but I have not determined whether it is now perforated. The posterior
border of the hyoid arch is prolonged into an opercular fold. Behind
the hyoid arch are seen the true branchial arches.
[FIG. 67. LARVA OF LEPIDOSTEUS SHORTLY AFTER HATCHING. (After
Parker.)
_ol._ olfactory pit; _op._ optic vesicle; _au.v._ auditory vesicle;
_mb._ mid-brain; _sd._ suctorial disc; _md._ mandibular arch; _hy._
hyoid arch with operculum; _br._ branchial arches; _an._ anus.]
There is still a continuous dorso-ventral fin, in which there are as
yet no fin-rays, and the anterior paired fins are present.
The yolk-sack is very large, but its communication with the alimentary
canal is confined to a narrow vitelline duct, which opens into the
commencement of the intestine _immediately behind_ the duct of the
liver, which is now a compact gland. The yolk in Lepidosteus thus
behaves very differently from that in the Sturgeon. In the first place
it forms a special external yolk-sack, instead of an internal
dilatation of part of the alimentary tract; and in the second place it
is placed behind instead of in front of the liver.
I failed to find any trace of a pancreas. There is however, _opening
on the dorsal side of the throat_, a well-developed appendage
continued backwards beyond the level of the commencement of the
intestine. This appendage is no doubt the air-bladder.
In the course of the further growth of the young Lepidosteus, the
yolk-sack is rapidly absorbed, and has all but disappeared after three
weeks. A rich development of pigment early takes place; and the
pigment is specially deposited on the parts of the embryonic fin which
will develop into the permanent fins.
The notochord in the tail bends slightly upwards, and by the special
development of a caudal lobe an externally heterocercal tail like that
of Acipenser is established. The ventral paired fins are first visible
after about the end of the third week, and by this time the operculum
has grown considerably, and the gills have become well developed.
The most remarkable changes in the later periods are those of the
mouth.
[FIG. 68. HEAD OF AN ADVANCED LARVA OF LEPIDOSTEUS. (After Parker.)
_ol._ openings of the olfactory pit; _sd._ remains of the larval
suctorial disc.]
The upper and lower jaws become gradually prolonged, till they
eventually form a snout; while at the end of the upper jaw is placed
the suctorial disc, which is now considerably reduced in size (fig.
68, _sd_). The "fleshy globular termination of the upper jaw of the
adult Lepidosteus is the remnant of this embryonic sucking disc."
(Agassiz, No. 92.)
The fin-rays become formed as in Teleostei, and parts of the
continuous embryonic fin gradually undergo atrophy. The dorsal limb of
the embryonic tail, as has been shewn by Wilder, is absorbed in
precisely the same manner as in Teleostei, leaving the ventral lobe to
form the whole of the permanent tail-fin.
BIBLIOGRAPHY.
(92) Al. Agassiz. "The development of Lepidosteus." _Proc. Amer. Acad.
of Arts and Sciences_, Vol. XIII. 1878.
_General observations on the Embryology of the Ganoids._
The very heterogeneous character of the Ganoid group is clearly shewn
both in its embryology and its anatomy. The two known types of
formation of the central nervous system are exemplified in the two
species which have been studied, and these two species, though in
accord in having a holoblastic segmentation, yet differ in other
important features of development, such as the position of the yolk
etc. Both types exhibit Teleostean affinities in the character of the
pronephros; but as might have been anticipated Lepidosteus presents in
the origin of the nervous system, the relations of the hypoblast, and
other characters, closer approximations to the Teleostei than does
Acipenser. There are no very prominent Amphibian characters in the
development of either type, other than a general similarity in the
segmentation and formation of the layers. In the young of Polypterus
an interesting amphibian and dipnoid character is found in the
presence of a pair of true external gills covered by epiblast. These
gills are attached at the hinder end of the operculum, and receive
their blood from the hyoid arterial arch[41]. In the peculiar
suctorial disc of Lepidosteus, and in the more or less similar
structure in the Sturgeon, these fishes retain, I believe, a very
primitive vertebrate organ, which has disappeared in the adult state
of almost all the Vertebrata; but it is probable that further
investigations will shew that the Teleostei, and especially the
Siluroids, are not without traces of a similar structure.
[41] Vide Steindachner, _Polypterus Lapradei_, &c., and
Hyrtl, "Ueber d. Blutgefässe, &c." _Sitz. Wiener Akad._,
Vol. LX.
CHAPTER VII.
AMPHIBIA[42].
[42] The following classification of the Amphibia is employed in
the present chapter:
I. Anura. {AGLOSSA.
{PHANEROGLOSSA.
{PERENNIBRANCHIATA {Trachystomata.
{ {Proteidæ.
II. Urodela. {CADUCIBRANCHIATA {Amphiumidæ.
{ {Menopomidæ.
{MYCTODERA {Amblystomidæ.
{Salamandridæ.
III. Gymnophiona.
The eggs of most Amphibia[43] are laid in water. They are smallish
nearly spherical bodies, and in the majority of known Anura (all the
European species), and in many Urodela (Amblystoma, Axolotl, though
not in the common Newt) part of the surface is dark or black, owing to
the presence of a superficial layer of pigment, while the remainder is
unpigmented. The pigmented part is at the upper pole of the egg, and
contains the germinal vesicle till the time of its atrophy; and the
yolk-granules in it are smaller than those in the unpigmented part.
The ovum is closely surrounded by a vitelline membrane[44], and
receives, in its passage down the oviduct, a gelatinous investment of
varying structure.
[43] I am under great obligations to Mr Parker for having kindly
supplied me, in answer to my questions, with a large amount of
valuable information on the development of the Amphibia.
[44] Within the vitelline membrane there appears to be present,
in the Anura at any rate, a very delicate membrane closely
applied to the yolk.
In the Anura the eggs are fertilized as they leave the oviduct. In
some of the Urodela the mode of fertilization is still imperfectly
understood. In Salamanders and probably Newts it is internal[45]; but
in Amblystoma punctatum (Clark, No. 98), the male deposits the semen
in the water. The eggs are laid by the Anura in masses or strings. By
Newts they are deposited singly in the angle of a bent blade of grass
or leaf of a water-plant, and by Amblystoma punctatum in masses
containing from four eggs to two hundred. Salamandra atra and
Salamandra maculosa are viviparous. The period of gestation for the
latter species lasts a whole year.
[45] Allen Thomson informs me that he has watched the process of
fertilization in the Newt, and that the male deposits the semen
in the water close to the female. From the water it seems to
enter the female generative aperture. Von Siebold has shewn that
there is present in female Newts and Salamanders a spermatic
bursa. In this bursa the spermatozoa long (three months) retain
their vitality in some Salamanders. Various peculiarities in the
gestation are to be explained by this fact.
A good many exceptions to the above general statements have been
recorded[46].
[46] For a summary of these and the literature of the subject
_vide_ "Amphibia," by C. K. Hoffmann, in Bronn's _Classen und
Ordnungen d. Thier-reichs_.
In Notodelphis ovipara the eggs are transported (by the male?) into a
peculiar dorsal pouch of the skin of the female, which has an anterior
opening, but is continued backwards into a pair of diverticula. The
eggs are very large, and in this pouch, which they enormously distend,
they undergo their development. A more or less similar pouch is found
in Nototrema marsupiatum.
In the Surinam toad (Pipa dorsigera) the eggs are placed by the male
on the back of the female. A peculiar pocket of skin becomes developed
round each egg, the open end of which is covered by a gelatinous
operculum. The larvæ are hatched, and actually undergo their
metamorphosis, in these pockets. The female during this period lives
in water. Pipa Americana (if specifically distinct from P. dorsigera)
presents nearly the same peculiarities. The female of a tree frog of
Ceylon (Polypedates reticulatus) carries the eggs attached to the
abdomen.
Rhinoderma Darwinii[47] behaves like some of the Siluroid fishes, in
that the male carries the eggs during their development in an
enormously developed laryngeal pouch.
[47] _Vide_ Spengel, "Die Fortpflanzung des Rhinoderma Darwinii."
_Zeit. f. wiss. Zool._, Bd. XXIX., 1877. This paper contains a
translation of a note by Jiminez de la Espada on the development
of the species.
Some Anura do not lay their eggs in water. Chiromantis Guineensis
attaches them to the leaves of trees; and Cystignathus mystacius lays
them in holes near ponds, which may become filled with water after
heavy rains.
The eggs of Hylodes Martinicensis are laid under dead leaves in moist
situations.
_Formation of the layers._
Anura. The formation of the germinal layers has so far only been
studied in some Anura and in the Newt. The following description
applies to the Anura, and I have called attention, at the end of the
section, to the points in which the Newt is peculiar.
The segmentation of the Frog's ovum has already been described (Vol.
II. pp. 95-7), but I may remind the reader that the segmentation (fig.
69) results in the formation of a vesicle, the cavity of which is
situated excentrically; the roof of the cavity being much thinner than
the floor. The cavity is the segmentation cavity. The roof is formed
of two or three layers of smallish pigmented cells, and the floor of
large cells, which form the greater part of the ovum. These large
cells, which are part of the primitive hypoblast, will be spoken of in
the sequel as yolk-cells: they are equivalent to the food-yolk of the
majority of vertebrate ova.
[FIG. 69. SEGMENTATION OF COMMON FROG. RANA TEMPORARIA.
(After Ecker.)
The numbers above the figures refer to the number of segments at the
stage figured.]
The cells forming the roof of the cavity pass without any sharp
boundary into the yolk-cells, there being at the junction of the two a
number of cells of an intermediate character. The cells both of the
roof and the floor continue to increase in number, and those of the
roof become divided into two distinct strata (fig. 70, _ep_).
The upper of these is formed of a single row of somewhat cubical
cells, and the lower of several rows of more rounded cells. Both of
these strata eventually become the epiblast, of which they form the
epidermic and nervous layers. The roof of the segmentation cavity
appears therefore to be entirely constituted of epiblast.
The next changes which take place lead (1) to the formation of the
mesenteron[48], and (2) to the enclosure of the yolk-cells by the
epiblast.
[48] Since the body cavity is not developed as diverticula from
the cavity of invagination, the latter cavity may conveniently be
called the mesenteron and not the archenteron.
The mesenteron is formed as in Petromyzon and Lepidosteus by an
unsymmetrical form of invagination. The invagination first commences
by an inflection of the epiblast-cells for a small arc on the
equatorial line which marks the junction between the epiblastic cells
and the yolk-cells (fig. 70, _x_).
The inflected cells become continuous with the adjoining cells; and
the region where the inflection is formed constitutes a kind of lip,
below which a slit-like cavity is soon established. This lip is
equivalent to the embryonic rim of the Elasmobranch blastoderm, and
the cavity beneath it is the rudiment of the mesenteron.
[FIG. 70. SECTION THROUGH FROG'S OVUM AT THE CLOSE OF SEGMENTATION.
(After Götte.)
_sg._ segmentation cavity; _ll._ large yolk-containing cells; _ep._
small cells at formative pole (epiblast); _x._ point of inflection
of epiblast; _y._ small cells close to junction of the epiblast and
yolk.]
The mesenteron now rapidly extends by the invagination of the cells on
its dorsal side. These cells grow inwards towards the segmentation
cavity as a layer of cells several rows deep. At its inner end, this
layer is continuous with the yolk-cells; and is divided into two
strata (fig. 71 A), viz. (1) a stratum of several rows of cells
adjoining the epiblast, which becomes the mesoblast (_m_), and (2) a
stratum of a single row of more columnar cells lining the cavity of
the mesenteron, which forms the hypoblast (_hy_). The growth inwards
of the dorsal wall of the mesenteron is no doubt in part a true
invagination, but it seems probable that it is also due in a large
measure to an actual differentiation of yolk-cells along the line of
growth. The mesenteron is at first a simple slit between the yolk and
the hypoblast (fig. 71 A), but as the involution of the hypoblast and
mesoblast extends further inwards, this slit enlarges, especially at
its inner end, into a considerable cavity; the blind end of which is
separated by a narrow layer of yolk-cells from the segmentation cavity
(fig. 71 B).
In the course of the involution, the segmentation cavity becomes
gradually pushed to one side and finally obliterated. Before
obliteration, it appears in some forms (Pelobates fuscus) to become
completely enclosed in the yolk-cells.
[FIG. 71. DIAGRAMMATIC LONGITUDINAL SECTIONS THROUGH THE EMBRYO OF A
FROG AT TWO STAGES, TO SHEW THE FORMATION OF THE GERMINAL LAYERS.
(Modified from Götte.)
_ep._ epiblast; _m._ dorsal mesoblast; _m´._ ventral mesoblast;
_hy._ hypoblast; _yk._ yolk; _x._ point of junction of the epiblast
and hypoblast at the dorsal side of the blastopore; _al._
mesenteron; _sg._ segmentation cavity.]
While the invagination to form the mesenteron takes place as above
described, the enclosure of the yolk has been rapidly proceeding. It
is effected by the epiblast growing over the yolk at all points of its
circumference. The nature of the growth is however very different at
the embryonic rim and elsewhere. At the embryonic rim it takes place
by the simple growth of the rim, so that the point _x_ in figs. 70 and
71 is carried further and further over the surface of the yolk.
Elsewhere the epiblast at first extends over the yolk as in a typical
epibolic gastrula, without being inflected to form a definite lip.
While a considerable patch of yolk is still left uncovered, the whole
of the edge of the epiblast becomes however inflected, as at the
embryonic rim (fig. 71 A); and a circular blastopore is established,
round the whole edge of which the epiblast and intermediate cells are
continuous.
From the ventral lip of the blastopore the mesoblast (fig. 71, _m´_),
derived from the small intermediate cells, grows inwards till it comes
to the segmentation cavity; the growth being not so much due to an
actual invagination of cells at the lip of the blastopore, as to a
differentiation of yolk-cells _in situ_. Shortly after the stage
represented in fig. 71 B, the plug of yolk, which fills up the opening
of the blastopore, disappears, and the mesenteron communicates freely
with the exterior by a small circular blastopore (fig. 73). The
position of the blastopore is the same as in other types, viz. at the
hinder end of the embryo.
By this stage the three layers of the embryo are definitely
established. The epiblast, consisting from the first of two strata,
arises from the small cells forming the roof of the segmentation-cavity.
It becomes continuous at the lip of the blastopore with cells
intermediate in size between the cells of which it is formed and the
yolk-cells. These latter, increasing in number by additions from the
yolk-cells, give rise to the mesoblast and to part of the hypoblast;
while to the latter layer the yolk-cells, as mentioned above, must
also be considered as appertaining. Their history will be dealt with
in treating of the general fate of the hypoblast.
Urodela. The early stages of the development of the Newt have been
adequately investigated by Scott and Osborn (No. 114). The
segmentation and formation of the layers is in the main the same as in
the Frog. The ovum is without black pigment. There is a typical
unsymmetrical invagination, but the dorsal lip of the blastopore is
somewhat thickened. The most striking feature in which the Newt
differs from the Frog is the fact that _the epiblast is at first
constituted of a single layer of cells_ (fig. 75, _ep_). The roof of
the segmentation cavity is constituted, during the later stages of
segmentation, of several rows of cells (Bambeke, No. 95), but
subsequently it would appear to be formed of a single row of cells
only (Scott and Osborn, No. 114).
_General history of the layers._
Epiblast: Anura. At the completion of the invagination the epiblast
forms a continuous layer enclosing the whole ovum, and constituted
throughout of two strata. The formation of the medullary canal
commences by the nervous layer along the axial dorsal line becoming
thickened, and giving rise to a somewhat pyriform medullary plate, the
sides of which form the projecting medullary folds (fig. 77 A). The
medullary plate is thickened at the two sides, and is grooved in the
median line by a delicate furrow (fig. 72, _r_). The dilated extremity
of the medullary plate, situated at the end of the embryo opposite the
blastopore, is the cerebral part of the plate, and the remainder the
spinal. The medullary folds bend upwards, and finally meet above,
enclosing a central cerebrospinal canal (fig. 74). The point at which
they first meet is nearly at the junction of the brain and spinal
cord, and from this point their junction extends backwards and
forwards; but the whole process is so rapid that the closure of the
medullary canal for its whole length is effected nearly
simultaneously. In front the medullary canal ends blindly, but behind
it opens freely into the still persisting blastopore, with the lips of
which the medullary folds become, as in other types, continuous. Fig.
73 represents a longitudinal section through an embryo, shortly after
the closure of the medullary canal (_nc_); the opening of which into
the blastopore (_x_) is clearly seen.
[FIG. 72. TRANSVERSE SECTION THROUGH THE POSTERIOR CEPHALIC REGION
OF AN EARLY EMBRYO OF BOMBINATOR. (After Götte.)
_l._ medullary groove; _r._ axial furrow in the medullary groove;
_h._ nervous layer of epidermis; _as._ outer portion of vertebral
plate; _is._ inner portion of vertebral plate; _s._ lateral plate of
mesoblast; _g._ notochord; _e._ hypoblast.]
On the closure of the medullary canal, its walls become separated from
the external epiblast, which extends above it as a continuous layer.
In the formation of the central nervous system both strata of the
epiblast have a share, though the main mass is derived from the
nervous layer. After the central nervous tube has become separated
from the external skin, the two layers forming it fuse together; but
there can be but little doubt that at a later period the epidermic
layer separates itself again as the central epithelium of the nervous
system.
Both the nervous and epidermic strata have a share in forming the
general epiblast; and though eventually they partially fuse together
yet the horny layer of the adult epidermis, where such can be
distinguished, is probably derived from the epidermic layer of the
embryo, and the mucous layer of the epidermis from the embryonic
nervous layer.
[FIG. 73. DIAGRAMMATIC LONGITUDINAL SECTION OF THE EMBRYO OF A FROG.
(Modified from Götte.)
_nc._ neural canal; _x._ point of junction of epiblast and hypoblast
at the dorsal lip of the blastopore; _al._ alimentary tract; _yk._
yolk-cells; _m._ mesoblast. For the sake of simplicity the epiblast
is represented as if composed of a single row of cells.]
In the formation of the organs of sense the nervous layer shews itself
throughout as the active layer. The lens of the eye and the auditory
sack are derived exclusively from it, the latter having no external
opening. The nervous layer also plays the more important part in the
formation of the olfactory sack.
The outer layer of epiblast-cells becomes ciliated after the close of
the segmentation, but the cilia gradually disappear on the formation
of the internal gills. The cilia cause a slow rotatory movement of the
embryo within the egg, and probably assist in the respiration after it
is hatched. They are especially developed on the external gills.
Urodela. In the Newt (Scott and Osborn, No. 114) the medullary plate
becomes established, while the epiblast is still formed of a single
row of cells; and it is not till after the closure of the neural
groove that any distinction is observable between the epithelium of
the central canal, and the remaining cells of the cerebrospinal cord
(fig. 75).
Before the closure of the medullary folds the lateral epiblast becomes
divided into the two strata present from the first in the Frog; and in
the subsequent development the inner layer behaves as the active
layer, precisely as in the Anura.
The mesoblast and notochord: Anura. After the disappearance of the
segmentation cavity, the mesoblast is described by most observers,
including Götte, as forming a continuous sheet round the ovum,
underneath the epiblast. The first important differentiations in it
take place, as in the case of the epiblast, in the axial dorsal line.
Along this line a central cord of the mesoblast becomes separated from
the two lateral sheets to form the notochord. Calberla states,
however, that when the mesoblast is distinctly separated from the
hypoblast it does not form a continuous sheet, but two sheets one on
each side, between which is placed a ridge of cells continuous with
the hypoblastic sheet. This ridge subsequently becomes separated from
the hypoblast as the notochord. Against this view Götte has recently
strongly protested, and given a series of careful representations of
his sections which certainly support his original account.
My own observations are in favour of Calberla's statement, and so far
as I can determine from my sections the mesoblast never appears as a
perfectly continuous sheet, but is always deficient in the dorsal
median line. My observations are unfortunately not founded on a
sufficient series of sections to settle the point definitely.
[FIG. 74. SECTION THROUGH THE ANTERIOR PART OF THE TRUNK OF A YOUNG
EMBRYO OF BOMBINATOR. (After Götte.)
_as´´´._ medulla oblongata; _is^x._ splanchnopleure; _as^x._
somatopleure in the vertebral part of the mesoblastic plate; _s._
lateral plate of mesoblast; _f._ throat; _e._ passage of epithelial
cells into yolk-cells; _d._ yolk-cells; _r._ dorsal groove along the
line of junction of the medullary folds.]
After the formation of the notochord (fig. 72), the mesoblast may be
regarded as consisting of two lateral plates, continuous ventrally,
but separated in the median dorsal line. By the division of the dorsal
parts of these plates into segments, which commences in the region of
the neck and thence extends backwards, the mesoblast of the trunk
becomes divided into a vertebral portion, cleft into separate somites,
and a lateral unsegmented portion (fig. 74).
The history of these two parts and of the mesoblast is generally the
same as in Elasmobranchs.
The mesoblast in the head becomes, according to Götte, divided into
four segments, equivalent to the trunk somites. Owing to a confusion
into which Götte has fallen from not recognizing the epiblastic origin
of the cranial nerves, his statements on this head must, I think, be
accepted with considerable reserve; but some part of his segments
appears to correspond with the head-cavities of Elasmobranchii.
Urodela. Scott and Osborn (No. 114) have shewn that in the Newt the
mesoblast (fig. 75) is formed of two lateral plates, split off from
the hypoblast, and that the ventral growth of these plates is largely
effected by the conversion of yolk-cells into mesoblast-cells. They
have further shewn that the notochord is formed of an _axial portion
of the hypoblast_, as in the types already considered (fig. 75). The
body cavity is continued into the region of the head; and the
mesoblast lining the cephalic section of the body cavity is divided
into the same number of head cavities as in Elasmobranchii, viz. one
in front of the mouth, and one in the mandibular and one in each of
the following arches.
The hypoblast. There are no important points of difference in the
relations of the hypoblast between the Anura and Urodela. The
mesenteron, at the stage represented in fig. 73, forms a wide cavity
lined dorsally by a layer of invaginated hypoblast, and ventrally by
the yolk-cells. The hypoblast is continuous laterally and in front
with the yolk-cells (figs. 72, 74 and 75). At an earlier stage, when
the mesenteron has a less definite form, such a continuity between the
true hypoblast and the yolk-cells does not exist at the sides of the
cavity.
[FIG. 75. TRANSVERSE SECTION THROUGH THE CEPHALIC REGION OF A YOUNG
NEWT EMBRYO. (After Scott and Osborn.)
_In.hy._ invaginated hypoblast, the dorsal part of which will form
the notochord; _ep._ epiblast of neural plate; _sp._
splanchnopleure; _al._ alimentary tract; _yk._ and _Y.hy._
yolk-cells.]
The definite closing in of the mesenteron by the true hypoblast-cells
commences in front and behind, and takes place last of all in the
middle (fig. 76). In front this process takes place with the greatest
rapidity. The cells of the yolk-floor become continuously
differentiated into hypoblast-cells, and very soon the whole of the
front end becomes completely lined by true hypoblastic cells, while
the yolk-cells become confined to the floor of the middle part.
The front portion of the mesenteron gives rise to the oesophagus,
stomach and duodenum. Close to its hinder boundary there appears a
ventral outgrowth, which is the commencement of the hepatic
diverticulum (fig. 76, _l_). The yolk is thus post-hepatic, as in
Vertebrates generally.
The stomodæum is formed comparatively late by an epiblastic
invagination (fig. 76, _m_).
[FIG. 76. LONGITUDINAL SECTION THROUGH AN ADVANCED EMBRYO OF
BOMBINATOR. (After Götte.)
_m._ mouth; _an._ anus; _l._ liver; _ne._ neurenteric canal; _mc._
medullary canal; _ch._ notochord; _pn._ pineal gland.]
It should be noticed that the conversion of the yolk-cells into
hypoblast-cells to form the ventral wall of the anterior region of the
alimentary tract is a closely similar occurrence to the formation of
cells in the yolk-floor of the anterior part of the alimentary tract
in Elasmobranchii. This conversion is apparently denied by Götte, but
since I find cells in all stages of transition between yolk-cells and
hypoblast-cells I cannot doubt the fact of its occurrence.
At first, the mesenteron freely communicates with the exterior by the
opening of the blastopore. The lips of the blastopore gradually
approximate, and form a narrow passage on the dorsal side of which the
neural tube opens, as has already been described (fig. 73). The
external opening of this passage finally becomes obliterated, and the
passage itself is left as a narrow diverticulum leading from the hind
end of the mesenteron into the neural canal (fig. 76). It forms the
postanal gut, and gradually narrows and finally atrophies. At its
front border, on the ventral side, there may be seen a slight
ventrally directed diverticulum of the alimentary tract, which first
becomes visible at a somewhat earlier stage (fig. 73). This
diverticulum becomes longer and meets an invagination of the skin
(fig. 76, _an_), which arises in Rana temporaria at a somewhat earlier
period than represented by Götte in Bombinator. This epiblastic
invagination is the proctodæum, and an anal perforation eventually
appears at its upper extremity.
The differentiation of the hinder end of the præanal gut proceeds in
the same fashion as that of the front end, though somewhat later. It
gives rise to the cloacal and intestinal part of the alimentary tract.
From the ventral wall of the cloacal section, there grows out the
bifid allantoic bladder, which is probably homologous with the
allantois of the higher Vertebrata. After the differentiation of the
ventral wall of the fore and hind ends of the alimentary tract has
proceeded for a certain distance, the yolk only forms a floor for a
restricted median region of the alimentary cavity, which corresponds
to the umbilical canal of the Amniota. The true hypoblastic epithelium
then grows over the outer side of the yolk, which thus constitutes a
true, though small, and internal yolk-sack. The yolk-cells enclosed in
this sack become gradually absorbed, and the walls of the sack form
part of the intestine.
_General growth of the Embryo._
Anura. The pyriform medullary plate, already described, is the first
external indication of the embryo. This plate appears about the stage
represented in longitudinal section in fig. 71 B. The feature most
conspicuous in it at first is the axial groove. It soon becomes more
prominent (fig. 77 A), and ends behind at the blastopore (_bl_), the
lips of which are continuous with the two medullary folds. As the
sides of this plate bend upwards to form the closed medullary canal,
the embryo elongates itself and assumes a somewhat oval form. At the
same time the cranial flexure becomes apparent (fig. 73), and the
blastopore shortly afterwards becomes shut off from the exterior. The
embryo now continues to grow in length (fig. 77 B), and the mesoblast
becomes segmented. The somites are first formed in the neck, and are
added successively behind in the unsegmented posterior region of the
embryo. The hind end of the embryo grows out into a rounded
prominence, which rapidly elongates, and becomes a well-marked tail
entirely formed by the elongation of the postanal section of the body.
The whole body has a very decided dorsal flexure, the ventral surface
being convex. Fig. 78 represents an embryo of Bombinator in side view,
with the tail commencing to project. The longitudinal section (fig.
76) is taken through an embryo of about the same age. In the cephalic
region important changes have taken place. The cranial flexure has
become more marked, but is not so conspicuous a feature in the
Amphibia as in most other types, owing to the small size of the
cerebral rudiment. The mid-brain is shewn at fig. 78 _a_ forming the
termination of the long axis of the body, and the optic vesicles
(_a´_) are seen at its sides.
[FIG. 77. EMBRYOS OF THE COMMON FROG. (After Remak.)
A. Young stage represented enclosed in the egg-membrane. The
medullary plate is distinctly formed, but no part of the medullary
canal is closed. _bl._ blastopore.
B. Older embryo after the closure of the medullary canal. _oc._
optic vesicle. Behind the optic vesicle are seen two visceral
arches.]
[FIG. 78. LATERAL VIEW OF AN ADVANCED EMBRYO OF BOMBINATOR. (After
Götte.)
_a._ mid-brain, _a´._ eye; _b._ hind-brain; _d._ mandibular arch;
_d´._ Gasserian ganglion; _e._ hyoid arch; _e´._ first branchial
arch; _f._ seventh nerve; _f´._ glossopharyngeal and vagus nerve;
_g._ auditory vesicle; _i._ boundary between liver and yolk-sack;
_k._ suctorial disc; _l._ pericardial prominence; _m._ prominence
formed by the pronephros.]
The rudiments of the mandibular (_d_), hyoid (_e_), and first
branchial (_e´_) arches project as folds at the side of the head, but
the visceral clefts are not yet open. Rudiments of the proctodæum and
stomodæum have appeared, but neither of them as yet communicates with
the mesenteron. Below the hyoid arch is seen a peculiar disc (_k_)
which is an embryonic suctorial organ, formed of a plate of thickened
epiblast. There is a pair of these discs, one on each side, but only
one of them is shewn in the figure. At a later period they meet each
other in the middle line, though they separate again before their
final atrophy. They are found in the majority of the Anura, but are
absent according to Parker in the Aglossa (Pipa and Dactylethra (fig.
83)). They are probably remnants of the same primitive organs as the
suctorial disc of Lepidosteus.
[FIG. 79. TRANSVERSE SECTION THROUGH A VERY YOUNG TADPOLE OF
BOMBINATOR AT THE LEVEL OF THE ANTERIOR END OF THE YOLK-SACK. (After
Götte.)
_a._ fold of epiblast continuous with the dorsal fin; _is^x._ neural
cord; _m._ lateral muscle; _as^x._ outer layer of muscle-plate; _s._
lateral plate of mesoblast; _b._ mesentery; _u._ fold of the
peritoneal epithelium which forms the segmental duct; _f._
alimentary tract; _f´._ ventral diverticulum which becomes the
liver; _e._ junction of yolk-cells and hypoblast-cells; _d._
yolk-cells.]
The embryo continues to grow in length, while the tail becomes more
and more prominent, and becomes bent round to the side owing to the
confinement of the larva within the egg-membrane. At the front of the
head the olfactory pits become distinct. The stomodæum deepens, though
still remaining blind, and three fresh branchial arches become formed;
the last two being very imperfectly differentiated, and not visible
from the exterior. There are thus six arches in all, viz. the
mandibular, the hyoid and four branchial arches. Between the
mandibular and the hyoid, and between each of the following arches,
pouches of the mesenteron push their way towards the external skin. Of
these pouches there are five, there being no pouch behind the last
branchial arch. The first of these will form the hyomandibular cleft,
the second the hyobranchial, and the third, fourth and fifth the three
branchial clefts.
Although the pouches of the throat meet the external skin, an external
opening is not formed in them till after the larva is hatched. Before
this takes place there grow, in the majority of forms, from the outer
side of the first and second branchial arches small processes, each
forming the rudiment of an external gill; a similar rudiment is
formed, either before or after hatching, on the third arch; but the
fourth arch is without it (figs. 80 and 82).
These external gills, which differ fundamentally from the external
gills of Elasmobranchii in being covered by epiblast, soon elongate
and form branched ciliated processes floating freely in the medium
around the embryo (fig. 80).
Before hatching the excretory system begins to develop. The segmental
duct is formed as a fold of the somatic wall at the dorsal side of the
body cavity (fig. 79, _u_). Its anterior end alone remains open to the
body cavity, and gives rise to a pronephros with two or three
peritoneal openings, opposite to which a glomerulus is formed.
The mesonephros (permanent kidney of Amphibia) is formed as a series
of segmental tubes much later than the pronephros, during late larval
life. Its anterior end is situated some distance behind the
pronephros, and during its formation the pronephros atrophies.
The period of hatching varies in different larvæ, but in most cases,
at the time of its occurrence, the mouth has not yet become
perforated. The larva, familiarly known as a tadpole, is at first
enclosed in the detritus of the gelatinous egg envelopes. The tail, by
the development of a dorsal and ventral fin, very soon becomes a
powerful swimming organ. Growth, during the period before the larva
begins to feed, is no doubt carried on at the expense of the yolk,
which is at this time enclosed within the mesenteron.
The mouth and anal perforations are not long in making their
appearance, and the tadpole is then able to feed. The gill slits also
become perforated, but the hyomandibular diverticulum in most species
never actually opens to the exterior, and in all cases becomes very
soon closed.
There can be but little doubt that the hyomandibular diverticulum
gives rise, as in the Amniota, to the Eustachian tube and tympanic
cavity, except when these are absent (_i.e._ Bombinatoridæ). Götte
holds however that these parts are derived from the hyobranchial
cleft, but his statements on this head, which would involve us in
great morphological difficulties, stand in direct contradiction to the
careful researches of Parker.
[FIG. 80. TADPOLES WITH EXTERNAL BRANCHIÆ. (From Huxley; after Ecker.)
A. Lateral view of a young tadpole.
B. Ventral view of a somewhat older tadpole.
_kb._ external branchiæ; _m._ mouth; _n._ nasal sack; _a._ eye; _o._
auditory vesicle; _z._ horny jaws; _s._ ventral sucker; _d._
opercular fold.
C. More advanced larva, in which the opercular fold has nearly
covered the branchiæ.
_s._ ventral sucker; _ks._ external branchiæ; _y._ rudiment of hind
limb.]
Shortly after hatching, there grows out from the hyoid arch on each
side an opercular fold of skin, which gradually covers over the
posterior branchial arches and the external gills (fig. 80 _d_). It
fuses with the skin at the upper part of the gill arches, and also
with that of the pericardial wall below them; but is free in the
middle, and so assists in forming a cavity, known as the branchial
cavity, in which the gills are placed. Each branchial cavity at first
opens by a separate widish pore behind (fig. 80), and in Dactylethra
both branchial apertures are preserved (Huxley). In the larva of
Bombinator, and it would seem also that of Alytes and Pelodytes, the
original widish openings of the two branchial chambers meet together
in the ventral line, and form a single branchial opening or spiracle.
In most other forms, _i.e._ Rana, Bufo, Pelobates, etc., the two
branchial chambers become united by a transverse canal, and the
opening of the right sack then vanishes, while that of the left
remains as the single unsymmetrical spiracle. In breathing the water
is taken in at the mouth, passes through the branchial clefts into the
branchial cavities, and is thence carried out by the spiracle.
Immediately after the formation of the branchial cavities, the
original external gills atrophy, but in their place fresh gills,
usually called internal gills, appear on the outer side of the middle
region of the four branchial arches.
There is a single row of these on the first and fourth branchial
arches, and two rows on the second and third. In addition to these
gills, which are vascular processes of the mesoblast, covered,
according to Götte, with an epiblastic (?) epithelium, branchial
processes appear on the hypoblastic walls of the three branchial
clefts. The last-named branchial processes would appear to be
homologous with the gills of Lampreys. In Dactylethra no other gills
but these are formed (Parker).
[FIG. 81. TADPOLE OF BOMBINATOR FROM THE VENTRAL SIDE, WITH THE
ABDOMINAL WALL REMOVED. (After Götte.)
Behind the mouth are placed the two suckers, and behind these are
seen the gills projecting through the spiracles.]
The mouth, even before the tadpole begins to feed, acquires a
transversely oval form (fig. 81), and becomes armed with provisional
structures in the form of a horny beak and teeth, which are in use
during larval life.
The beak is formed of a pair of horny plates moulded on the upper and
lower pairs of labial cartilages. The upper valve of the beak is the
larger of the two, and covers the lower. The beak is surrounded by a
projecting lip formed of a circular fold of skin, the free edge of
which is covered by papillæ. Between the papillæ and the beak rows of
horny teeth are placed on the inner surface of the lip. There are
usually two rows of these on the upper side, the inner one not
continuous across the middle line, and three or four rows on the lower
side, the inner one or two divided into two lateral parts.
As the tadpole attains its full development, the suctorial organs
behind the mouth gradually atrophy. The alimentary canal, which is
(fig. 81) at first short, rapidly elongates, and fills up with its
numerous coils the large body cavity. In the meantime, the lungs
develop as outgrowths from the oesophagus.
Various features in the anatomy of the Tadpole point to its being a
repetition of a primitive vertebrate type. The nearest living
representative of this type appears to be the Lamprey.
The resemblance between the mouths of the Tadpole and Lamprey is very
striking, and many of the peculiarities of the larval skull of the
Anura, especially the position of the Meckelian cartilages and the
subocular arch, perhaps find their parallel in the skull of the
Lamprey[49]. The internal hypoblastic gill-sacks of the Frog, with
their branchial processes, are probably equivalent to the gill-sacks
of the Lamprey[50]; and it is not impossible that the common posterior
openings of the gill-pouches in Myxine are equivalent to the
originally paired openings of the branchial sack of the Tadpole.
[49] _Vide_ Huxley, "Craniofacial apparatus of Petromyzon."
_Journ. of Anat. and Phys._ Vol. X. 1876. Huxley's views about
the Meckelian arch, etc., are plausible, but it seems probable
from Scott's observations that true branchial bars are not
developed in the Lamprey. How far this fact necessarily disproves
Huxley's views is still doubtful.
[50] Conf. Huxley and Götte.
The resemblances between the Lamprey and the Tadpole appear to me to
be sufficiently striking not to be merely the results of more or less
similar habits; but at the same time there are no grounds for
supposing that the Lamprey itself is closely related to an ancestral
form of the Amphibia. In dealing with the Ganoids and other types
arguments have been adduced to shew that there was a primitive
vertebrate stock provided with a perioral suctorial disc; and of this
stock the Cyclostomata are the degraded, but at the same time the
nearest living representatives. The resemblances between the Tadpole
and the Lamprey are probably due to both of them being descended from
this stock. The Ganoids, as we have seen, also shew traces of a
similar descent; and the resemblance between the larva of Dactylethra
(fig. 83), the Old Red Sandstone Ganoids[51] and Chimæra, probably
indicates that an extension of our knowledge will bring to light
further affinities between the primitive Ganoid and Holocephalous
stocks and the Amphibia.
[51] Cf. Parker (No. 107).
Metamorphosis. The change undergone by the Tadpole in its passage into
the Frog is so considerable as to deserve the name of a metamorphosis.
This metamorphosis essentially consists in the reduction and atrophy
of a series of provisional embryonic organs, and the appearance of
adult organs in their place. The stages of this metamorphosis are
shewn in fig. 82, 5, 6, 7, 8.
The two pairs of limbs appear nearly simultaneously as small buds; the
hinder pair at the junction of the tail and body (fig. 82, 5), and the
anterior pair concealed under the opercular membrane. The lungs
acquire a greater and greater importance, and both branchial and
pulmonary respirations go on together for some time.
[FIG. 82. TADPOLES AND YOUNG OF THE COMMON FROG. (From Mivart.)
1. Recently-hatched Tadpoles twice the natural size. 2. Tadpole with
external gills. 2_a_. Same enlarged. 3 and 4. Later stages after the
enclosure of the gills by the opercular membrane. 5. Stage with
well-developed hind-limbs visible. 6. Stage after the ecdysis, with
both pairs of limbs visible. 7. Stage after partial atrophy of the
tail. 8. Young Frog.]
When the adult organs are sufficiently developed an ecdysis takes
place, in which the gills are completely lost, the provisional horny
beak is thrown off, and the mouth loses its suctorial form. The eyes,
hitherto concealed under the skin, become exposed on the surface, and
the front limbs appear (fig. 82, 6). With these external changes
important internal modifications of the mouth, the vascular system,
and the visceral arches take place. A gradual atrophy of the tail,
commencing at the apex, next sets in, and results in the complete
absorption of this organ.
The long alimentary canal becomes shortened, and the, in the main,
herbivorous Tadpole gradually becomes converted into the carnivorous
Frog (fig. 82, 6, 7, 8).
The above description of the metamorphosis of the Frog applies fairly
to the majority of the Anura, but it is necessary to notice a few of
the more instructive divergences from the general type.
In the first place, several forms are known, which are hatched in the
condition of the adult. The exact amount of metamorphosis which these
forms pass through in the egg is still a matter of some doubt. Hylodes
Martinicensis is one of these forms. The larva no doubt acquires
within the egg a long tail; but while Bavay[52] states that it is
provided with external gills, which however are not covered by an
operculum, Peters[53] was unable to see any traces of such structures.
[52] _Annal. de Sciences Nat._, 5th Series, Vol. XVII., 1873.
[53] _Berlin. Monatsbericht_, 1876, p. 703, and _Nature_, April
5, 1877.
In Pipa Americana, and apparently in Pipa dorsigera also if a distinct
species, the larva leaves the cells on the back of the mother in a
condition closely resembling the adult. The embryos of both species
develop a long tail in the egg, which is absorbed before hatching, and
according to Wyman[54] P. Americana is also temporarily provided with
gills, which atrophy early.
[54] _Proceed. of Boston Nat. Hist. Society_, Vol. V., 1854.
The larva of Rhinoderma Darwinii is stated by Jiminez de la Espada to
be without external gills, and it appears to be hatched while still in
the laryngeal pouch of the male. In Nototrema marsupiatum the larvæ
are also stated to be without external gills.
Amongst the forms with remarkable developments Pseudis paradoxa
deserves especial mention, in that the tadpole of this form attains an
immensely greater bulk than the adult; a peculiarity which may be
simply a question of nutrition, or may perhaps be explained by
supposing that the larva resembles a real ancestral form, which was
much larger than the existing Frog.
Another form of perhaps still greater morphological interest is the
larva of Dactylethra. The chief peculiarities of this larva (fig. 83)
have been summarized by Parker (No. 107, p. 626), from whom I quote
the following passage:
_a._ "The mouth is not inferior in position, suctorial and small, but
is very wide like that of the 'Siluroids and Lophius;' has an
underhung lower jaw, an immensely long tentacle from each upper lip,
and possesses no trace of the primordial horny jaws of the ordinary
kind.
_b._ "In conformity with these characters the head is extremely flat
or depressed, instead of being high and thick.
_c._ "There are no claspers beneath the chin.
_d._ "The branchial orifice is not confined to the left side, but
exists on the right side also.
_e._ "The tail, like the skull, is remarkably chimæroid; it terminates
in a long thin pointed lash, and the whole caudal region is narrow and
elongated as compared with that of our ordinary Batrachian larvæ.
_f._ "The fore-limbs are not hidden beneath the opercular fold."
[FIG. 83. LARVA OF DACTYLETHRA. (After Parker.)]
Although most Anurous embryos are not provided with a sufficient
amount of yolk to give rise to a yolk-sack as an external appendage of
the embryo, yet in some forms a yolk-sack, nearly as large as that of
Teleostei, is developed. One of these forms, Alytes obstetricans,
belongs to a well-known European genus allied to Pelobates. The
embryos of Pipa dorsigera (Parker) are also provided with a very large
yolk-sack, round which they are coiled like a Teleostean embryo. A
large yolk-sack is also developed in the embryo of Pseudophryne
australis.
The actual complexity of the organization of different tadpoles, and
their relative size, as compared with the adult, vary considerably.
The tadpoles of Toads are the smallest, Pseudophryne australis
excelling in this respect; those of Pseudis are the largest known.
The external gills reach in certain forms, which are hatched in late
larval stages, a very great development. It seems however that this
development is due to these gills being especially required in the
stages before hatching. Thus in Alytes, in which the larva leaves the
egg in a stage after the loss of the external gills, these structures
reach in the egg a very great development. In Notodelphis ovipara, in
which the eggs are carried in a dorsal pouch of the mother, the
embryos are provided with long vesicular gills attached to the neck by
delicate threads. The fact (if confirmed) that some of the forms which
are not hatched till post-larval stages are without external gills,
probably indicates that there may be various contrivances for
embryonic respiration[55]; and that the external gills only attain a
great development in those instances in which respiration is mainly
carried on by their means. The external gills of Elasmobranchii are
probably, as stated in a previous chapter, examples of secondarily
developed structures, which have been produced by the same causes as
the enlarged gills of Alytes, Notodelphis, etc.
[55] In confirmation of this view it may be mentioned that in
Pipa Americana the tail appears to function as a respiratory
organ in the later stages of development (Peters).
Urodela. Up to the present time complete observations on the
development of the Urodela are confined to the Myctodera[56].
[56] The recent observations on this subject are those of Scott
and Osborn (No. 114) on Triton, of Bambeke (No. 95) on various
species of Triton and the Axolotl, and of Clark (No. 98) on
Amblystoma punctatum.
The early stages are in the main similar to those of the Anura. The
body of the embryo is, as pointed out by Scott and Osborn, ventrally
instead of dorsally flexed. The metamorphosis is much less complete
than in the Anura. The larva of Triton may be taken as typical. At
hatching, it is provided with a powerful swimming tail bearing a
well-developed fin: there are three pairs of gills placed on the three
anterior of the true branchial arches.
Between the hyoid and first branchial arch, and between the other
branchial arches, slits are developed, there being four slits in all.
At the period just before hatching, only three of these have made
their appearance. The hyomandibular cleft is not perforated. Stalked
suckers, of the same nature as the suckers of the Anura, are formed on
the ventral surface behind the mouth. A small opercular fold,
developed from the lower part of the hyoid arch, covers over the bases
of the gills. The suctorial mouth and the provisional horny beak of
the Anura have no counterpart in these larvæ. The skin is ciliated,
and the cilia cause a rotation in the egg. Even before hatching, a
small rudiment of the anterior pair of limbs is formed, but the
hind-limbs are not developed till a later stage, and the limbs do not
attain to any size till the larva is well advanced. In the course of
the subsequent metamorphosis lungs become developed, and a pulmonary
respiration takes the place of the branchial one. The branchial slits
at the same time close and the branchiæ atrophy.
The other types of Myctodera, so far investigated, agree fairly with
the Newt.
The larva of Amblystoma punctatum (fig. 84) is provided with two very
long processes (_s_), like the suctorial processes in Triton, placed
on the throat in front of the external gills. They are used to support
the larva when it sinks to the bottom, and have been called by Clarke
(No. 98) balancers. On the development of the limbs, these processes
drop off. The external gills atrophy about one hundred days after
hatching.
It might have been anticipated that the Axolotl, being a larval form
of Amblystoma, would agree in development with Amblystoma punctatum.
The conspicuous suctorial processes of the latter form are however
represented by the merest rudiments in the Axolotl.
[FIG. 84. LARVÆ OF AMBLYSTOMA PUNCTATUM. (After Clarke.)
_n._ nasal pit; _f._ oral invagination; _op._ eye; _s._ balancers;
_f.l._ front limb; _br._ branchiæ.]
The young of Salamandra maculata leave the uterus with external gills,
but those of the Alpine Salamander (Salamandra atra) are born in the
fully developed condition without gills. In the uterus they pass
through a metamorphosis, and are provided (in accordance with the
principle already laid down) with very long gill-filaments[57].
[57] Allen Thomson informs me that the crested Newt, Triton
cristatus, is in rare instances viviparous.
Salamandra atra has only two embryos, but there are originally a
larger number of eggs (Von Siebold), of which all but two fail to
develop, while their remains are used as pabulum by the two which
survive. Both species of Salamander have a sufficient quantity of
food-yolk to give rise to a yolk-sack.
Spelerpes only develops three post-hyoid arches, between which slits
are formed as in ordinary types. Menobranchus and Proteus agree with
Spelerpes in the number of post-hyoid arches.
One of the most remarkable recent discoveries with reference to the
metamorphosis of the Urodela was made by Dumeril[58]. He found that
some of the larvæ of the Axolotl, bred in the Jardin des Plantes, left
the water, and in the course of about a fortnight underwent a similar
metamorphosis to that of the Newt, and became converted into a form
agreeing in every particular with the American genus Amblystoma.
During this metamorphosis a pulmonary respiration takes the place of a
branchial one, the gills are lost, and the gill slits close. The tail
loses its fin and becomes rounded, the colour changes, and alterations
take place in the gums, teeth, and lower jaw.
[58] _Comptes Rendus_, 1870, p. 782.
Madame von Chauvin[59] was able, by gradually accustoming Axolotl
larvæ to breathe, artificially to cause them to undergo the above
metamorphosis.
[59] _Zeit. f. wiss. Zool._, Bd. XXVII. 1876.
It seems very possible, as suggested by Weismann[60], that the
existing Axolotls are really descendants of Amblystoma forms, which
have reverted to a lower stage. In favour of this possibility a very
interesting discovery of Filippi's[61] may be cited. He found in a
pond in a marsh near Andermat some examples of Triton alpestris,
which, though they had become sexually mature, still retained the
external gills and the other larval characters. Similar sexually
mature larval forms of Triton tæniatus have been described by Jullien.
These discoveries would seem to indicate that it might be possible
artificially to cause the Newt to revert to a perennibranchiate
condition.
[60] _Zeit. f. wiss. Zool._, Bd. XXV. sup. 1875.
[61] _Archivio per la Zoologia, l'Anatomia e la Fisiologia_, Vol.
1. Genoa, 1861. Conf. also Von Siebold, "Ueber die
geschlechtliche Entwicklung d. Urodelen-Larven." _Zeit. f. wiss.
Zool._, Bd. XXVIII., 1877.
Gymnophiona. The development of the Gymnophiona is almost unknown, but
it is certain that some larval forms are provided with a single
gill-cleft, while others have external gills.
A gill-cleft has been noticed in Epicrium glutinosum (Müller), and in
Coecilia oxyura. In Coecilia compressicauda, Peters (No. 108) was
unable to find any trace of a gill-cleft, but he observed in the larvæ
within the uterus two elongated vesicular gills.
BIBLIOGRAPHY.
_Amphibia._
(93) Ch. van Bambeke. "Recherches sur le développement du Pélobate
brun." _Mémoires couronnés, etc. de l'Acad. roy. de Belgique_, 1868.
(94) Ch. van Bambeke. "Recherches sur l'embryologie des Batraciens."
_Bulletin de l'Acad. roy. de Belgique_, 1875.
(95) Ch. van Bambeke. "Nouvelles recherches sur l'embryologie des
Batraciens." _Archives de Biologie_, Vol. 1. 1880.
(96) K. E. von Baer. "Die Metamorphose des Eies der Batrachier."
Müller's _Archiv_, 1834.
(97) B. Benecke. "Ueber die Entwicklung des Erdsalamanders."
_Zoologischer Anzeiger_, 1880.
(98) S. F. Clarke. "Development of Amblystoma punctatum," Part I.,
External. _Studies from the Biological Laboratory of the Johns Hopkins
University_, No. II. 1880.
(99) H. Cramer. "Bemerkungen üb. d. Zellenleben in d. Entwick. d.
Froscheies." Müller's _Archiv_, 1848.
(100) A. Ecker. _Icones Physiolog._ 1851-1859.
(101) A. Götte. _Die Entwicklungsgeschichte der Unke._ Leipzig, 1875.
(102) C. K. Hoffmann. "Amphibia." _Klassen u. Ordnungen d.
Thierreichs_, 1873-1879.
(103) T. H. Huxley. Article "Amphibia" in the _Encyclopædia
Britannica_.
(104) A. Moquin-Tandon. "Développement des Batraciens anures."
_Annales des Sciences Naturelles_, III. 1875.
(105) G. Newport. "On the impregnation of the Ovum in Amphibia" (three
memoirs). _Phil. Trans._ 1851, 1853, and 1854.
(106) W. K. Parker. "On the structure and development of the Skull of
the common Frog." _Phil. Trans._, CLXI. 1871.
(107) W. K. Parker. "On the structure and development of the Skull of
the Batrachia." _Phil. Trans._, Vol. CXLVI., Part 2. 1876.
(108) W. C. H. Peters. "Ueber die Entwicklung der Coecilien und
besonders von Coecilia compressicauda." _Berlin Monatsbericht_, p. 40,
1874.
(109) W. C. H. Peters. "Ueber die Entwicklung der Coecilien." _Berl.
Monatsbericht_, p. 483, 1875.
(110) J. L. Prevost and J. B. Dumas. "Deuxième Mém. s. l. génération.
Développement de l'oeuf d. Batraciens." _Ann. Sci. Nat._ II. 1824.
(111) R. Remak. _Untersuchungen über die Entwicklung der
Wirbelthiere_, 1850-1858.
(112) M. Rusconi. _Développement de la grenouille commune depuis le
moment de sa naissance jusqu'à son état parfait_, 1826.
(113) M. Rusconi. _Histoire naturelle, développement et métamorphose
de la Salamandre terrestre_, 1854.
(114) W. B. Scott and H. F. Osborn. "On the early development of the
common Newt." _Quart. J. of Micr. Science_, Vol. XXIX. 1879.
(115) S. Stricker. "Entwicklungsgeschichte von Bufo cinereus." _Sitzb.
der kaiserl. Acad. zu Wien_, 1860.
(116) S. Stricker. "Untersuchungen über die ersten Anlagen in
Batrachier-Eiern." _Zeitschrift f. wiss. Zoologie_, Bd. XI. 1861.
CHAPTER VIII.
AVES.
INTRODUCTION.
The variations in the character of the embryonic development of the
Amniota are far less important than in the case of the Ichthyopsida.
There are, it is true, some very special features in the early
developmental history of the Mammalia, but apart from these there is
such a striking uniformity in the embryos of all the groups that it
would, in many cases, be difficult to assign a young embryo to its
proper class.
Amongst the Sauropsida the Aves have for obvious reasons received a
far fuller share of attention than any other group; and an account of
their embryology forms a suitable introduction to this part of our
subject. For the convenience of the student many parts of their
developmental history will be dealt with at greater length than in the
case of the previous groups.
_The development of the Aves._
Comparatively few types of Birds have been studied embryologically.
The common Fowl has received a disproportionately large share of
attention; although within quite recent times the Duck, the Goose, the
Pigeon, the Starling, and a Parrot (Melopsittacus undulatus) have also
been studied. The result of these investigations has been to shew that
the variations in the early development of different Birds are
comparatively unimportant. In the sequel the common Fowl will be
employed as type, attention being called when necessary to the
development of the other forms.
[FIG. 85. YOLK ELEMENTS FROM THE EGG OF THE FOWL.
_A._ Yellow yolk. _B._ White yolk.]
The ovum of the Fowl, at the time when it is clasped by the expanded
extremity of the oviduct, is a large yellow body enclosed in a
vitelline membrane. It is mainly formed of spherules of food-yolk. Of
these there are two varieties; one known as yellow yolk, and the other
as white. The white yolk spherules form a small mass at the centre of
the ovum, which is continued to the surface by a narrow stalk, and
there expands into a somewhat funnel-shaped disc, the edges of which
are continued over the surface of the ovum as a delicate layer. The
major part of the ovum is formed of yellow yolk. The yellow yolk
consists of large delicate spheres, filled with small granules (fig.
85 A); while the white yolk is formed of vesicles of a smaller size
than the yellow yolk spheres, in which are a variable number of highly
refractive bodies (fig. 85 B).
[FIG. 86. SECTION THROUGH THE GERMINAL DISC OF THE RIPE OVARIAN OVUM
OF A FOWL WHILE YET ENCLOSED IN ITS CAPSULE.
_a._ Connective-tissue capsule of the ovum; _b._ epithelium of the
capsule, at the surface of which nearest the ovum lies the vitelline
membrane; _c._ granular material of the germinal disc, which becomes
converted into the blastoderm. (This is not very well represented in
the woodcut. In sections which have been hardened in chromic acid it
consists of fine granules.) _w.y._ white yolk, which passes
insensibly into the fine granular material of the disc; _x._
germinal vesicle enclosed in a distinct membrane, but shrivelled up;
_y._ space originally completely filled up by the germinal vesicle,
before the latter was shrivelled up.]
In addition to the yolk there is present in the ovum a small
protoplasmic region, containing the remains of the germinal vesicle,
which forms the germinal disc (fig. 86). It overlies the funnel-shaped
disc of white yolk, into which it is continued without any marked line
of demarcation. It contains numerous minute spherules of the same
nature as the smallest white yolk spherules.
Impregnation takes place at the upper extremity of the oviduct.
In its passage outwards the ovum gradually receives its accessory
coverings in the form of albumen, shell-membrane, and shell (fig. 87).
[FIG. 87. DIAGRAMMATIC SECTION OF AN UNINCUBATED FOWL'S EGG.
(Modified from Allen Thomson.)
_bl._ blastoderm; _w.y._ white yolk. This consists of a central
flask-shaped mass and a number of layers concentrically arranged
around it. _y.y._ yellow yolk; _v.t._ vitelline membrane; _x._ layer
of more fluid albumen immediately surrounding the yolk; _w._ albumen
consisting of alternate denser and more fluid layers; _ch.l._
chalaza; _a.ch._ air-chamber at the broad end of the egg. This
chamber is merely a space left between the two layers of the
shell-membrane. _i.s.m._ internal layer of shell-membrane; _s.m._
external layer of shell-membrane; _s._ shell.]
[FIG 88. SURFACE VIEWS OF THE EARLY STAGES OF THE SEGMENTATION IN A
FOWL'S EGG. (After Coste.)
_a._ edge of germinal disc; _b._ vertical furrow; _c._ small central
segment; _d._ larger peripheral segment.]
[FIG. 89. SURFACE VIEW OF THE GERMINAL DISC OF FOWL'S EGG DURING A
LATE STAGE OF THE SEGMENTATION.
_c._ small central segmentation spheres; _b._ larger segments
outside these; _a._ large, imperfectly circumscribed, marginal
segments; _e._ margin of germinal disc.]
The segmentation commences in the lower part of the oviduct, shortly
before the shell has begun to be formed. It is meroblastic, being
confined to the germinal disc, through the full depth of which however
the earlier furrows do not extend. It is mainly remarkable for being
constantly somewhat unsymmetrical (Kölliker)--a feature which is not
represented in fig. 88, copied from Coste. Owing to the absence of
symmetry the cells at one side of the germinal disc are larger than
those at the other, but the relations between the disc and the axis of
the embryo are not known. During the later stages the segmentation is
irregular, and not confined to the surface; and towards its close the
germinal disc becomes somewhat lenticular in shape; and is formed of
segments, which are smallest in the centre and increase in size
towards the periphery (figs. 89 and 90). The superficial segments in
the centre of the germinal disc are moreover smaller than those below,
and more or less separated as a distinct layer (fig. 90). As
development proceeds the segmentation reaches its limits in the
centre, but continues at the periphery; and thus eventually the masses
at the periphery become of the same size as those at the centre. At
the time when the ovum is laid (fig. 91) the uppermost layer of
segments has given rise to a distinct membrane, the epiblast, formed
of a single row of columnar nar cells (_ep_). The lower or hypoblast
segments are larger, in some cases very much larger, than those of the
epiblast, and are so granular that their nuclei can only with
difficulty be seen. They form a somewhat irregular mass, several
layers deep, and thicker at the periphery than at the centre: they
rest on a bed of white yolk, from which they are in parts separated by
a more or less developed cavity, which is probably filled with fluid
yolk matter about to be absorbed. In the bed of white yolk nuclei are
present, which are of the same character, and have the same general
fate, as those in Elasmobranchii. They are generally more numerous in
the neighbourhood of the thickened periphery of the blastoderm than
elsewhere. Peculiar large spherical bodies are to be found amongst the
lower layer cells, which superficially resemble the larger cells
around them, and have been called formative cells [_vide_ Foster and
Balfour (No. 126)]. Their real nature is still very doubtful, and
though some are no doubt true cells, others are perhaps only nutritive
masses of yolk. In a surface view the blastoderm, as the segmented
germinal disc may now be called, appears as a circular disc; the
central part of which is distinguished from the peripheral by its
greater transparency, and forms what is known in the later stages as
the area pellucida. The narrow darker ring of blastoderm, outside the
area pellucida, is the commencing area opaca.
[FIG. 90. SECTION OF THE GERMINAL DISC OF A FOWL DURING THE LATER
STAGES OF SEGMENTATION.
The section, which represents rather more than half the breadth of
the blastoderm (the middle line being shewn at _c_), shews that the
upper and central parts of the disc segment faster than those below
and towards the periphery. At the periphery the segments are still
very large. One of the larger segments is shewn at _a_. In the
majority of segments a nucleus can be seen; and it seems probable
that the nucleus is present in them all. Most of the segments are
filled with highly refracting spherules, but these are more numerous
in some cells (especially the larger cells near the yolk) than in
others. In the central part of the blastoderm the upper cells have
commenced to form a distinct layer. No segmentation cavity is
present.
_a._ large peripheral cell; _b._ larger cells of the lower parts of
the blastoderm; _c._ middle line of blastoderm; _e._ edge of the
blastoderm adjoining the white yolk; _w._ white yolk.]
[FIG. 91. SECTION OF A BLASTODERM OF A FOWL'S EGG AT THE
COMMENCEMENT OF INCUBATION.
The thin epiblast _ep_ composed of columnar cells rests on the
incomplete lower layer _l_, composed of larger and more granular
hypoblast cells. The lower layer is thicker in some places than in
others, and is especially thick at the periphery. The line below the
under layer marks the upper surface of the white yolk. The larger
so-called formative cells are seen at _b_, lying on the white yolk.
The figure does not take in quite the whole breadth of the
blastoderm; but the reader must understand that both to the right
hand and to the left _ep_ is continued farther than _l_, so that at
the extreme edge it rests directly on the white yolk.]
As a result of incubation the blastoderm undergoes a series of
changes, which end in the definite formation of three germinal layers,
and in the establishment of the chief systems of organs of the embryo.
The more important of these changes are accomplished in the case of
the common Fowl during the first day and the early part of the second
day of incubation.
There is hardly any question in development which has been the subject
of so much controversy as the mode of formation of the germinal layers
in the common Fowl. The differences in the views of authors have been
caused to a large extent by the difficulties of the investigation, but
perhaps still more by the fact that many of the observations were made
at a time when the methods of making sections were very inferior to
those of the present day. The subject itself is by no means of an
importance commensurate with the attention it has received. The
characters which belong to the formation of the layers in the
Sauropsida are secondarily derived from those in the Ichthyopsida, and
are of but little importance for the general questions which concern
the nature and origin of the germinal layers. In the account in the
sequel I have avoided as much as possible discussion of controverted
points. My statements are founded in the main on my own observations,
more especially on a recent investigation carried on in conjunction
with my pupil, Mr Deighton. It is to Kölliker (No. 135), and to Gasser
(No. 127) that the most important of the more recent advances in our
knowledge are due. Kölliker, in his great work on Embryology,
definitely established the essential connection between the primitive
streak and the formation of the mesoblast; but while confirming his
statement on this head, I am obliged to differ from him with reference
to some other points.
Gasser's work, especially that part of it which relates to the
passages leading from the neural to the alimentary canal, which he was
the first to discover, is very valuable.
The blastoderm gradually grows in size, and extends itself over the
yolk; the growth over the yolk being very largely effected by an
increase in the size of the area opaca, which during this process
becomes more distinctly marked off from the area pellucida. The area
pellucida gradually assumes an oval form, and at the same time becomes
divided into a posterior opaque region and an anterior transparent
region. The posterior opacity is named by some authors the embryonic
shield.
[FIG. 92. TRANSVERSE SECTION THROUGH THE BLASTODERM OF A CHICK
BEFORE THE APPEARANCE OF THE PRIMITIVE STREAK.
The epiblast is represented somewhat diagrammatically. The hyphens
shew the points of junction of the two halves of the section.]
During these changes the epiblast (fig. 92) becomes two layers deep
over the greater part of the area pellucida, though still only one
cell deep in the area opaca. The irregular hypoblast spheres of the
unincubated blastoderm flatten themselves out, and unite into a
definite hypoblastic membrane (fig. 92). Between this membrane and the
epiblast there remain a number of scattered cells (fig. 92) which
cannot however be said to form a definite layer altogether distinct
from the hypoblast. They are almost entirely confined to the posterior
part of the area pellucida, and give rise to the opacity of that part.
At the edge of the area pellucida the hypoblast becomes continuous
with a thickened rim of material, underlying the epiblast, and derived
from the original thickened edge of the blastoderm and the subjacent
yolk. It is mainly formed of yolk granules, with a varying number of
cells and nuclei imbedded in it. It is known as the germinal wall, and
is spoken of more in detail on pp. 160 and 161.
[FIG. 93. DIAGRAMS ILLUSTRATING THE POSITION OF THE BLASTOPORE, AND
THE RELATION OF THE EMBRYO TO THE YOLK IN VARIOUS MEROBLASTIC
VERTEBRATE OVA.
A. Type of Frog. B. Elasmobranch type. C. Amniotic Vertebrate.
_mg._ medullary plate; _ne._ neurenteric canal; _bl._ portion of
blastopore adjoining the neurenteric canal. In B this part of the
blastopore is formed by the edges of the blastoderm meeting and
forming a linear streak behind the embryo; and in C it forms the
structure known as the primitive streak. _yk._ part of yolk not yet
enclosed by the blastoderm.]
The changes which next take place result in the complete
differentiation of the embryonic layers, a process which is intimately
connected with the formation of the structure known as the primitive
streak. The meaning of the latter structure, and its relation to the
embryo, can only be understood by comparison with the development of
the forms already considered. The most striking peculiarity in the
first formation of the embryo Bird, as also in that of the embryos of
all Amniota, consists in the fact that _they do not occupy a position
at the edge of the blastoderm, but are placed near its centre_.
Behind the embryo there is however a peculiar structure--the primitive
streak above mentioned--which is a linear body placed in the posterior
region of the blastoderm. This body, the nature of which will be more
fully explained in the chapter on the comparative development of
Vertebrates, is really a rudimentary part of the blastopore, of the
same nature as the linear streak behind the embryo in Elasmobranchii
formed by the concrescence of the edges of the blastoderm (_vide_ p.
64); although there is no ontogenetic process in the Amniota, like the
concrescence in Elasmobranchii. The relations of the blastopore in
Elasmobranchii and Aves is shewn in figs. B and C of the diagram (fig.
93).
[FIG. 94. AREA PELLUCIDA OF A VERY YOUNG BLASTODERM OF A CHICK,
SHEWING THE PRIMITIVE STREAK AT ITS FIRST APPEARANCE.
_pr.s._ primitive streak; _ap._ area pellucida; _a.op._ area opaca.]
[FIG. 95. TRANSVERSE SECTION THROUGH A BLASTODERM OF ABOUT THE AGE
REPRESENTED IN FIG. 94, SHEWING THE FIRST DIFFERENTIATION OF THE
PRIMITIVE STREAK.
The section passes through about the middle of the primitive streak.
_pvs._ primitive streak; _ep._ epiblast; _hy._ hypoblast; _yk._ yolk
of the germinal wall.]
In describing in detail the succeeding changes we may at first confine
our attention to the area pellucida. As this gradually assumes an oval
form the posterior opacity becomes replaced by a very dark median
streak, which extends forwards some distance from the posterior border
of the area (fig. 94). This is the first rudiment of the primitive
streak. In the region in front of it the blastoderm is still formed of
two layers only, but in the region of the streak itself the structure
of the blastoderm is greatly altered. The most important features in
it are represented in fig. 95. This figure shews that the median
portion of the blastoderm has become very much thickened (thus
producing the opacity of the primitive streak), and that this
thickening is caused by a proliferation of rounded cells from the
epiblast. In the very young primitive streak, of which fig. 95 is a
section, the rounded cells are still continuous throughout with the
epiblast, but they form nevertheless the rudiment of the greater part
of a sheet of mesoblast, which will soon arise in this region.
In addition to the cells clearly derived from the epiblast, there are
certain other cells (_vide_ fig. 95), closely adjoining the hypoblast,
which appear to me to be the derivatives of the cells interposed
between the epiblast and hypoblast, which gave rise to the posterior
opacity in the blastoderm during the previous stage. In my opinion
these cells also have a share in forming the future mesoblast.
The number and distribution of these cells is subject to not
inconsiderable variations. In a fair number of cases they are entirely
congregated along the line of the primitive streak, leaving the sides
of the blastoderm quite free. They then form a layer, which can only
with difficulty be distinguished from the cells derived from the
epiblast by slight peculiarities of staining, and by the presence of a
considerable proportion of large granular cells. It is, I believe, by
the study of such blastoderms that Kölliker has been led to deny to
the intermediate cells of the previous stage any share in the
formation of the mesoblast. In other instances, of which fig. 95 is a
fairly typical example, they are more widely scattered. To follow with
absolute certainty the history of these cells, and to prove that they
join the mesoblast is not, I believe, possible by means of sections,
and I must leave the reader to judge how far the evidence given in the
sequel is sufficient to justify my opinions on this subject.
[FIG. 96. SURFACE VIEW OF THE AREA PELLUCIDA OF A CHICK'S BLASTODERM
SHORTLY AFTER THE FORMATION OF THE PRIMITIVE GROOVE.
_pr._ primitive streak with primitive groove; _af._ amniotic fold.
The darker shading round the primitive streak shews the extension of
the mesoblast.]
In the course of further growth the area pellucida soon becomes
pyriform, the narrower extremity being the posterior. The primitive
streak (fig. 96) elongates considerably, so as to occupy about
two-thirds of the length of the area pellucida; but its hinder end in
many instances does not extend to the posterior border of the area
pellucida. The median line of the primitive streak becomes marked by a
shallow groove, known as the primitive groove.
[FIG. 97. TRANSVERSE SECTION THROUGH THE FRONT END OF THE PRIMITIVE
STREAK OF A BLASTODERM OF THE SAME AGE AS FIG. 96.
_pv._ primitive groove; _m._ mesoblast; _ep._ epiblast; _hy._
hypoblast; _yh._ yolk of germinal wall.]
During these changes in external appearance there grow from the sides
of the primitive streak two lateral wings of mesoblast cells, which
gradually extend till they reach the sides of the area pellucida (fig.
97). The mesoblast still remains attached to the epiblast along the
line of the primitive streak. During this extension many sections
through the primitive streak give an impression of the mesoblast being
involuted at the lips of a fold, and so support the view above
propounded, that the primitive streak is the rudiment of the coalesced
lips of the blastopore. The hypoblast below the primitive streak is
always quite independent of the mesoblast above, though much more
closely attached to it in the median line than at the sides. The part
of the mesoblast, which I believe to be derived from the primitive
hypoblast, can generally be distinctly traced. In many cases,
especially at the front end of the primitive streak, it forms, as in
fig. 97, a distinct layer of stellate cells, quite unlike the rounded
cells of the mesoblastic involution of the primitive streak.
[FIG. 98. LONGITUDINAL SECTION THROUGH THE AXIAL LINE OF THE
PRIMITIVE STREAK, AND THE PART OF THE BLASTODERM IN FRONT OF IT, OF
AN EMBRYO CHICK SOMEWHAT YOUNGER THAN FIG. 99.
_pr.s._ primitive streak; _ep._ epiblast; _hy._ hypoblast of region
in front of primitive streak; _n._ nuclei; _yk._ yolk of germinal
wall.]
In the region in front of the primitive streak, where the first trace
of the embryo will shortly appear, the layers at first undergo no
important changes, except that the hypoblast becomes somewhat thicker.
Soon, however, as shewn in longitudinal section in fig. 98, the
hypoblast along the axial line becomes continuous behind with the
front end of the primitive streak. Thus at this point, which is the
future hind end of the embryo, the mesoblast, the epiblast, and the
hypoblast all unite together; just as they do in all the types of
Ichthyopsida.
Shortly afterwards, at a slightly later stage than that represented in
fig. 96, an important change takes place in the constitution of the
hypoblast in front of the primitive streak. The rounded cells, of
which it is at first composed (fig. 98), break up into (1) a layer
formed of a single row of more or less flattened elements below--the
hypoblast--and (2) into a layer formed of several rows of stellate
elements, between the hypoblast and the epiblast--the mesoblast (fig.
99). A separation between these two layers is at first hardly
apparent, and before it has become at all well marked, especially in
the median line, an axial opaque line makes its appearance in surface
views, continued forwards from the front end of the primitive streak,
but stopping short at a semicircular fold--the future head-fold--near
the front end of the area pellucida. In section (fig. 100) this opaque
line is seen to be due to a special concentration of cells in the form
of a cord. This cord is the commencement of the notochord (_ch_). In
some instances the commencing notochord remains attached to the
hypoblast, while the mesoblast is laterally quite distinct (_vide_
fig. 100), and is therefore formed in the same manner as in most
Ichthyopsida; while in other instances, and always apparently in the
Goose (Gasser, No. 127), the notochord appears to become
differentiated in the already separated layer of mesoblast. In all
cases _the notochord and the hypoblast below it unite with the front
end of the primitive streak_; with which also the two lateral plates
of mesoblast become continuous.
[FIG. 99. TRANSVERSE SECTION THROUGH THE EMBRYONIC REGION OF THE
BLASTODERM OF A CHICK SHORTLY PRIOR TO THE FORMATION OF THE
MEDULLARY GROOVE AND NOTOCHORD.
_m._ median line of the section; _ep._ epiblast; _ll._ lower layer
cells (primitive hypoblast) not yet completely differentiated into
mesoblast and hypoblast; _n._ nuclei of germinal wall.]
From what has just been said it is clear that in the region of the
embryo the mesoblast originates as two lateral plates split off from
the hypoblast, and that the notochord originates as a median plate,
simultaneously with the mesoblast, with which it may sometimes be at
first continuous.
Kölliker holds that the mesoblast of the region of the embryo is
derived from a forward growth from the primitive streak. There is no
theoretical objection to this view, and I think it would be impossible
to shew for certain by sections whether or not there is a growth such
as he describes; but such sections as that represented in fig. 99 (and
I have series of similar sections from several embryos) appear to me
to be conclusive in favour of the view that the mesoblast of the
region of the embryo is to a large extent derived from a
differentiation of the primitive hypoblast. I am however inclined to
believe that some of the mesoblast cells of the embryonic region have
the derivation which Kölliker ascribes to all of them.
[FIG. 100. TRANSVERSE SECTION THROUGH THE EMBRYONIC REGION OF THE
BLASTODERM OF A CHICK AT THE TIME OF THE FORMATION OF THE NOTOCHORD,
BUT BEFORE THE APPEARANCE OF THE MEDULLARY GROOVE.
_ep._ epiblast; _hy._ hypoblast; _ch._ notochord; _me._ mesoblast;
_n._ nuclei of the germinal wall _yk._ yolk.]
As regards the mesoblast of the primitive streak, in a purely
objective description like that given above, the greater part of it
may fairly be described as being derived from the epiblast. But if it
is granted that the primitive streak corresponds with the blastopore,
it is obvious to the comparative embryologist that the mesoblast
derived from it really originates from the lips of the blastopore, as
in so many other cases; and that to describe it, without explanation,
as arising from the epiblast, would give an erroneous impression of
the real nature of the process.
[FIG. 101. TRANSVERSE SECTION OF A BLASTODERM INCUBATED FOR 18 HOURS.
The section passes through the medullary groove _mc._, at some
distance behind its front end.
A. epiblast. B. mesoblast. C. hypoblast.
_m.c._ medullary groove; _m.f._ medullary fold; _ch._ notochord.]
The differentiation of the embryo may be said to commence with the
formation of the notochord and the lateral plates of mesoblast. Very
shortly after the formation of these structures the axial part of the
epiblast, above the notochord and in front of the primitive streak,
which is somewhat thicker than the lateral parts, becomes
differentiated into a distinct medullary plate, the sides of which
form two folds--the medullary folds--enclosing between them a
medullary groove (fig. 101).
In front the two medullary folds meet, while posteriorly they thin out
and envelop between them the front end of the primitive streak. On the
formation of the medullary folds the embryo assumes a form not unlike
that of the embryos of many Ichthyopsida at a corresponding stage. The
appearance of the embryo, and its relation to the surrounding parts is
somewhat diagrammatically represented in fig. 102. The primitive
streak now ends with an anterior swelling (not represented in the
figure), and is usually somewhat unsymmetrical. In most cases its axis
is more nearly continuous with the left, or sometimes the right,
medullary fold than with the medullary groove. In sections its front
end appears as a ridge on one side or on the middle of the floor of
the widened end of the medullary groove.
[FIG. 102. SURFACE VIEW OF THE PELLUCID AREA OF A BLASTODERM OF 18
HOURS.
None of the opaque area is shewn, the pear-shaped outline indicating
the limits of the pellucid area.
At the hinder part of the area is seen the primitive groove _pr._,
with its nearly parallel walls, fading away behind, but curving
round and meeting in front so as to form a distinct anterior
termination to the groove, about halfway up the pellucid area.
Above the primitive groove is seen the medullary groove _m.c._, with
the medullary folds _A._ These, diverging behind, slope away on
either side of the primitive groove, while in front they curve round
and meet each other close upon a curved line which represents the
head-fold.
The second curved line in front of and concentric with the first is
the commencing fold of the amnion.]
The mesoblast and hypoblast, within the area pellucida, do not give
rise to the whole of these two layers in the surrounding area opaca;
but the whole of the hypoblast of the area opaca, and a large portion
of the mesoblast, and possibly even some of the epiblast, take their
origin from the peculiar material already spoken of, which forms the
germinal wall, and is continuous with the hypoblast at the edge of the
area opaca (_vide_ figs. 91, 94, 97, 98, 99, 100).
The exact nature of this material has been the subject of many
controversies. Into these controversies it is not my purpose to enter,
but subjoined are the results of my own examination. The germinal wall
first consists, as already mentioned, of the lower cells of the
thickened edge of the blastoderm, and of the subjacent yolk material
with nuclei. During the period before the formation of the primitive
streak the epiblast extends itself over the yolk, partly, it appears,
at the expense of the cells of the germinal wall, and possibly even of
cells formed around the nuclei in this part. This mode of growth of
the epiblast is very similar to that in the epibolic gastrulas of many
Invertebrata, of the Lamprey, etc.; but how far this process is
continued in the subsequent extension of the epiblast I am unable to
say. The cells of the germinal wall, which are at first well separated
from the yolk below, become gradually absorbed in the growth of the
hypoblast, and the remaining cells and yolk then become mingled
together, and constitute a compound structure, continuous at its inner
border with the hypoblast. This structure is the germinal wall usually
so described. It is mainly formed of yolk granules with numerous
nuclei, and a somewhat variable number of largish cells imbedded
amongst them. The nuclei typically form a special layer immediately
below the epiblast, some of which are probably enclosed by a definite
cell-body. A special mass of nuclei (_vide_ figs. 98 and 100, _n_) is
usually present at the junction of the hypoblast with the germinal
wall.
The germinal wall at this stage corresponds in many respects with the
granular material, forming a ring below the edge of the blastoderm in
Teleostei.
It retains the characters above enumerated till near the close of the
first day of incubation, _i.e._ till several mesoblastic somites have
become established. It then becomes more distinctly separated from the
subjacent yolk, and its component parts change very considerably in
character. The whole wall becomes much less granular. It is then
mainly formed of large vesicles, which often assume a palisade-like
arrangement, and contain granular balls, spherules of white yolk, and
in an early stage a good deal of granular matter (_vide_ fig. 115).
These bodies have some resemblance to cells, and have been regarded as
such by Kölliker (No. 135) and Virchow (No. 150): they contain however
nothing which can be considered as a nucleus. Between them however
nuclei[62] may easily be seen in specimens hardened in picric acid,
and stained with hæmatoxylin (these nuclei are not shewn in fig. 115).
These nuclei are about the same size as those of the hypoblast cells,
and are surrounded by a thin layer of granular protoplasm, which is
continuous with a mesh-work of granular protoplasm enveloping the
above described vesicles. The germinal wall is still continuous with
the hypoblast at its edge; and close to the junction of the two the
hypoblast at first forms a layer of moderately columnar cells, one or
two deep and directly continuous with the germinal wall, and at a
later period usually consists of a mass of rounder cells lying above
the somewhat abrupt inner edge of the germinal wall.
[62] The presence of numerous nuclei in the germinal wall was, I
believe, first clearly proved by His (No. 132). I cannot however
accept the greater number of his interpretations.
The germinal wall certainly gives rise to the hypoblast cells, which
mainly grow at its expense. They arise at the edge of the area
pellucida, and when first formed are markedly columnar, and enclose in
their protoplasm one of the smaller vesicles of the germinal wall.
In the later stages (fourth day and onwards) the whole germinal wall
is stated to break up into columnar hypoblast cells, each of them
mainly formed of one of the vesicles just spoken of. After the
commencing formation of the embryo the mesoblast becomes established
at the inner edge of the area opaca, between the germinal wall and the
epiblast; and gives rise to the tissue which eventually forms the area
vasculosa. It seems probable that the mesoblast in this situation is
mainly derived from cells formed around the nuclei of the germinal
wall, which are usually specially aggregated close below the epiblast.
Disse (No. 122) has especially brought evidence in favour of this
view, and my own observations also support it.
The mesoblastic somites begin to be formed in the lateral plates of
the mesoblast before the closure of the medullary folds. The first
somite arises close to the foremost extremity of the primitive streak,
but the next is stated to arise in front of this, so that the first
formed somite corresponds to the second permanent vertebra[63]. The
region of the embryo in front of the second formed somite--at first
the largest part of the embryo--is the cephalic region. The somites
following the second are formed in the regular manner, from before
backwards, out of the unsegmented posterior part of the embryo, which
rapidly grows in length to supply the necessary material (fig. 103).
As the somites retain during the early stages of development an
approximately constant breadth, their number is a fair test of the
length of the trunk. With the growth of the embryo the primitive
streak is continually carried back, the lengthening of the embryo
always taking place between the front end of the primitive streak and
the last somite; and during this process the primitive streak
undergoes important changes both in itself and in its relation to the
embryo. Its anterior thicker part, which is enveloped in the diverging
medullary folds, soon becomes distinguished in structure from the part
behind this, and placed symmetrically in relation to the axis of the
embryo (fig. 103, _a.pr_), and at the same time the medullary folds,
which at first simply diverge on each side of the primitive streak,
bend in again and meet behind so as completely to enclose the front
part of the primitive streak. The region of the embryo bird, where the
medullary folds diverge, is known as the sinus rhomboidalis, though it
has no connection with the similarly named structure in the adult. By
the time that ten somites are formed the sinus rhomboidalis is
completely established, and the medullary groove has become converted
into a tube till close up to the front end of the sinus. In the
following stages the closure of the medullary canal extends to the
sinus rhomboidalis, and the folding off of the hind end of the embryo
from the yolk commences. Coincidently with the last-named changes the
sides of the front part of the primitive streak become thickened, and
give rise to conspicuous caudal swellings; in which the layers of the
embryo are indistinguishably fused. The apparently hinder part of the
primitive streak becomes, as more particularly explained in the
sequel, folded downwards and forwards on the ventral side.
[63] Further investigations in confirmation of this widely
accepted statement are very desirable.
[FIG. 103. DORSAL VIEW OF THE HARDENED BLASTODERM OF A CHICK WITH
FIVE MESOBLASTIC SOMITES. THE MEDULLARY FOLDS HAVE MET FOR PART OF
THEIR EXTENT, BUT HAVE NOT UNITED.
_a.pr._ anterior part of the primitive streak; _p.pr._ posterior
part of the primitive streak.]
This is a convenient place to notice remarkable appearances which
present themselves close to the junction of the neural plate and the
primitive streak. These are temporary passages leading from the hinder
end of the neural tube into the alimentary canal. They vary somewhat
in different species of birds, and it appears that in the same species
there may be several openings of the kind, which appear one after the
other and then close again. They were first discovered by Gasser (No.
127). In all cases[64] they lead round the posterior end of the
notochord, or through the point where the notochord falls into the
primitive streak.
[64] This does not appear to be the case with the anterior
opening in Melopsittacus undulatus, though its relations are not
clear from Braun's description (No. 120).
If the primitive streak is, as I believe, formed of the lips of the
blastopore, there can be but little doubt that these structures are
disappearing, and functionless rudiments of the opening of the
blastopore, and they thus lend support to my view as to the nature of
the primitive streak. That, in part, they correspond with the
neurenteric canal of the Ichthyopsida is clear from the detailed
statements below. Till their relations have been more fully worked out
it is not possible to give a more definite explanation of them.
According to Braun (No. 120) three independent communications are to
be distinguished in Birds. These are best developed in the Duck. The
first of these is a small funnel-shaped diverticulum leading from the
neural groove through the hypoblast. It is visible when eight
mesoblastic somites are present, and soon disappears. The second,
which is the only one I have myself investigated, is present in the
embryo duck with twenty-six mesoblastic somites, and is represented in
the series of sections (fig. 104). The passage leads obliquely
backwards and ventralwards from the hind end of the neural tube into
the notochord, where the latter joins the primitive streak (B). A
narrow diverticulum from this passage is continued forwards for a
short distance along the axis of the notochord (A, _ch_). After
traversing the notochord, the passage is continued into a hypoblastic
diverticulum, which opens ventrally into the future lumen of the
alimentary tract (C). Shortly behind the point where the neurenteric
passage communicates with the neural tube the latter structure opens
dorsally, and a groove on the surface of the primitive streak is
continued backwards from it for a short distance (C). The first part
of this passage to appear is the hypoblastic diverticulum above
mentioned.
This passage does not long remain open, but after its closure, when
the tail-end of the embryo has become folded off from the yolk, a
third passage is established, and leads round the end of the notochord
from the closed medullary canal into the postanal gut. It is shewn
diagrammatically in fig. 106, _ne_, and, as may be gathered from that
figure, has the same relations as the neurenteric canal of the
Ichthyopsida.
In the goose a passage has been described by Gasser, which appears
when about fourteen or fifteen somites are present, and lasts till
twenty-three are formed. Behind its opening the medullary canal is
continued back as a small diverticulum, which follows the course of
the primitive groove and is apparently formed by the conversion of
this groove into a canal. It is at first open to the exterior, but
soon becomes closed, and then atrophies.
[FIG. 104. FOUR TRANSVERSE SECTIONS THROUGH THE NEURENTERIC PASSAGE
AND ADJOINING PARTS IN A DUCK EMBRYO WITH TWENTY-SIX MESOBLASTIC
SOMITES.
A. Section in front of the neurenteric canal shewing a lumen in the
notochord.
B. Section through the passage from the medullary canal into the
notochord.
C. Section shewing the hypoblastic opening of the neurenteric canal,
and the groove on the surface of the primitive streak, which opens
in front into the medullary canal.
D. Primitive streak immediately behind the opening of the
neurenteric passage.
_mc._ medullary canal; _ep._ epiblast; _hy._ hypoblast; _ch._
notochord; _pr._ primitive streak.]
In the chick there is a perforation on the floor of the neural canal,
which is not so marked as those in the goose or duck, and never
results in a complete continuity between the neural and alimentary
tracts; but simply leads from the floor of the neural canal into the
tissues of the tail swelling, and thence into a cavity in the
posterior part of the notochord. The hinder diverticulum of the neural
canal along the line of the primitive groove is, moreover, very
considerable in the chick, and is not so soon obliterated as in the
goose. The incomplete passage in the chick arises when about twelve
somites are present. It is regarded by Braun as equivalent to the
first formed passage in the duck, but I very much doubt whether there
is a very exact equivalence between the openings in different types,
and think it more probable that they are variable remnants of a
primitive neurenteric canal, which in the ancestors of those forms
persisted through the whole period of the early development. The third
passage is formed in the chick (Kupffer) during the third day of
incubation. In Melopsittacus undulatus the two first communications
are stated by Braun (No. 120) to be present at the same time, the one
in front of the other.
It is probable, from the above description, that the front portion of
the primitive streak in the bird corresponds with that part of the
lips of the blastopore in Elasmobranchii which becomes converted into
the tail swelling and the lining of the neurentic canal; while the
original groove of the front part of the primitive streak appears to
be converted into the posterior diverticulum of the neural canal. The
hinder part of the primitive streak of the bird corresponds, in a very
general way, with the part of the blastopore in Elasmobranchii, which
shuts off the embryo from the edge of the blastoderm (_vide_ p. 64),
though there is of course no genetic relation between the two
structures. When the anterior part of the streak is becoming converted
into the tail swelling, the groove of the posterior part gradually
shallows and finally disappears. The hinder part itself atrophies from
behind forwards, and in the course of the folding off of the embryo
from the yolk the part of the blastoderm where it was placed becomes
folded in, so as to form part of the ventral wall of the embryo. The
apparent hinder part of the primitive streak is therefore in reality
the ventral and anterior part[65].
[65] This nomenclature may seem a little paradoxical. But on
reflection it will appear that so long as the embryo is simply
extended on the yolk-sphere, the point where the ventral surface
begins has to be decided on purely morphological grounds. That
point may fairly be considered to be close to the junction of the
medullary plate and primitive streak. To use a mathematical
expression the sign will change when we pass from the dorsal to
the ventral surface, so that in strict nomenclature we ought in
continuing round the egg in the same direction to speak of
passing backwards along the medullary, but forwards along the
primitive streak. Thus the apparent hind end of the primitive
streak is really the front end, and _vice versâ_. I have avoided
using this nomenclature to simplify my description, but it is of
the utmost importance that the morphological fact should be
grasped. If any reader fails to understand my point, a reference
to fig. 52 B will, I trust, make everything quite clear. The
heart of Acipenser (_ht_) is there seen apparently in front of
the head. It is of course really ventral, and its apparent
position is due to the extension of the embryo on a sphere. The
apparent front end of the heart is really the hind end, and _vice
versâ_.
It has generally been maintained that the primitive streak and groove
become wholly converted into the dorsal portion of the trunk of the
embryo, _i.e._ into the posterior part of the medullary plate and
subjacent structures. This view appears to me untenable in itself, and
quite incompatible with the interpretation of the primitive streak
given above. To shew how improbable it is, apart from any theoretical
considerations, I have compiled two tables of the relative lengths of
the primitive streak and the body of the embryo, measured by the
number of sections made through them, in a series of examples from the
data in Gasser's important memoir (No. 127). In these tables each
horizontal line relates to a single embryo. The first column shews the
number of somites, and the second the number of sections through the
primitive streak. Where the primitive streak becomes divided into two
parts the sections through the two parts are given separately: the
left column (A) referring to the anterior part of the streak; the
right column (P) to the posterior part. The third column gives the
number of sections through the embryo. The first table is for fowl
embryos, the second for goose embryos.
+--------+--------------+----------+
| No. of | No. of | No. of |
|Somites.| sections | sections |
| | through | through |
| | the | the |
| | Primitive | Embryo. |
| | Streak. | |
+--------+--------------+----------+
| 0 | 29 | 7 |
| 0 | 45 | 10 |
| 0 | 39 | 23 |
| 2 | 30 | 30 |
| 4 | 30 | 30 |
| | A P | |
| 5 or 6 | 10 + 17 = 27 | |
| 8 | 12 + 20 = 32 | 48 |
| 12 | 13 + 10 = 23 | |
| 14 | 9 + 12 = 21 | |
| 18 | 10 + 7 = 17 | 70 |
| | 8 + 4 = 12 | |
| | 8 + 3 = 11 | |
+--------+--------------+----------+
+--------+--------------+----------+
| No. of | No. of | No. of |
|Somites.| sections | sections |
| | through | through |
| | the | the |
| | Primitive | Embryo. |
| | Streak. | |
+--------+--------------+----------+
| 0 | 10 | 4 |
| 0 | 28 | 5 |
| 0 | 44 | 12 |
| 2 | 36 | 32 |
| 4 | 24 | 42 |
| | A P | |
| 9 | 10 + 10 = 20 | 61 |
| 14 | 8 + 10 = 18 | 68 |
| 17 | 8 + 5 = 13 | |
| 22 | 9 + 6 = 15 | |
| 26 | 6 + 5 = 11 | |
+--------+--------------+----------+
An inspection of these two tables shews that an actual diminution in
the length of the primitive streak takes place just about the time
when the first somites are being formed, but there is no ground for
thinking that the primitive streak becomes then converted into the
medullary plate. Subsequently the primitive streak does not for a
considerable time become markedly shorter, and certainly its
curtailment is not really sufficient to account for the increased
length of the embryo--an increase in length, which (with the exception
of the head) takes place entirely by additions at the hind end. At the
stage with fourteen somites the primitive streak is still pretty long.
In the later stages, as is clearly demonstrated by the tables, the
diminution in the length of the primitive streak mainly concerns the
posterior part and not that adjoining the embryo.
_General history of the germinal layers._
The epiblast. The epiblast of the body of the embryo, though several
rows of cells deep, does not become divided into two strata till late
in embryonic life; so that the organs of sense formed from the
epiblast, which are the same as in the types already described, are
not specially formed from an inner nervous stratum. The medullary
canal is closed in the same manner as in Elasmobranchii, the Frog,
etc., by the simple conversion of an open groove into a closed canal.
The closure commences first of all in the region of the mid-brain, and
extends rapidly backwards and more slowly forwards. It is completed in
the Fowl by about the time that twelve mesoblastic somites are formed.
The mesoblast. The general changes of this layer do not exhibit any
features of special interest--the division into lateral and vertebral
plates, etc., being nearly the same as in the lower forms.
[FIG. 105. DIAGRAMMATIC LONGITUDINAL SECTION THROUGH THE AXIS OF AN
EMBRYO BIRD.
The section is supposed to be made at a time when the head-fold has
commenced but the tail-fold has not yet appeared.
_F.So._ head-fold of the somatopleure. _F.Sp._ head-fold of the
splanchnopleure.
_pp._ pleuroperitoneal cavity; _Am._ commencing (head-) fold of the
amnion; _D._ alimentary tract; _N.C._ neural canal; _Ch._ notochord;
_A._ epiblast; _B._ mesoblast; _C._ hypoblast.]
[FIG. 106. DIAGRAMMATIC LONGITUDINAL SECTION THROUGH THE POSTERIOR
END OF AN EMBRYO BIRD AT THE TIME OF THE FORMATION OF THE ALLANTOIS.
_ep._ epiblast; _Sp.c._ spinal canal; _ch._ notochord; _n.e._
neurenteric canal; _hy._ hypoblast; _p.a.g._ postanal gut; _pr._
remains of primitive streak folded in on the ventral side; _al._
allantois; _me._ mesoblast; _an._ point where anus will be formed;
_p.c._ perivisceral cavity; _am._ amnion; _so._ somatopleure; _sp._
splanchnopleure.]
The hypoblast. The closure of the alimentary canal is entirely
effected by a process of tucking in or folding off of the embryo from
the yolk-sack. The general nature of the process is seen in the
diagrams figs. 105 and 121. The folds by which it is effected are
usually distinguished as the head-, the tail- and the lateral folds.
The head-fold (fig. 105) is the first to appear; and in combination
with the lateral folds gives rise to the anterior part of the
mesenteron (_D_) (including the oesophagus, stomach and duodenum),
which by its mode of formation clearly ends blindly in front. The
tail-fold, in combination with the two lateral folds, gives rise to
the hinder part of the alimentary tract, including the cloaca, which
is a true part of the mesenteron. At the junction between the two
folds there is present a circular opening leading into the yolk-sack,
which becomes gradually narrowed as development proceeds. The opening
is completely closed long before the embryo is hatched. Certain
peculiarities in reference to the structure of the tail-fold are
caused by the formation of the allantois, and are described with the
embryonic appendages. The stomodæum and proctodæum are formed by
epiblastic invaginations. The communication between the stomodæum and
the mesenteron is effected comparatively early (on the 4th day in the
chick), while that between the proctodæum and mesenteron does not take
place till very late (15th day in the chick). The proctodæum gives
rise to the bursa Fabricii, as well as to the anus. Although the
opening of the anus is so late in being formed, the proctodæum itself
is very early apparent. Soon after the hinder part of the primitive
streak becomes tucked in on the ventral side of the embryo, an
invagination may be noticed where the tail of the embryo is folded
off. This gradually becomes deeper, and finally comes into contact
with the hypoblast at the front (primitively the apparent hind) border
of the posterior section of the primitive streak. An early stage in
the invagination is shewn in the diagram (fig. 106, _an_). It deserves
to be noted that the anus lies some way in front of the blind end of
the mesenteron, so that there is in fact a well-developed postanal
section of the gut (fig. 106, _p.a.g_), which corresponds with that in
the Ichthyopsida. For a short period, as mentioned above (p. 163), a
neurenteric canal is present connecting the postanal gut with the
medullary tube in the duck, fowl, and other birds. On the ventral wall
of the postanal gut there are at first two prominences. The posterior
of these is formed of part of the tail swelling, and is therefore
derived from the apparent anterior part of the primitive streak. The
anterior is formed from what was originally the apparent posterior
part of the primitive streak. The postanal gut becomes gradually less
and less prominent, and finally atrophies.
_General development of the Embryo._
It will be convenient to take the Fowl as a type for the general
development of the Sauropsida.
The embryo occupies a fairly constant position with reference to the
egg-shell. Its long axis is placed at right angles to that of the egg,
and the broad end of the egg is on the left side of the embryo. The
general history of the embryo has already been traced up to the
formation of the first formed mesoblastic somites (fig. 107). This
stage is usually reached at about the close of the first day. After
this stage the embryo rapidly grows in length, and becomes, especially
in front and to the sides, more and more definitely folded off from
the yolk-sack.
The general appearance of the embryo between the 30th and 40th hours
of incubation is shewn in fig. 108 from the upper surface, and in fig.
109 from the lower. The outlines of the embryo are far bolder than
during the earlier stages. Fig. 109 shews the nature of the folding,
by which the embryo is constricted off from the yolk-sack. The folds
are complicated by the fact that the mesoblast has already become
split into two layers--a splanchnic layer adjoining the hypoblast and
a somatic layer adjoining the epiblast--and that the body cavity
between these two layers has already become pretty wide in the lateral
parts of the body of the embryo and the area pellucida. The fold by
which the embryo is constricted off from the yolk-sack is in
consequence a double one, formed of two limbs or laminæ, an inner limb
constituted by the splanchnopleure, and an outer limb by the
somatopleure. The relation of these two limbs is shewn in the
diagrammatic longitudinal section (fig. 105), and in the surface view
(fig. 109) the splanchnic limb being shewn at _sf_ and the somatic at
_so_. Between the two limbs, and closely adjoining the splanchnopleure,
is seen the heart (_ht_). At the stage figured the head is well marked
off from the trunk, but the first separation between the two regions
was effected at an earlier period, on the appearance of the foremost
somite (fig. 107). Very shortly after the cephalic region is
established, and before the closure of the medullary folds, the
anterior part of the neural canal becomes enlarged to form the first
cerebral vesicle, from which two lateral diverticula--rudiments of the
optic lobes--are almost at once given off (fig. 108, _op.v_). By the
stage figured the cephalic part of the neural canal has become
distinctly differentiated into a fore- (_f.b_), a mid- (_m.b_) and a
hind-brain (_h.b_); and the hind-brain is often subdivided into
successive lobes. In the region of the hind-brain two shallow
epiblastic invaginations form the rudiments of the auditory pits
(_au.p_).
[FIG. 107. DORSAL VIEW OF THE HARDENED BLASTODERM OF A CHICK WITH
FIVE MESOBLASTIC SOMITES. THE MEDULLARY FOLDS HAVE MET FOR PART OF
THEIR EXTENT, BUT HAVE NOT UNITED.
_a.pr._ anterior part of the primitive streak; _p.pr._ posterior
part of the primitive streak.]
A section through the posterior part of the head of an embryo of 30
hours is represented in fig. 110. The enlarged part of the neural
tube, forming the hind-brain, is shewn at (_hb_). It is still
connected with the epidermis, and at its dorsal border an outgrowth on
each side forming the root of the vagus nerve is present (_vg_). The
notochord (_ch_) is seen below the brain, and below this again the
crescentic foregut (_al_). The commencing heart (_ht_), formed at this
stage of two distinct tubes, is attached to the ventral side of the
foregut.
On the dorsal side of the foregut immediately below the notochord is
seen a small body (_x_) formed as a thickening of the hypoblast. This
may possibly be a rudiment of the subnotochordal rod of the
Ichthyopsida.
[FIG. 108. EMBRYO OF THE CHICK BETWEEN 30 AND 36 HOURS VIEWED FROM
ABOVE AS AN OPAQUE OBJECT. (Chromic acid preparation.)
_f.b._ front-brain; _m.b._ mid-brain; _h.b._ hind-brain; _op.v._
optic vesicle; _au.p._ auditory pit; _o.f._ vitelline vein; _p.v._
mesoblastic somite; _m.f._ line of junction of the medullary folds
above the medullary canal; _s.r._ sinus rhomboidalis; _t._
tail-fold; _p.r._ remains of primitive groove (not satisfactorily
represented); _a.p._ area pellucida.
The line to the side between _p.v._ and _m.f._ represents the true
length of the embryo.
The fiddle-shaped outline indicates the margin of the pellucid area.
The head, which reaches as far back as _o.f._, is distinctly marked
off; but neither the somatopleuric nor splanchnopleuric folds are
shewn in the figure; the latter diverge at the level of _o.f._, the
former considerably nearer the front, somewhere between the lines
_m.b._ and _h.b._ The optic vesicles _op.v._ are seen bulging out
beneath the superficial epiblast. The heart lying underneath the
opaque body cannot be seen. The tail-fold _t._ is just indicated; no
distinct lateral folds are as yet visible in the region midway
between head and tail. At _m.f._ the line of junction between the
medullary folds is still visible, being lost forwards over the
cerebral vesicles, while behind may be seen the remains of the sinus
rhomboidalis, _s.r._]
In the trunk (fig. 108) the chief point to be noticed is the complete
closure of the neural canal, though in the posterior part, where the
open sinus rhomboidalis was situated at an earlier stage, there may
still be seen a dilatation of the canal (fig. 108, _s.r_), on each
side of which are the tail swellings; while the mesoblastic somites
stop short somewhat in front of it. Underneath the neural canal may be
seen the notochord (fig. 109, _ch_) extending into the head, as far as
the base of the mid-brain. At the sides of the trunk are seen the
mesoblastic somites (_p.v_), the outer edges of which mark the
boundary between the vertebral and lateral plates. A fainter line can
be seen marking off the part of the lateral plates which will become
part of the body-wall, from that which pertains to the yolk-sack.
[FIG. 109. AN EMBRYO CHICK OF ABOUT THIRTY-SIX HOURS VIEWED FROM
BELOW AS A TRANSPARENT OBJECT.
_FB._ the fore-brain or first cerebral vesicle, projecting from the
sides of which are seen the optic vesicles _op_. A definite head is
now constituted, the backward limit of the somatopleure fold being
indicated by the faint line _S.O._ Around the head are seen the two
limbs of the amniotic head-fold: one, the true amnion _a_, closely
enveloping the head, the other, the false amnion _a´_, at some
distance from it. The head is seen to project beyond the anterior
limit of the pellucid area.
The splanchnopleure fold extends as far back as _sp_. Along its
diverging limbs are seen the conspicuous venous roots of the
vitelline veins, uniting to form the heart _h_, already established
by the coalescence of two lateral halves which, continuing forward
as the bulbus arteriosus _b.a_, is lost in the substance of the head
just in front of the somatopleure fold.
_HB._ hind-brain; _MB._ mid-brain; _p.v._ and _v.pl._ mesoblastic
somites; _ch._ front end of notochord; _mc._ posterior part of
notochord; _e._ parietal mesoblast; _pl._ outline of area pellucida;
_pv._ primitive streak.]
[FIG. 110. TRANSVERSE SECTION THROUGH THE POSTERIOR PART OF THE HEAD
OF AN EMBRYO CHICK OF THIRTY HOURS.
_hb._ hind-brain; _vg._ vagus nerve; _ep._ epiblast; _ch._
notochord; _x._ thickening of hypoblast (possibly a rudiment of the
subnotochordal rod); _al._ throat; _ht._ heart; _pp._ body cavity;
_so._ somatic mesoblast; _sf._ splanchnic mesoblast; _hy._
hypoblast.]
[FIG. 111. CHICK OF THE THIRD DAY (54 HOURS) VIEWED FROM UNDERNEATH
AS A TRANSPARENT OBJECT.
_a´._ the outer amniotic fold or false amnion. This is very
conspicuous around the head, but may also be seen at the tail.
_a._ the true amnion, very closely enveloping the head, and here
seen only between the projections of the several cerebral vesicles.
It may also be traced at the tail, _t_.
In the embryo of which this is a drawing the head-fold of the amnion
reached a little farther backward than the reference _u_, but its
limit cannot be distinctly seen through the body of the embryo.
_C.H._ cerebral hemisphere; _F.B._ vesicle of the third ventricle;
_M.B._ mid-brain; _H.B._ hind-brain; _Op._ eye; _Ot._ auditory
vesicle.
_OfV._ vitelline veins forming the venous roots of the heart. The
trunk on the right hand (left trunk when the embryo is viewed in its
natural position from above) receives a large branch, shewn by
dotted lines, coming from the anterior portion of the sinus
terminalis. _Ht._ the heart, now completely twisted on itself. _Ao._
the bulbus arteriosus, the three aortic arches being dimly seen
stretching from it across the throat, and uniting into the aorta,
still more dimly seen as a curved dark line running along the body.
The other curved dark line by its side, ending near the reference
_y_, is the notochord _ch_.
About opposite the line of reference _x_ the aorta divides into two
trunks, which running in the line of the somewhat opaque somites on
either side, are not clearly seen. Their branches however, _Of.a_,
the vitelline arteries, are conspicuous and are seen to curve round
the commencing side-folds.
_Pv._ mesoblastic somites.
_x_ is placed at the "point of divergence" of the splanchnopleure
folds. The blind foregut begins here and extends about up to near
_y_, the more transparent space marked by that letter is however
mainly due to the presence there of investing mass at the base of
the brain. _x_ marks the hind limit of the splanchnopleure folds.
The limit of the more transparent somatopleure folds cannot be seen.
It will be of course understood that all the body of the embryo
above the level of the reference _x_, is seen through the portion of
the yolk-sack (vascular and pellucid area), which has been removed
with the embryo from the egg, as well as through the double amniotic
fold.
The view being from below, whatever is described in the natural
position as being to the right appears here to the left, and _vice
versâ_.]
During the latter half of the second day, and during the third day,
great progress is made in the folding off of the embryo. Both the
head- and tail-ends of the embryo become quite distinct, and the
side-folds make such considerable progress that the embryo is only
connected with the yolk by a broad stalk. This stalk is double, and
consists of an inner splanchnic stalk, continuous with the walls of
the alimentary canal, and an outer somatic stalk, continuous with the
body-walls of the embryo. The somatic stalk is very much wider than
the splanchnic. (Compare fig. 121 E and F, which may be taken as
diagrammatic longitudinal and transverse sections of the embryo on the
third day.) A change also takes place in the position of the embryo.
Up to the third day it is placed symmetrically, on the yolk, with its
ventral face downwards. During this day it turns so as partially to
lie on its left side. This rotation affects first the head (fig. 111),
but in the course of the fourth day gradually extends to the rest of
the body (fig. 118). Coincidently with this change in position the
whole embryo undergoes a ventral and somewhat spiral flexure.
During the latter part of the second day and during the third day
important changes take place in the head. One of these is the cranial
flexure. This, which must not be confounded with the curvature of the
body just referred to, commences by the bending downwards of the front
part of the head round a point which may be considered as the extreme
end either of the notochord or of the alimentary canal.
The cranial flexure progresses rapidly, the front-brain being more and
more folded down till, at the end of the third day, it is no longer
the first vesicle or fore-brain, but the second cerebral vesicle or
mid-brain, which occupies the extreme front of the long axis of the
embryo. In fact a straight line through the long axis of the embryo
would now pass through the mid-brain instead of, as at the beginning
of the second day, through the fore-brain, so completely has the front
end of the neural canal been folded over the end of the notochord. The
commencement of this cranial flexure gives the body of an embryo of
the third day somewhat the appearance of a chemist's retort, the head
of the embryo corresponding to the bulb. On the fourth day the flexure
is still greater than on the third, but on the fifth and succeeding
days it becomes less obvious.
The anterior part of the fore-brain has now become greatly dilated,
and may be distinguished from the posterior part as the unpaired
rudiment of the cerebral hemispheres. It soon bulges out laterally
into two lobes, which do not however become separated by a median
partition till a much later period.
[FIG. 112. SIDE VIEW OF THE HEAD OF AN EMBRYO CHICK OF THE THIRD DAY
AS AN OPAQUE OBJECT. (Chromic acid preparation.)
_CH._ Cerebral hemispheres; _F.B._ Vesicle of third ventricle;
_M.B._ Mid-brain; _Cb._ Cerebellum; _H.B._ Medulla oblongata; _N._
Nasal pit; _ot._ auditory vesicle in the stage of a pit with the
opening not yet closed up; _op._ Optic vesicle, with _l._ lens and
_ch.f._ choroidal fissure. The choroidal fissure, though formed
entirely underneath the superficial epiblast, is distinctly visible
from the outside.
_1 F._ The first visceral fold; above it is seen a slight indication
of the superior maxillary process.
_2_, _3_, _4 F._ Second, third and fourth visceral folds, with the
visceral clefts between them.]
Owing to the development of the cerebral rudiment the posterior part
of the fore-brain no longer occupies the front position (fig. 111, and
112 _FB_), and ceases to be the conspicuous object that it was.
Inasmuch as its walls will hereafter be developed into the parts
surrounding the so-called third ventricle of the brain, it is known as
the vesicle of the third ventricle, or the thalamencephalon.
On the summit of the thalamencephalon there may now be seen a small
conical projection, the rudiment of the _pineal gland_, while the
centre of the floor is produced into a funnel-shaped process, the
infundibulum, which, stretching towards the extreme end of the
alimentary canal, joins the pituitary body.
Beyond an increase in size, which it shares with nearly all parts of
the embryo, and the change of position which has already been referred
to, the mid-brain undergoes no great alterations during the third day.
Its sides will ultimately become developed into the corpora bigemina
or optic lobes, its floor will form the crura cerebri, and its cavity
will be reduced to the narrow canal known as the iter a tertio ad
quartum ventriculum and two diverticula leading from this into the
optic lobes.
In the hind-brain, or third cerebral vesicle, the roof of the part
which lies nearest to the mid-brain, becomes during the third day
marked off from the rest by a slight constriction. This distinction,
which becomes much more evident later on by a thickening of the walls
and roof of the front portion, separates the hind-brain into the
cerebellum and the medulla oblongata (fig. 112 _Cb_ and _HB_). While
the walls of the cerebellar portion of the hind-brain become very much
thickened as well at the roof as at the sides, the roof of the
posterior portion or medulla oblongata thins out into a mere membrane,
forming a delicate covering to the cavity of the vesicle (fig. 114
_IV_), which here becoming broad and shallow with greatly thickened
floor and sides, is known as the fourth ventricle, subsequently
overhung by the largely-developed posterior portion of the cerebellum.
[FIG. 113. HEAD OF AN EMBRYO CHICK OF THE FOURTH DAY VIEWED AS AN
OPAQUE OBJECT: FROM THE FRONT IN A, AND FROM THE SIDE IN B. (Chromic
acid preparation.)
_CH._ cerebral hemispheres; _FB._ vesicle of the third ventricle;
_Op._ eyeball; _nf._ nasofrontal process; _M._ cavity of mouth;
_SM._ superior maxillary process of _F. 1_, the first visceral fold
(inferior maxillary process); _F. 2_, _F. 3_, second and third
visceral folds; _N._ nasal pit; _ot._ otic vesicle.
In order to gain the view here given the neck was cut across between
the third and fourth visceral folds. In the section _e_ thus made,
are seen the alimentary canal _al_, the neural canal _n.c._, the
notochord _ch_, the dorsal aorta _AO_, and the vertebral veins _V_.]
The third day, therefore, marks the distinct differentiation of the
brain into five distinct parts: the cerebral hemispheres, the central
masses round the third ventricle, the corpora bigemina, the cerebellum
and the medulla oblongata; the original cavity of the neural canal at
the same time passing from its temporary division of three single
cavities into the permanent arrangement of a series of connected
ventricles, viz. the lateral ventricles, the third ventricle, the iter
(with a prolongation into the optic lobe on each side), and the fourth
ventricle.
By the third day the lens of the eye has become formed by an
invagination of the epiblast, and other changes in the eye have taken
place. The external opening of the auditory pit is closed before the
completion of the third day (fig. 114, _RL_); and the rudiments of the
external parts of the organ of smell have become formed as small pits
on the under surface of the fore-brain (fig. 112, _N_). Like the lens
and the labyrinth of the ear, they are formed as invaginations of the
external epiblast; unlike them they are never closed up.
[FIG. 114. SECTION THROUGH THE HIND-BRAIN OF A CHICK AT THE END OF
THE THIRD DAY OF INCUBATION.
_IV._ Fourth ventricle. The section shews the very thin roof and
thicker sides of the ventricle. _Ch._ Notochord; _CV._ Anterior
cardinal vein; _CC._ Involuted auditory vesicle; _CC_ points to the
end which will form the cochlear canal; _RL._ Recessus labyrinthi
(remains of passage connecting the vesicle with the exterior); _hy._
Hypoblast lining the alimentary canal; _AO._, _AOA._ Aorta, and
aortic arch.]
During the second and third days there are formed the visceral or
branchial clefts, homologous with those of the Ichthyopsida, though
never developing branchial processes from their walls.
They are however real clefts or slits passing right through the walls
of the throat, and are placed in series on either side across the axis
of the alimentary canal, lying not quite at right angles to that axis
nor parallel to each other, but converging somewhat to the middle of
the throat in front (fig. 112 and fig. 113).
Four in number on either side, the anterior is the first to be formed,
the other three following in succession. They originate as pouches of
the hypoblast, which meet the epiblast. At the junction of the
epiblast and hypoblast an absorption of the tissue is effected,
placing the pouches in communication with the exterior.
No sooner has a cleft been formed than its anterior border (_i.e._ the
border nearer the head) becomes raised into a thick lip or fold, the
_visceral_ or _branchial fold_. Each cleft has its own fold on its
anterior border, and in addition the posterior border of the fourth or
last visceral cleft is raised into a similar fold. There are thus
_five_ visceral folds to _four_ visceral clefts (figs. 112 and 113).
The last two folds however, and especially the last, are not nearly so
thick and prominent as the other three, the second being the broadest
and most conspicuous of all. The first fold meets, or nearly meets,
its fellow in the middle line in front, but the second falls short of
reaching the middle line, and the third, fourth and fifth do so in an
increasing degree. Thus in front views of the neck a triangular space
with its apex directed towards the head is observed between the ends
of the several folds (fig. 113 A).
Into this space the pleuroperitoneal cavity extends, the somatopleure
separating from the splanchnopleure along the ends of the folds; and
it is here that the aorta plunges into the mesoblast of the body.
The history of these most important visceral folds and clefts will be
dealt with in detail hereafter; meanwhile I may say that in the Chick
and higher Vertebrates the first three pairs of folds are those which
call for most notice.
The first fold on either side, increasing rapidly in size and
prominence, does not, like the others, remain single, but sends off in
the course of the third day a branch or bud-like process from its
upper edge (fig. 113). This branch, starting from near the outer end
of the fold, runs forwards and upwards in front of the stomodæum,
tending to meet the corresponding branch from the fold on the other
side, at a point in the middle line nearer the front of the head than
the junction of the main folds (fig. 113, _sm_). The two branches do
not quite meet, being separated by a median process, which at the same
time grows down from the extreme front of the head, and against which
they abut (fig. 120, _k_). Between the main folds, which are directed
somewhat downwards and their branches which slant upwards, the
somewhat lozenge-shaped stomodæum is placed, which, as the folds
become more and more prominent, grows deeper and deeper (fig. 120 A).
The main folds form the mandibular arch, and their branches the
maxillary processes, and the descending process which helps to
complete the anterior margin of the stomodæum or oral cavity is
called, from the parts which will be formed out of it, the
_frontonasal process_.
[FIG. 115. TRANSVERSE SECTION THROUGH THE DORSAL REGION OF AN EMBRYO
CHICK OF 45 HOURS.
_M.c._ medullary canal; _P.v._ mesoblastic somite; _W.d._ Wolffian
duct; _So._ Somatopleure; _S.p._ Splanchnopleure; _p.p._
pleuroperitoneal cavity; _ao._ aorta; _v._ blood-vessels; _w._
germinal wall; _ch._ notochord; _op._ junction between area opaca
and area pellucida.]
In two succeeding pairs of visceral folds, which correspond with the
hyoid and first branchial arches of the Ichthyopsida, are developed
the parts of the hyoid bone, which will be best considered in
connection with the development of the skull. The last two disappear
in the Chick without giving rise to any permanent structures. The
external opening of the first visceral _i.e._ hyomandibular cleft
becomes closed[66], but the inner part of the cleft, opening into the
mouth, gives rise to the Eustachian tube and the tympanic cavity, the
latter being formed as a special diverticulum.
[66] _Vide_ Moldenhauer, "Die Entwicklung des mittleren und des
äusseren Ohres." _Morphologisches Jahrbuch_, Vol. III. 1877.
Part of the membranous mandibular and hyoid arches form a wall round
the dorsal part of the original opening of this cleft, and so give
rise to the meatus auditorius externus. At the bottom of this is
placed the tympanic membrane, which is probably derived from the
tissue which grows over the dorsal part of the opening of the first
cleft. It is formed of an external epiblast epithelium, a middle layer
of mesoblast, and an internal hypoblastic epithelium.
[FIG. 116. TRANSVERSE SECTION THROUGH THE TRUNK OF A DUCK EMBRYO
WITH ABOUT TWENTY-FOUR MESOBLASTIC SOMITES.
_am._ amnion; _so._ somatopleure; _sp._ splanchnopleure; _wd._
Wolffian duct; _st._ segmental tube; _ca.v._ cardinal vein; _ms._
muscle-plate; _sp.g._ spinal ganglion; _sp.c._ spinal cord; _ch._
notochord; _ao._ aorta; _hy._ hypoblast.]
The general nature of the changes, which take place in the trunk
between the commencement of the second half of the second day and the
end of the third day, is illustrated by the sections figs. 115, 116,
117.
[FIG. 117. SECTION THROUGH THE DORSAL REGION OF AN EMBRYO CHICK AT
THE END OF THE THIRD DAY.
_Am._ amnion; _m.p._ muscle-plate. _C.V._ cardinal vein. _Ao._
dorsal aorta. The section passes through the point where the dorsal
aorta is just commencing to divide into two branches. _Ch._
notochord; _W.d._ Wolffian duct; _W.b._ commencing differentiation
of the mesoblast cells to form the Wolffian body; _ep._ epiblast;
_So._ somatopleure; _Sp._ splanchnopleure; _hy._ hypoblast. The
section passes through the point where the digestive canal
communicates with the yolk-sack, and is consequently still _open_
below.]
In the earliest of these sections there is not a trace of a folding
off of the embryo from the yolk, and the body walls are quite
horizontal. In the second section (fig. 116), from an embryo of about
two days, the body walls are already partially inclined, and the
splanchnopleure is very distinctly folded inwards. There is a
considerable space between the notochord and the hypoblast, which
forms the rudiment of the mesentery.
In the third section (fig. 117) the body walls have become nearly
vertical, the folding of the splanchnopleure is nearly completed, and
it is only for a small region that the alimentary tract is open, by
the vitelline duct, to the yolk-sack.
[FIG. 118. EMBRYO CHICK AT THE END OF THE FOURTH DAY SEEN AS A
TRANSPARENT OBJECT.
The amnion has been completely removed, the cut end of the somatic
stalk is shewn at _S.S._ with the allantois (_Al_) protruding from
it.
_C.H._ cerebral hemisphere; _F.B._ vesicle of the third ventricle
with the pineal gland (_Pn_) projecting from its summit; _M.B._
mid-brain; _Cb._ cerebellum. _IV. V._ fourth ventricle; _L._ lens;
_ch.s._ choroid slit. Owing to the growth of the optic cup the two
layers of which it is composed cannot any longer be seen from the
surface, but the retinal surface of the layer alone is visible.
_Cen. V._ auditory vesicle; _s.m._ superior maxillary process; _1
F_, _2 F_, etc. first, second, third and fourth visceral arches;
_V._ fifth nerve sending one branch to the eye, the ophthalmic
branch, and another to the first visceral arch; _VII._ seventh nerve
passing to the second visceral arch; _G.Ph._ glossopharyngeal nerve
passing towards the third visceral arch; _Pg._ pneumogastric nerve
passing towards the fourth visceral arch; _iv._ investing mass. No
attempt has been made in the figure to indicate the position of the
dorsal wall of the throat, which cannot be easily made out in the
living embryo; _ch._ notochord. The front end of this cannot be seen
in the living embryo. It does not end however as shewn in the
figure, but takes a sudden bend downwards and then terminates in a
point. _Ht._ heart seen through the walls of the chest; _M.P._
muscle-plates. _W._ wing; _H.L._ hind limb. Beneath the hind limb is
seen the curved tail.]
These three sections further illustrate (1) the gradual
differentiation of the mesoblastic somites (fig. 115, _P.v_) into
(_a_) the muscle-plates (figs. 116, _ms_ and 117, _m.p_), and (_b_)
the tissue to form the vertebral bodies and adjacent connective
tissue; (2) the formation of a mass of tissue between the lateral
plates and the mesoblastic somites (fig. 115), known as the
intermediate cell mass, on the dorsal side of which the Wolffian duct
is formed, while the intermediate cell mass itself breaks up into the
segmental tubes (fig. 116, _st_) and connective tissue of the Wolffian
body.
[FIG. 119. SECTION THROUGH THE LUMBAR REGION OF AN EMBRYO CHICK AT
THE END OF THE FOURTH DAY.
_n.c._ neural canal; _p.r._ posterior root of spinal nerve with
ganglion; _a.r._ anterior root of spinal nerve; _A.G.C._ anterior
grey column of spinal cord; _A.W.C._ anterior white column of spinal
cord just commencing to be formed, and not very distinctly marked in
the figure; _m.p._ muscle-plate; _ch._ notochord; _W.R._ Wolffian
ridge; _AO._ dorsal aorta; _V.c.a._ posterior cardinal vein; _W.d._
Wolffian duct; _W.b._ Wolffian body, consisting of tubules and
Malpighian bodies; _g.e._ germinal epithelium; _d._ alimentary
canal; _M._ commencing mesentery; _SO._ somatopleure; _SP._
splanchnopleure; _V._ blood-vessels; _pp._ pleuroperitoneal cavity.]
Various other features in the development of the vascular system,
general mesoblast, etc., are also represented in these sections. It
may more especially be noted that there are at first two widely
separated dorsal aortæ, which gradually approach (figs. 115 and 116);
and meeting first of all in front finally coalesce (figs. 117 and 119)
for their whole length.
The general appearance of the embryo of the fourth day may be gathered
from fig. 118.
[FIG. 120. HEAD OF A CHICK FROM BELOW ON THE SIXTH AND SEVENTH DAYS
OF INCUBATION. (From Huxley.)
_I^a._ cerebral vesicles; _a._ eye, in which the remains of the
choroid slit can still be seen in A; _g._ nasal pits; _k._
frontonasal process; _l._ superior maxillary process; _1._ inferior
maxillary process or first visceral arch; _2._ second visceral arch;
_x._ first visceral cleft.
In A the cavity of the mouth is seen enclosed by the frontonasal
process, the superior maxillary processes and the first pair of
visceral arches. At the back of it is seen the opening leading into
the throat. The nasal grooves leading from the nasal pits to the
mouth are already closed over and converted into canals.
In B the external opening of the mouth has become much constricted,
but it is still enclosed by the frontonasal process and superior
maxillary processes above, and by the inferior maxillary processes
(first pair of visceral arches) below.
The superior maxillary processes have united with the frontonasal
process, along nearly the whole length of the latter.]
The changes which have taken place consist for the most part in the
further development of the parts already present, and do not need to
be specified in detail. The most important event of the day is perhaps
the formation of the limbs. They appear as outgrowths from a slightly
marked lateral ridge (fig. 119, _WR_), which runs on the level of the
lower end of the muscle-plates for nearly the whole length of the
trunk. This ridge is known as the Wolffian ridge. The first trace of
the limbs can be seen towards the end of the third day; and their
appearance at the end of the fourth day is shown in fig. 118, _W_ and
_HL_.
A section through the trunk of the embryo on the fourth day is
represented in fig. 119. The section passes through the region of the
trunk behind the vitelline duct. The mesentery (_M_) is very much
deeper and thinner than on the previous day. The notochord has become
invested by a condensed mesoblastic tissue, which will give rise to
the vertebral column. The two dorsal aortæ have now completely
coalesced into the single dorsal aorta, and the Wolffian body has
reached a far more complete development.
In the course of the fifth day the face begins to assume a less
embryonic character, and by the sixth and succeeding days presents
distinctive avian characters.
The general changes which take place between the sixth day and the
time of hatching do not require to be specified in detail.
_Foetal Membranes._
The Reptilia, Aves and Mammalia are distinguished from the
Ichthyopsida by the possession of certain provisional foetal
membranes, known as the amnion and allantois.
As the mode of development of these membranes may be most conveniently
studied in the Chick, I have selected this type for their detailed
description.
The Amnion. The amnion is a peculiar sack which envelopes and protects
the embryo.
At the end of the first day of incubation, when the cleavage of the
mesoblast has somewhat advanced, there appears, a little way in front
of the semilunar head-fold, a second fold (fig. 102, also fig. 121 C,
_af_ and fig. 122, _Am_), running more or less parallel or rather
concentric with the first and not unlike it in general appearance,
though differing widely from it in nature. This second fold gives rise
to the amnion, and is limited entirely to the somatopleure. Rising up
as a semilunar fold with its concavity directed towards the embryo
(fig. 121 C, _af_), as it increases in height it is gradually drawn
backwards over the developing head of the embryo. The fold thus
covering the head is in due time accompanied by similar folds of
somatopleure, starting at some little distance behind the tail, and at
some little distance from the side (fig. 121 C, D, E, F, and 116,
_am_). In this way the embryo becomes surrounded by a series of folds
of thin somatopleure, which form a continuous wall all round it. All
are drawn gradually over the body of the embryo, and at last meet and
completely coalesce (fig. 121, H, I, and 117, _Am_), all traces of
their junction being removed. Beneath these united folds there is
therefore a cavity, within which the embryo lies (fig. 121 H, _ae_).
This cavity is the cavity of the amnion.
[FIG. 121. A to N forms a series of purely diagrammatic
representations introduced to facilitate the comprehension of the
manner in which the body of the embryo is formed, and of the various
relations of the yolk-sack, amnion, and allantois.
In all _vt_ is the vitelline membrane, placed, for convenience sake,
at some distance from its contents, and represented as persisting in
the later stages; in reality it is in direct contact with the
blastoderm or yolk, and early ceases to have a separate existence.
In all _e_ indicates the embryo proper; _pp_ the general
pleuroperitoneal space with its extension between the membranes;
_af_ the folds of the amnion; _a_ the amnion proper; _ae_ or _ac_
the cavity holding the liquor amnii; _al_ the allantois; _a´_ the
alimentary canal; _y_ or _ys_ the yolk or yolk-sack.
A, which may be considered as a vertical section taken
longitudinally along the axis of the embryo, represents the
relations of the parts of the egg at the time of the first
appearance of the head-fold, seen on the right-hand side of the
embryo _e_. The blastoderm is spreading both behind (to the left
hand in the figure), and in front (to right hand) of the head-fold,
its limits being indicated by the shading and thickening for a
certain distance of the margin of the yolk _y_. As yet there is no
fold on the left side of _e_ corresponding to the head-fold on the
right.
B is a vertical transverse section of the same period drawn for
convenience sake on a larger scale (it should have been made flatter
and less curved). It shews that the blastoderm (vertically shaded)
is extending laterally as well as fore and aft, in fact in all
directions; but there are no lateral folds, and therefore no lateral
limits to the body of the embryo as distinguished from the
blastoderm.
Incidentally it shews the formation of the medullary groove by the
rising up of the laminæ dorsales. Beneath the section of the groove
is seen the rudiment of the notochord. On either side a line
indicates the cleavage of the mesoblast just commencing.
In C, which represents a vertical longitudinal section of later
date, both head-fold (on the right) and tail-fold (on the left) have
advanced considerably. The alimentary canal is therefore closed in,
both in front and behind, but is in the middle still widely open to
the yolk _y_ below. Though the axial parts of the embryo have become
thickened by growth, the body-walls are still thin; in them however
is seen the cleavage of the mesoblast, and the divergence of the
somatopleure and splanchnopleure. The splanchnopleure both at the
head and at the tail is folded in to a greater extent than the
somatopleure, and forms the still wide splanchnic stalk. At the end
of the stalk, which is as yet short, it bends outwards again and
spreads over the surface of the yolk. The somatopleure, folded in
less than the splanchnopleure to form the wider somatic stalk,
sooner bends round and runs outwards again. At a little distance
from both the head and the tail it is raised up into a fold, _af_,
_af_, that in front of the head being the highest. These are the
amniotic folds. Descending from either fold, it speedily joins the
splanchnopleure again, and the two, once more united into an uncleft
membrane, extend some way downwards over the yolk, the limit or
outer margin of the opaque area not being shewn. All the space
between the somatopleure and the splanchnopleure is shaded with
dots, _pp_. Close to the body this space may be called the
pleuroperitoneal cavity; but outside the body it runs up into either
amniotic fold, and also extends some little way over the yolk.
D represents the tail end at about the same stage on a more enlarged
scale, in order to illustrate the position of the allantois _al_
(which was for the sake of simplicity omitted in C), shewn as a bud
from the splanchnopleure, stretching downwards into the
pleuroperitoneal cavity _pp_. The dotted area representing as before
the whole space between the splanchnopleure and the somatopleure, it
is evident that a way is open for the allantois to extend from its
present position into the space between the two limbs of the
amniotic fold _af_.
E, also a longitudinal section, represents a stage still farther
advanced. Both splanchnic and somatic stalks are much narrowed,
especially the former, the cavity of the alimentary canal being now
connected with the cavity of the yolk by a mere canal. The folds of
the amnion are spreading over the top of the embryo and nearly meet.
Each fold consists of two walls or limbs, the space between which
(dotted) is as before merely a part of the space between the
somatopleure and splanchnopleure. Between these arched amniotic
folds and the body of the embryo is a space not as yet entirely
closed in.
F represents on a different scale a transverse section of E taken
through the middle of the splanchnic stalk. The dark ring in the
body of the embryo shews the position of the neural canal, below
which is a black spot, marking the notochord. On either side of the
notochord the divergence of somatopleure and splanchnopleure is
obvious. The splanchnopleure, more or less thickened, is somewhat
bent in towards the middle line, but the two sides do not unite, the
alimentary canal being as yet open below at this spot; after
converging somewhat they diverge again and run outwards over the
yolk. The somatopleure, folded in to some extent to form the
body-walls, soon bends outwards again, and is almost immediately
raised up into the lateral folds of the amnion _af_. The continuity
of the pleuroperitoneal cavity, within the body, with the interior
of the amniotic fold, outside the body, is evident; both cavities
are dotted.
G, which corresponds to D at a later stage, is introduced to shew
the manner in which the allantois, now a considerable hollow body,
whose cavity is continuous with that of the alimentary canal,
becomes directed towards the amniotic fold.
In H a longitudinal, and I a transverse section of later date, great
changes have taken place. The several folds of the amnion have met
and coalesced above the body of the embryo. The inner limbs of the
several folds have united into a single membrane (_a_), which
encloses a space (_ae_ or _ac_) round the embryo. This membrane _a_
is the amnion proper, and the cavity within it, _i.e._ between it
and the embryo, is the cavity of the amnion containing the liquor
amnii. The allantois is omitted for the sake of simplicity.
It will be seen that the amnion _a_ now forms in every direction the
termination of the somatopleure; the peripheral portions of the
somatopleure, the united outer or descending limbs of the folds _af_
in C, D, F, G having been cut adrift, and now forming an independent
continuous membrane, the serous membrane, immediately underneath the
vitelline membrane.
In I the splanchnopleure is seen converging to complete the closure
of the alimentary canal _a´_ even at the stalk (elsewhere the canal
has of course long been closed in), and then spreading outwards as
before over the yolk. The point at which it unites with the
somatopleure, marking the extreme limit of the cleavage of the
mesoblast, is now much nearer the lower pole of the diminished yolk.
As a result of these several changes, a great increase in the dotted
space has taken place. It is now possible to pass from the actual
peritoneal cavity within the body, on the one hand round a great
portion of the circumference of the yolk, and on the other hand
above the amnion _a_, in the space between it and the serous
envelope.
Into this space the allantois is seen spreading in K at _al_.
In L the splanchnopleure has completely invested the yolk-sack, but
at the lower pole of the yolk is still continuous with that
peripheral remnant of the somatopleure now called the serous
membrane. In other words, cleavage of the mesoblast has been carried
all round the yolk (_ys_) except at the very lower pole.
In M the cleavage has been carried through the pole itself; the
peripheral portion of the splanchnopleure forms a complete
investment of the yolk quite unconnected with the peripheral portion
of the somatopleure, which now exists as a continuous membrane
lining the interior of the shell. The yolk-sack (_ys_) is therefore
quite loose in the pleuroperitoneal cavity, being connected only
with the alimentary canal (_a´_) by a solid pedicle.
Lastly, in N the yolk-sack (_ys_) is shewn being withdrawn into the
cavity of the body of the embryo. The allantois is as before, for
the sake of simplicity, omitted; its pedicle would of course lie by
the side of _ys_ in the somatic stalk marked by the usual dotted
shading.
It may be repeated that the above are diagrams, the various spaces
being shewn distended, whereas in many of them in the actual egg the
walls have collapsed, and are in near juxtaposition.]
[FIG. 122. DIAGRAMMATIC LONGITUDINAL SECTION THROUGH THE AXIS OF AN
EMBRYO.
The section is supposed to be made at a time when the head-fold has
commenced but the tail-fold has not yet appeared.
_F.So._ fold of the somatopleure. _F.Sp._ fold of the
splanchnopleure; _D._ foregut.
_pp._ pleuroperitoneal cavity between somatopleure and
splanchnopleure; _Am._ commencing (head) fold of the amnion. For
remaining reference letters _vide_ p. 167.]
Each fold is necessarily formed of two limbs, both limbs consisting of
epiblast and a very thin layer of mesoblast; but in one limb the
epiblast looks towards the embryo, while in the other it looks away
from it. The space between the two limbs of the fold, as can easily be
seen in fig. 121, is really part of the space between the somatopleure
and splanchnopleure; it is therefore continuous with the general
space, part of which afterwards becomes the pleuroperitoneal cavity of
the body, shaded with dots in the figure and marked (_pp_); so that it
is possible to pass from the cavity between the two limbs of the
amniotic folds into the cavity which surrounds the alimentary canal.
When the several folds meet and coalesce together above the embryo,
they unite in such a way that all their inner limbs unite to form a
continuous inner membrane or sack, and all their outer limbs a
similarly continuous outer membrane or sack. The inner membrane thus
built up forms a completely closed sack round the body of the embryo,
and is called the amniotic sack, or _amnion proper_ (fig. 121, H, I,
&c., _a_), and the fluid which it afterwards contains is called the
amniotic fluid, or _liquor amnii_. The space between the inner and
outer sack is, from the mode of its formation, simply a part of the
general cavity found everywhere between somatopleure and
splanchnopleure. The outer sack over the embryo lies close under the
vitelline membrane, and the cavity between it and the true amnion is
gradually extended over the whole yolk-sack.
The actual manner in which the amniotic folds meet is somewhat
peculiar (His and Kölliker). The head-fold of the amnion is the
earliest formed, and completely covers over the head before the end of
the second day. The side and tail folds are later in developing. The
side-folds finally meet in the dorsal line, and their coalescence
proceeds backwards from the head-fold in a linear direction, till
there is only a small opening left over the tail. This also becomes
closed early on the third day.
The allantois[67] is essentially a diverticulum of the alimentary
tract into which it opens immediately in front of the anus. Its walls
are formed of splanchnic mesoblast with blood-vessels, within which is
a lining of hypoblast. It becomes a conspicuous object on the third
day of incubation, but its first development takes place at an earlier
period, and is intimately connected with the formation of the
posterior section of the gut.
[67] For details on the development of the allantois the reader
is referred to the works of Kölliker (No. 135), Gasser (No. 127),
and for a peculiar view on the subject Kupffer (No. 136). In
addition to these works he may refer to Dobrynin "Ueber die erste
Anlage der Allantois." _Sitz. der k. Akad. Wien_, Bd. 64, 1871.
E. Gasser, _Beiträge zur Entwicklungsgeschichte d. Allantois_,
etc.
At the time of the folding in of the hinder end of the mesenteron the
splitting of the mesoblast into somatopleure and splanchnopleure has
extended up to the border of the hinder division of the primitive
streak. As has been already mentioned, the ventral wall of the
postanal section of the alimentary tract is formed by the primitive
streak. Immediately in front of this is the involution which forms the
proctodæum; while the wall of the hindgut in front of the anus owes
its origin to a folding in of the splanchnopleure.
The allantois first appears as a protuberance of the splanchnopleure
just in front of the anus. This protuberance arises, however, before
the splanchnopleure has begun to be tucked in so as to form the
ventral wall of the hindgut; and it then forms a diverticulum (fig.
123 A, _All_) the open end of which is directed forward, while its
blind end points somewhat upwards and towards the peritoneal space
behind the embryo.
[FIG. 123. TWO LONGITUDINAL SECTIONS OF THE TAIL-END OF AN EMBRYO
CHICK TO SHEW THE ORIGIN OF THE ALLANTOIS. A AT THE BEGINNING OF THE
THIRD DAY; B AT THE MIDDLE OF THE THIRD DAY. (After Dobrynin.)
_t._ the tail; _m._ the mesoblast of the body, about to form the
mesoblastic somites; _x´._ the roof of _x´´._ the neural canal;
_Dd._ the hind end of the hindgut; _So._ somatopleure; _Spl._
splanchnopleure; _u._ the mesoblast of the splanchnopleure carrying
the vessels of the yolk-sack; _pp._ pleuroperitoneal cavity; _Df._
the epithelium lining the pleuroperitoneal cavity; _All._ the
commencing allantois; _w._ projection formed by anterior and
posterior divisions of the primitive streak; _y._ hypoblast which
will form the ventral wall of the hindgut; _v._ anal invagination;
_G._ cloaca.]
As the hindgut becomes folded in the allantois shifts its position,
and forms (figs. 123 B and 124) a rather wide vesicle lying
immediately below the hind end of the digestive canal, with which it
communicates freely by a still considerable opening; its blind end
projects into the pleuroperitoneal cavity below.
Still later the allantois grows forward, and becomes a large spherical
vesicle, still however remaining connected with the cloaca by a narrow
canal which forms its neck or stalk (fig. 121 G, _al_). From the first
the allantois lies in the pleuroperitoneal cavity. In this cavity it
grows forwards till it reaches the front limit of the hindgut, where
the splanchnopleure turns back to enclose the yolk-sack. It does not
during the third day project beyond this point; but on the fourth day
begins to pass out beyond the body of the chick, along the as yet wide
space between the splanchnic and somatic stalks of the embryo, on its
way to the space between the external and internal folds of the
amnion, which it will be remembered is directly continuous with the
pleuroperitoneal cavity (fig. 121 K). In this space it eventually
spreads out over the whole body of the chick. On the first half of the
fourth day the vesicle is still very small, and its growth is not very
rapid. Its mesoblast wall still remains very thick. In the latter half
of the day its growth becomes very rapid, and it forms a very
conspicuous object in a chick of that date (fig. 118, _Al_). At the
same time its blood-vessels become important. It receives its supply
of blood from two branches of the iliac arteries known as the
allantoic arteries[68], and the blood is brought back from it by two
allantoic veins which run along in the body walls (fig. 119) and after
uniting into a single trunk fall into the vitelline vein close behind
the liver.
[68] I propose to call these arteries and the corresponding veins
the allantoic arteries and veins, instead of using the confusing
term 'umbilical.'
[FIG. 124. DIAGRAMMATIC LONGITUDINAL SECTION THROUGH THE POSTERIOR
END OF AN EMBRYO BIRD AT THE TIME OF THE FORMATION OF THE ALLANTOIS.
_ep._ epiblast; _Sp.c._ spinal canal; _ch._ notochord; _n.e._
neurenteric canal; _hy._ hypoblast; _p.a.g._ postanal gut; _pr._
remains of primitive streak folded in on the ventral side; _al._
allantois; _me._ mesoblast; _an._ point where anus will be formed;
_p.c._ perivisceral cavity; _am._ amnion; _so._ somatopleure; _sp._
splanchnopleure.]
Before dealing with the later history of the foetal membranes, it will
be convenient to complete the history of the yolk-sack.
Yolk-Sack. The origin of the area opaca has already been described. It
rapidly extends over the yolk underneath the vitelline membrane; and
is composed of epiblast and of the hypoblast of the germinal wall
continuous with that of the area pellucida, which on the fourth day
takes the form of a more or less complete layer of columnar cells[69].
Between the epiblast and hypoblast there is a layer of mesoblast,
which does not extend as far as the two other layers. The yolk is
completely surrounded by the seventh day.
[69] Further investigations are required as to the character of
this layer.
[FIG. 125. DIAGRAM OF THE CIRCULATION OF THE YOLK-SACK AT THE END OF
THE THIRD DAY OF INCUBATION.
_H._ heart; _AA._ the second, third and fourth aortic arches; the
first has become obliterated in its median portion, but is continued
at its proximal end as the external carotid, and at its distal end
as the internal carotid; _AO._ dorsal aorta; _L.Of.A._ left
vitelline artery; _R.Of.A._ right vitelline artery; _S.T._ sinus
terminalis; _L.Of._ left vitelline vein; _R.Of._ right vitelline
vein; _S.V._ sinus venosus; _D.C._ ductus Cuvieri; _S.Ca.V._
superior cardinal vein; _V.Ca._ inferior cardinal vein. The veins
are marked in outline and the arteries are black. The whole
blastoderm has been removed from the egg and is supposed to be
viewed from below. Hence the left is seen on the right, and _vice
versâ_.]
Towards the end of the first day blood-vessels begin to be developed
in the inner part of the mesoblast of the area opaca. Their
development is completed on the second day; and the region through
which they extend is known as the area vasculosa. The area vasculosa
also grows round the yolk, and completely encloses it not long after
the area opaca. The part of the blastoderm which thus encloses the
yolk forms the yolk-sack. The splitting of the mesoblast gradually
extends to the mesoblast of the yolk-sack, and eventually the
somatopleure of the sack, which is continuous, it will be remembered,
with the outer limb of the amnion, separates completely from the
splanchnopleure; and between the two the allantois inserts itself.
These features are represented in fig. 121 E, K, and L.
The circulation of the yolk-sack is most important during the third
day of incubation. The arrangement of the vessels during that day is
shewn in fig. 125.
The blood leaving the body of the embryo by the vitelline arteries
(fig. 125, _R.Of.A_, _L.Of.A_), which are branches of the dorsal
aortæ, is carried to the small vessels and capillaries of the vascular
area, a small portion only being appropriated by the pellucid area.
From the vascular area part of the blood returns directly to the sinus
venosus by the main lateral trunks of the vitelline veins (_R.Of_,
_L.Of_), and so to the heart. During the second day these venous
trunks join the body of the embryo considerably in front of, that is
nearer, the head than the corresponding arterial ones. Towards the end
of the third day, owing to the continued lengthening of the heart, the
veins and arteries run not only parallel to each other, but almost in
the same line, the points at which they respectively join and leave
the body being nearly at the same distance from the head.
The rest of the blood brought by the vitelline arteries finds its way
into the lateral portions of a venous trunk bounding the vascular
area, which is known as the sinus terminalis, _S.T._, and there
divides on each side into two streams. Of these, the two which, one on
either side, flow backward, meet at a point about opposite to the tail
of the embryo, and are conveyed along a distinct vein which, running
straight forward parallel to the axis of the embryo, empties itself
into the left vitelline vein. The two forward streams reaching a gap
in the front part of the sinus terminalis fall into either one, or in
some cases two veins, which run straight backwards parallel to the
axis of the embryo, and so reach the roots of the heart. When one such
vein only is present it joins the left vitelline trunk; where there
are two they join the left and right vitelline trunks respectively.
The left vein is always considerably larger than the right; and the
latter when present rapidly gets smaller and speedily disappears.
After the third day, although the vascular area goes on increasing in
size until it finally all but encompasses the yolk, the prominence of
the sinus terminalis becomes less and less.
The foetal membranes and the yolk-sack may conveniently be treated of
together in the description of their later changes and final fate.
On the sixth and seventh days they exhibit changes of great
importance.
The amnion, at its complete closure on the fourth day, very closely
invested the body of the chick: the true cavity of the amnion was then
therefore very small. On the fifth day fluid begins to collect in the
cavity, and raises the membrane of the amnion to some distance from
the embryo. The cavity becomes still larger by the sixth day, and on
the seventh day is of very considerable dimensions, the fluid
increasing with it. On the sixth day Von Baer observed movements of
the embryo, chiefly of the limbs; he attributes them to the
stimulation of the cold air on opening the egg. By the seventh day
very obvious movements begin to appear in the amnion itself; slow
vermicular contractions creeping rhythmically over it. The amnion in
fact begins to pulsate slowly and rhythmically, and by its pulsation
the embryo is rocked to and fro in the egg. This pulsation is probably
due to the contraction of involuntary muscular fibres, which seem to
be present in the attenuated portion of the mesoblast, forming part of
the amniotic fold. Similar movements are also seen in the allantois at
a considerably later period.
The growth of the allantois has been very rapid, and it forms a
flattened bag, covering the right side of the embryo, and rapidly
spreading out in all directions between the primitive folds of the
amnion, that is, between the amnion proper and the false amnion or
serous envelope. It is filled with fluid, so that in spite of its
flattened form its opposite walls are distinctly separated from each
other.
The vascular area has become still further extended than on the fifth
day, but with a corresponding loss in the definite character of its
blood-vessels. The sinus terminalis has indeed by the end of the
seventh day lost all its previous distinctness; and the vessels which
brought back the blood from it to the heart are no longer to be seen.
Both the vitelline arteries and veins now pass to and from the body of
the chick as single trunks, assuming more and more the appearance of
being merely branches of the mesenteric vessels.
The yolk is still more fluid than on the previous day, and its bulk
has (according to von Baer) increased. This can only be due to its
absorbing the white of the egg, which indeed is diminishing rapidly.
During the eighth, ninth, and tenth days, the amnion does not undergo
any very important changes. Its cavity is still filled with fluid, and
on the eighth day its pulsations are at their height, henceforward
diminishing in intensity.
The splitting of the mesoblast has now extended to the outer limit of
the vascular area, _i.e._ over about three-quarters of the yolk-sack.
The somatopleure at this point is continuous (as can be easily seen by
reference to fig. 121) with the original outer fold of the amnion. It
thus comes about that the further splitting of the mesoblast merely
enlarges the cavity in which the allantois lies. The growth of this
organ keeps pace with that of the cavity in which it is placed. Spread
out over the greater part of the yolk-sack as a flattened bag filled
with fluid, it now serves as the chief organ of respiration. It is
indeed very vascular and a marked difference may be observed between
the colour of the blood in the outgoing and the returning vessels.
The yolk now begins to diminish rapidly in bulk. The yolk-sack becomes
flaccid, and on the eleventh day is thrown into a series of internal
folds, abundantly supplied by large venous trunks. By this means the
surface of absorption is largely increased, and the yolk is more and
more rapidly taken up by the blood-vessels, and in a partially
assimilated condition transferred to the body of the embryo[70].
[70] For details on this subject _vide_ A. Courty, "Structure des
Appendices Vitellins chez le Poulet." _An. Sci. Nat._ Ser. III.
Vol. IX. 1848.
By the eleventh day the abdominal parietes, though still much looser
and less firm than the walls of the chest, may be said to be
definitely established; and the loops of intestine, which have
hitherto been hanging down into the somatic stalk, are henceforward
confined within the cavity of the abdomen. The body of the embryo is
therefore completed; but it still remains connected with its various
appendages by a narrow somatic umbilicus, in which run the stalk of
the allantois and the solid cord suspending the yolk-sack.
The cleavage of the mesoblast is still progressing, and the yolk is
completely invested by a splanchnopleural sack.
The allantois meanwhile spreads out rapidly, and lies over the embryo
close under the shell, being separated from the shell membrane by
nothing more than the attenuated serous envelope, formed out of the
outer primitive fold of the amnion and the remains of the vitelline
membrane. With this membrane the allantois partially coalesces, and in
opening an egg at the later stages of incubation, unless care be
taken, the allantois is in danger of being torn in the removal of the
shell-membrane. As the allantois increases in size and importance, the
allantoic vessels are correspondingly developed.
On about the sixteenth day, the white having entirely disappeared, the
cleavage of the mesoblast is carried right over the pole of the yolk
opposite the embryo, and is thus completed (fig. 121). The yolk-sack
now, like the allantois which closely wraps it all round, lies loose
in a space bounded outside the body by the serous membrane, and
continuous with the pleuroperitoneal cavity of the body of the embryo.
Deposits of urates now become abundant in the allantoic fluid.
The loose and flaccid walls of the abdomen enclose a space which the
empty intestines are far from filling, and on the nineteenth day the
yolk-sack, diminished greatly in bulk but still of some considerable
size, is withdrawn through the somatic stalk into the abdominal
cavity, which it largely distends. Outside the embryo there now
remains nothing but the highly vascular allantois and the bloodless
serous membrane and amnion. The amnion, whose fluid during the later
days of incubation rapidly diminishes, is continuous at the umbilicus
with the body-walls of the embryo. The serous membrane (or outer
primitive amniotic fold) is, by the completion of the cleavage of the
mesoblast and the withdrawal of the yolk-sack, entirely separated from
the embryo. The cavity of the allantois, by means of its stalk passing
through the umbilicus, is of course continuous with the cloaca.
When the chick is about to be hatched it thrusts its beak through the
egg-membranes and begins to breathe the air contained in the air
chamber. Thereupon the pulmonary circulation becomes functionally
active, and at the same time blood ceases to flow through the
allantoic arteries. The allantois shrivels up, the umbilicus becomes
completely closed, and the chick, piercing the shell at the broad end
of the egg with repeated blows of its beak, casts off the dried
remains of allantois, amnion and serous membrane, and steps out into
the world.
BIBLIOGRAPHY.
(117) K. E. von Baer. _Ueb. Entwicklungsgeschichte d. Thiere._
Königsberg, 1828-1837.
(118) F. M. Balfour. "The development and growth of the layers of the
Blastoderm," and "On the disappearance of the Primitive Groove in the
Embryo Chick." _Quart. J. of Micros. Science_, Vol. XIII. 1873.
(119) M. Braun. "Die Entwicklung d. Wellenpapagei's." Part I. _Arbeit.
d. zool.-zoot. Instit. Würzburg._ Vol. V. 1879.
(120) M. Braun. "Aus d. Entwick. d. Papageien; I. Rückenmark; II.
Entwicklung d. Mesoderms; III. Die Verbindungen zwischen Rückenmark u.
Darm bei Vögeln." _Verh. d. phys.-med. Ges. zu Würzburg._ N. F. Bd.
XIV. and XV. 1879 and 1880.
(121) J. Disse. "Die Entwicklung des mittleren Keimblattes im
Hühnerei." _Archiv für mikr. Anat._, Vol. XV. 1878.
(122) J. Disse. "Die Entstehung d. Blutes u. d. ersten Gefässe im
Hühnerei." _Archiv f. mikr. Anat._, Vol. XVI. 1879.
(123) Fr. Durante. "Sulla struttura della macula germinativa delle
uova di Gallina." _Ricerche nel Laboratorio di Anatomia della R.
Università di Roma._
(124) E. Dursy. _Der Primitivstreif des Hühnchens._ 1867.
(125) M. Duval. "Etude sur la ligne primitive de l'embryon de Poulet."
_Annales des Sciences Naturelles_, Vol. VII. 1879.
(126) M. Foster and F. M. Balfour. _Elements of Embryology._ Part I.
London, 1874.
(127) Gasser. "Der Primitivstreifen bei Vogelembryonen." _Schriften
d. Gesell. zur Beförd. d. gesammten Naturwiss. zu Marburg_, Vol. II.
Supplement I. 1879.
(128) A. Götte. "Beiträge zur Entwicklungsgeschichte d. Wirbelthiere.
II. Die Bildung d. Keimblatter u. d. Blutes im Hühnerei." _Archiv für
mikr. Anat._, Vol. X. 1874.
(129) V. Hensen. "Embryol. Mitth." _Archiv f. mikr. Anat._, Vol. III.
1867.
(130) W. His. _Untersuch. üb. d. erste Anlage d. Wirbelthierleibes._
Leipzig, 1868.
(131) W. His. _Unsere Körperform und das physiol. Problem ihrer
Entstehung._ Leipzig, 1875.
(132) W. His. "Der Keimwall des Hühnereies u. d. Entstehung d.
parablastischen Zellen." _Zeit. f. Anat. u. Entwicklungsgeschichte._
Bd. I. 1876.
(133) W. His. "Neue Untersuchungen üb. die Bildung des Hühnerembryo
I." _Archiv f. Anat. u. Phys._ 1877.
(134) E. Klein. "Das mittlere Keimblatt in seiner Bezieh. z. Entwick.
d. ers. Blutgefässe und Blutkörp. im Hühnerembryo." _Sitzungsber.
Wien. Akad._, Vol. LXIII. 1871.
(135) A. Kölliker. _Entwicklungsgeschichte d. Menschen u. d. höheren
Thiere._ Leipzig, 1879.
(136) C. Kupffer. "Die Entsteh. d. Allantois u. d. Gastrula d.
Wirbelth." _Zoolog. Anzeiger_, Vol. II. 1879, pp. 520, 593, 612.
(137) C. Kupffer and B. Benecke. "Photogramme z. Ontogenie d. Vögel."
_Nov. Act. d. k. Leop.-Carol.-Deutschen Akad. d. Naturforscher_, Vol.
XLI. 1879.
(138) J. Oellacher. "Untersuchungen über die Furchung u.
Blatterbildung im Hühnerei." _Stricker's Studien._ 1870.
(139) C. H. Pander. _Beiträge z. Entwick. d. Hühnchens im Eie._
Würzburg, 1817.
(140) A. Rauber. "Ueber die Embryonalanlage des Hühnchens."
_Centralblatt für d. medic. Wissenschaften._ 1874-75.
(141) A. Rauber. _Ueber die Stellung des Hühnchens im
Entwicklungsplan._ 1876.
(142) A. Rauber. "Primitivrinne und Urmund. Beiträge zur
Entwicklungsgeschichte des Hühnchens." _Morphol. Jahrbuch_, B. II.
1876.
(143) A. Rauber. _Primitivstreifen und Neurula der Wirbelthiere in
normaler und pathologischer Beziehung._ 1877.
(144) R. Remak. _Untersuch. üb. d. Entwicklung d. Wirbelthiere._
Berlin, 1850-55.
(145) S. L. Schenk. "Beiträge z. Lehre v. d. Organanlage im
motorischen Keimblatt." _Sitz. Wien. Akad._, Vol. LVII. 1860.
(146) S. L. Schenk. "Beiträge z. Lehre v. Amnion." _Archiv f. mikr.
Anat._, Vol. VII. 1871.
(147) S. L. Schenk. _Lehrbuch d. vergleich. Embryol. d. Wirbelthiere._
Wien, 1874.
(148) S. Stricker. "Mittheil. üb. d. selbstständigen Bewegungen
embryonaler Zellen." _Sitz. Wien. Akad._, Vol. XLIX. 1864.
(149) S. Stricker. "Beiträge zur Kenntniss des Hühnereies." _Wiener
Sitzungsber._, Vol. LIV. 1866.
(150) H. Virchow. _Ueber d. Epithel d. Dottersackes im Hühnerei._
Inaug. Diss. Berlin, 1875.
(151) W. Waldeyer. "Ueber die Keimblätter und den Primitivstreifen bei
der Entwicklung des Hühnerembryo." _Zeitschrift für rationelle
Medicin._ 1869.
(152) C. F. Wolff. _Theoria generationis._ Halæ, 1759.
(153) C. F. Wolff. _Ueb. d. Bildung d. Darmcanals im bebrüteten
Hünchen._ Halle, 1812.
CHAPTER IX.
REPTILIA.
The formation of the germinal layers in the Reptilia is very
imperfectly known. The Lizard has been studied in this respect more
completely than other types, and there are a few scattered
observations on Turtles and Snakes.
The ovum has in all Reptilia a very similar structure to that in
Birds. Impregnation is effected in the upper part of the oviduct, and
the early stages of development invariably take place in the oviduct.
A few forms are viviparous, viz. some of the blindworms amongst
Lizards (Anguis, Seps), and some of the Viperidæ and Hydrophidæ
amongst the Serpents. In the majority of cases, however, the eggs are
laid in moist earth, sand, &c. Around the true ovum an egg-shell (of
the same general nature as that in birds, though usually soft), and a
variable quantity of albumen, are deposited in the oviduct. The extent
to which development has proceeded in the oviparous forms before the
eggs are laid varies greatly in different species.
The general features of the development (for a knowledge of which we
are mainly indebted to Rathke's beautiful memoirs), the structure of
the amnion and allantois, &c. are very much the same as in Birds.
The Lizards will be taken as type of the class, and a few noteworthy
points in the development of other groups will be dealt with at the
close of the Chapter. The following description, taken in the main
from my own observations, applies to Lacerta muralis.
The segmentation is meroblastic, and similar to that in Birds. At its
close the resulting blastoderm becomes divided into two layers, a
superficial epiblast formed of a single row of cells, and a layer
below this several rows deep. Below this layer fresh segments continue
for some time to be added to the blastoderm from the subjacent yolk.
[FIG. 126. SECTIONS THROUGH AN EMBRYO OF LACERTA MURALIS REPRESENTED
IN FIG. 129.
_m.g._ medullary groove; _mep._ mesoblastic plate; _ep._ epiblast;
_hy._ hypoblast; _ch´._ notochordal thickening of hypoblast; _ch._
notochord; _ne._ neurenteric canal (blastopore). In E. _ne_ points a
diverticulum of the neurenteric canal into the primitive streak.]
The blastoderm, which is thickened at its edge, spreads rapidly over
the yolk. Shortly before the yolk is half enclosed a small embryonic
shield (area pellucida) makes its appearance near the centre of the
blastoderm. The embryonic shield is mainly distinguished from the
remainder of the blastoderm by the more columnar character of its
constituent epiblast cells. It is somewhat pyriform in shape, the
narrower end corresponding with the future posterior end of the
embryo. At the hind end of the shield a somewhat triangular primitive
streak is formed, consisting of epiblast continuous below with a great
mass of rounded mesoblast cells, probably mainly formed, as in the
bird, by a proliferation of the epiblast. To this mass of cells the
hypoblast is also partially adherent. At the front end of the streak
an epiblastic involution appears, which soon becomes extended into a
passage open at both extremities, leading obliquely forwards through
the epiblast to the space below the hypoblast. The walls of the
passage are formed of a layer of columnar cells continuous both with
epiblast and hypoblast. In front of the primitive streak the body of
the embryo becomes first differentiated by the formation of a
medullary plate; and at the same time there grows out from the
primitive streak a layer of mesoblast, which spreads out in all
directions between the epiblast and hypoblast. In the region of the
embryo the mesoblast plate is stated by Kupffer and Benecke to be
continuous across the middle line, but this appears very improbable.
In a slightly later stage the medullary plate becomes marked by a
shallow groove, and the mesoblast of the embryo is then undoubtedly
constituted of two lateral plates, one on each side of the median
line. In the median line the notochord arises as a ridge-like
thickening of the hypoblast, which is continued posteriorly into the
front wall of the passage mentioned above.
The notochord does not long remain attached to the hypoblast, and the
separation between the two is already effected for the greater part of
the length of the embryo by the stage represented in fig. 129. Fig.
126 represents a series of sections through this embryo.
[FIG. 127. DIAGRAMMATIC LONGITUDINAL SECTION OF AN EMBRYO OF
LACERTA.
_pp._ body cavity; _am._ amnion; _ne._ neurenteric canal; _ch._
notochord; _hy._ hypoblast; _ep._ epiblast of the medullary plate;
_pr._ primitive streak. In the primitive streak all the layers are
partially fused.]
In a section (A) through the trunk of the embryo a short way in front
of the primitive streak, there is a medullary plate with a shallow
groove (_mg_), well-developed mesoblastic plates (_mep_), already
divided into somatic and splanchnic layers, and a completely formed
notochord independent of the hypoblast (_hy_). In the next section
(B), taken just in front of the primitive streak, the notochord is
attached to the hypoblast, and the medullary groove is deeper; while
in the section following (C), which passes through the front border of
the primitive streak, the notochord and hypoblast have become fused
with the epiblast. The section behind (D) shews the neurenteric
passage leading through the floor of the medullary groove and through
the hypoblast (_ne_). On the right side the mesoblastic plate has
become continuous with the walls of the passage. The last section (E)
passes through the front part of the primitive streak behind the
passage. The mesoblast, epiblast, and to some extent the hypoblast,
are now fused together in the axial line, and in the middle of the
fused mass is seen a narrow diverticulum (_ne_) which is probably
equivalent to the posterior diverticulum of the neural canal in Birds
(_vide_ p. 164).
The general features of the stage will best be understood by an
examination of the diagrammatic longitudinal section represented in
fig. 127. In front is shewn the amnion (_am_), growing over the head
of the embryo. The notochord (_ch_) is seen as an independent cord for
the greater part of the length of the embryo, but falls into the
hypoblast shortly in front of the neurenteric passage. The neurenteric
passage is shewn at _ne_, and behind it is the front part of the
primitive streak.
It is interesting to notice the remarkable relations of the notochord
to the walls of the neurenteric passage. More or less similar
relations are also well marked in the case of the goose and the fowl,
and support the conclusion, deducible from the lower forms of
Vertebrata, that the notochord is essentially hypoblastic.
The passage at the front end of the primitive streak forms the
posterior boundary of the medullary plate, though the medullary groove
is not at first continued back to it. The anterior wall of this
passage connects together the medullary plate and the notochordal
ridge of the hypoblast. In the stage represented in fig. 126 and 129
the medullary groove has become continued back to the opening of the
passage, which thus becomes enclosed in the medullary folds, and forms
a true neurenteric passage[71].
[71] Kupffer and Benecke (No. 154) give a very different account
from the above of the early Lacertilian development, more
especially in what concerns the so-called neurenteric passage.
They believe this structure to be closed below, and to form
therefore a blind sack open externally. The open end of this sack
they regard as the blastopore--an interpretation which accords
with my own, but they regard the sack as the rudiment of the
allantois, and hold that it is equivalent to the invaginated
archenteron of Amphioxus. I need scarcely say that I believe
Kupffer and Benecke to have made a mistake in denying the
existence of the ventral opening of this organ. Kupffer in a
subsequent paper (No. 155) states that my descriptions of the
structure of this organ do not correspond with the fact. I have
perfect confidence in leaving the decision of this point to
future observers, and may say that my observations have already
been fully confirmed by Strahl (No. 160), who has also added some
observations on the later stages to which I shall hereafter have
occasion to allude.
It will be convenient at this point to say a few words as to what is
known of the further fate of the neurenteric canal, and the early
development of the allantois. According to Strahl, who has worked on
Lacerta vivipara, the canal gradually closes from below upwards, and
is obliterated before the completion of the neural canal. The hind end
of the alimentary tract appears also to become a closed canal before
this stage.
[FIG. 128. FOUR TRANSVERSE SECTIONS THROUGH THE HINDER END OF A
YOUNG EMBRYO OF LACERTA MURALIS.
Sections A and B pass through the whole embryo, while C and D only
pass through the allantois, which at this stage projects backwards
into the section of the body cavity behind the primitive streak.
_ne._ neurenteric canal; _pr._ primitive streak; _hg._ hindgut;
_hy._ hypoblast; _pp._ body cavity; _am._ amnion; _se._ serous
envelope (outer limb of the amnion fold not yet separated from the
inner limb or true amnion); _al._ allantois; _me._ mesoblastic wall
of the allantois; _v._ vessels passing to the allantois.]
In Lacerta muralis the history appears to be somewhat different, and
it is more especially to be noticed that in this species the hindgut
does not become closed till considerably after the completion of the
neural canal. In a stage shortly after that last described, the
neurenteric passage becomes narrower. The next stage which I have
observed is considerably later. The neural canal has become completely
closed, and the flexure of the embryo has already made its appearance.
There is still a well-developed, though somewhat slit-like,
neurenteric passage, but from the analogy of birds, it is not
impossible that it may have in the meantime closed up and opened
again. It has, in any case, the same relations as in the previous
stage.
It leads from the end of the medullary canal (at the point where its
walls are continuous with the cells of the primitive streak) round the
end of the notochord, which here becomes continuous with the medullary
cord, and so through the hypoblast. The latter layer is still a flat
sheet without any lateral infolding; but it gives rise, behind the
neurenteric passage, to a blind posteriorly directed diverticulum,
placed in the body cavity behind the embryo, and opening at the
ventral face of the apparent hind end of the primitive streak. There
is very little doubt that this diverticulum is the commencing
allantois.
At a somewhat later stage the arrangement of these parts has undergone
some changes. Their relations are shewn in the sections represented in
fig. 128.
The foremost section (A) passes through the alimentary opening of the
neurenteric passage (_ne_). Above this opening the section passes
through the primitive streak (_pr_) close to its junction with the
walls of the medullary canal. The hypoblast is folded in laterally,
but the gut is still open below. The amnion is completely established.
In the next section figured (B), the fourth of my series, the gut is
completely closed in; and the mesoblast has united laterally with the
axial tissue of the primitive streak. Vessels to supply the allantois
are shewn at _v_.
The three following sections are not figured, but they present the
same features as B, except that the primitive streak gets rapidly
smaller, and the lumen of the gut narrower. The section following (C)
represents, I believe, only the stalk of the allantoic diverticulum.
This diverticulum appears to be formed as usual of hypoblast (_hy_)
enveloped by splanchnic mesoblast (_me_), and projects into the
section of the body cavity present behind the embryo. Its position in
the body cavity is the cause of its somewhat peculiar appearance in
the figure. Had the whole section been represented the allantois would
have been enclosed in a space between the serous membrane (_se_) and a
layer of splanchnic mesoblast below which has also been omitted in
fig. B[72]. It still points directly backwards, as it primitively does
in the chick, _vide_ fig. 123 A, and Gasser, No. 127, Pl. V. figs. 1
and 2. I do not understand the apparently double character of the
lumen of the allantois. In the next section (not figured) the lumen of
the allantoic stalk is larger, but still apparently double, while in
the last section (D) the lumen is considerably enlarged and single.
The neurenteric canal appears to close shortly after the stage last
described, though its further history has not been followed in detail.
[72] Owing to the difficulty of procuring material I have only
been able to prepare the two sets of sections just described, and
in the absence of a fuller series there are some points in the
interpretation of the sections which must remain doubtful.]
_General development of the Embryo._
The formation of the embryo commences with the appearance of the
medullary plate, the sides of which soon grow up to form the medullary
folds. The medullary groove is developed anteriorly before any trace
of it is visible behind. In a general way the closure of the groove
takes place as in Birds, but the anterior part of the body is very
early folded off, sinks into the yolk, and becomes covered over by the
amnion as by a hood (figs. 127 and 129). All this takes place before
the closure of the medullary canal; and the changes of this part are
quite concealed from view.
[FIG. 129. SURFACE VIEW OF A YOUNG EMBRYO OF LACERTA MURALIS.
_am._ amnion; _pr._ primitive streak.]
The closure of the medullary canal commences in the neck, and extends
forwards and backwards; and the whole region of the brain becomes
closed in, while the groove is still largely open behind.
The later stages in the development of the Lacertilian embryo do not
require a detailed description, as they present the closest analogy
with those already described for Aves. The embryo soon turns on to its
left side; and then, becoming continuously folded off from the yolk,
passes through the series of changes of form with which the reader is
already familiar. An advanced embryo is represented in fig. 130. The
early development and great length of the tail, which is spirally
coiled on the ventral surface, is a special feature to which the
attention of the reader may be called.
_Embryonic Membranes and Yolk-Sack._
The early development of the cephalic portion of the amnion has
already been alluded to. The first traces of it become apparent while
the medullary groove is still extremely shallow. The medullary plate
in the region of the head forms an axial strip of a thickish plate of
epiblast. The edge of this plate coincides with the line of the
amniotic fold, and as this fold rises up the two sides of the plate
become bent over the embryo and give rise to the inner limb of the
amnion or amnion proper. The section (fig. 127), representing the
origin of the amniotic hood of the head, shews very well how the space
between the two limbs of the amnion is continuous with the body
cavity. The amnion very early completely encloses the embryo (fig. 128
A and B), and its external limb or serous membrane, after separating
from the true amnion, soon approaches and fuses with the vitelline
membrane.
[FIG. 130. ADVANCED EMBRYO OF LACERTA MURALIS AS AN OPAQUE
OBJECT[73].
The embryo was 7 mm. in length in the curled up state.
_fb._ fore-brain; _mb._ mid-brain; _cb._ cerebellum; _au._ auditory
vesicle (closed); _ol._ olfactory pit; _md._ mandible; _hy._ hyoid
arch; _br._ branchial arches; _fl._ fore-limb; _hl._ hind-limb.]
[73] This figure was drawn for me by Professor Haddon.
The first development of the allantois as a diverticulum of the
hypoblast covered by splanchnic mesoblast, at the apparent posterior
end of the primitive streak, has been described on p. 207. The
allantois continues for some time to point directly backwards; but
gradually assumes a more ventral direction; and, as it increases in
size, extends into the space between the serous membrane and amnion,
eventually to form a large, highly vascular, flattened sack
immediately below the serous membrane.
The Yolk-Sack. The blastoderm spreads in the Lizard with very great
rapidity over the yolk to form the yolk-sack. The early appearance of
the area pellucida, or as it has been called by Kupffer and Benecke
the embryonic shield, has already been noted. Outside this a vascular
area, which has the same function as in the chick, is not long in
making its appearance. In all Reptilia the vascular channels which
arise in the vascular area, and the vessels carrying the blood to and
from the vascular area, are very similar to those in the chick. In the
Snake the sinus terminalis never attains so conspicuous a development
and in Chelonia the stage with a pair of vitelline arteries is
preceded by a stage in which the vascular area is supplied, as it
permanently is in many Mammals, by numerous transverse arterial
trunks, coming off from the dorsal aorta (Agassiz, No. 164). The
vascular area gradually envelops the whole yolk, although it does so
considerably more slowly than the general blastoderm.
Ophidia. There is, as might have been anticipated, a very close
correspondence in general development between the Lacertilia and
Ophidia. The embryos of all the Amniota are, during part of their
development, more or less spirally coiled about their long axis. This
is well marked in the chick of the third day; it is still more
pronounced in the Lizard (fig. 130); but it reaches its maximum in the
Snake. The whole Snake embryo has at the time when most coiled
(Dutrochet, Rathke) somewhat the form of a Trochus. The base of the
spiral is formed by the head, while the majority of the coils are
supplied by the tail. There are in all at this stage seven coils, and
the spiral is right-handed.
Another point, which deserves notice in the Snake, is the absence in
the embryo of all external trace of the limbs. It might have been
anticipated, on the analogy of the branchial arches, that rudiments of
the limbs would be preserved in the embryo even when limbs were absent
in the adult. Such, however, is not the case. It is however very
possible that rudiments of the branchial arches and clefts have been
preserved because these structures were functional in the larva
(Amphibia) after they ceased to have any importance in the adult; and
that the limbs have disappeared even in the embryo because in the
course of their gradual atrophy there was no advantage to the organism
in their being specially preserved at any period of life[74].
[74] It is very probable that in those Ophidia in which traces of
limbs are still preserved, that more conspicuous traces would be
found in the embryos than in the adults.
[FIG. 131. CHELONE MIDAS, FIRST STAGE.
_Au._ auditory capsule; _br. 1_ and _2_, branchial arches; _C._
carapace; _E._ eye; _f.b._ fore-brain; _f.l._ fore-limb; _H._ heart;
_h.b._ hind-brain; _h.l._ hind-limb; _hy._ hyoid; _m.b._ mid-brain;
_mn._ mandible; _mx.p._ maxillopalatine; _N._ nostril; _u._
umbilicus.]
[FIG. 132. CHELONE MIDAS, SECOND STAGE.
Letters as in fig. 131.]
Chelonia[75]. In their early development the Chelonia resemble, so far
as is known, the Lacertilia. The amnion arises early, and soon forms a
great cephalic hood. Before development has proceeded very far the
embryo turns over on to its left side. The tail in many species
attains a very considerable development (fig. 133). The chief
peculiarity in the form of the embryo (figs. 131, 132, and 133) is
caused by the development of the carapace. The first rudiment of the
carapace appears in the form of two longitudinal folds, extending
above the line of insertion of the fore- and hind-limbs, which have
already made their appearance (fig. 131). These folds are subsequently
prolonged so as to mark out the area of the carapace on the dorsal
surface. On the surface of this area there are formed the horny plates
(tortoise shell), and in the mesoblast below the bony elements of the
carapace (figs. 132 and 133).
[75] _Vide_ Agassiz (No. 164), Kupffer and Benecke (No.
154), and Parker (No. 165).
[FIG. 133. CHELONE MIDAS, THIRD STAGE.
Letters as in fig. 131. _r._ rostrum.]
Immediately after hatching the yolk-sack becomes withdrawn into the
body; while the external part of the allantois shrivels up.
BIBLIOGRAPHY.
_General._
(154) C. Kupffer and Benecke. _Die erste Entwicklung am Ei d.
Reptilien._ Königsberg, 1878.
(155) C. Kupffer. "Die Entstehung d. Allantois u. d. Gastrula d.
Wirbelthiere." _Zoologischer Anzeiger_, Vol. II. 1879, pp. 520, 593,
612.
_Lacertilia._
(156) F. M. Balfour. "On the early Development of the Lacertilia,
together with some observations, etc." _Quart. J. of Micr. Science_,
Vol. XIX. 1879.
(157) Emmert u. Hochstetter. "Untersuchung üb. d. Entwick. d.
Eidechsen in ihren Eiern." Reil's _Archiv_, Vol. X. 1811.
(158) M. Lereboullet. "Développement de la Truite, du Lézard et du
Limnée. II. Embryologie du Lézard." _An. Sci. Nat._, Ser. IV., Vol.
XXVII. 1862.
(159) W. K. Parker. "Structure and Devel. of the Skull in Lacertilia."
_Phil. Trans._, Vol. 170, p. 2. 1879.
(160) H. Strahl. "Ueb. d. Canalis myeloentericus d. Eidechse."
_Schrift. d. Gesell. z. Beför. d. gesam. Naturwiss._ Marburg. July 23,
1880.
_Ophidia._
(161) H. Dutrochet. "Recherches s. l. enveloppes du foetus." _Mém. d.
Soc. Méd. d'Emulation_, Paris, Vol. VIII. 1816.
(162) W. K. Parker. "On the skull of the common Snake." _Phil.
Trans._, Vol. 169, Part II. 1878.
(163) H. Rathke. _Entwick. d. Natter._ Königsberg, 1839.
_Chelonia._
(164) L. Agassiz. _Contributions to the Natural History of the United
States_, Vol. II. 1857. _Embryology of the Turtle._
(165) W. K. Parker. "On the development of the skull and nerves in the
green Turtle." _Proc. of the Roy. Soc._, Vol. XXVIII. 1879. _Vide_
also _Nature_, April 14, 1879, and _Challenger Reports_, Vol. I. 1880.
(166) H. Rathke. _Ueb. d. Entwicklung d. Schildkröten._ Braunschweig,
1848.
_Crocodilia._
(167) H. Rathke. _Ueber die Entwicklung d. Krokodile._ Braunschweig,
1866.
CHAPTER X.
MAMMALIA.
The classical researches of Bischoff on the embryology of several
mammalian types, as well as those of other observers, have made us
acquainted with the general form of the embryos of the Placentalia,
and have shewn that, except in the earliest stages of development,
there is a close agreement between them. More recently Hensen,
Schäfer, Kölliker, Van Beneden and Lieberkühn have shed a large amount
of light on the obscurer points of the earliest developmental periods,
especially in the rabbit. For the early stages the rabbit necessarily
serves as type; but there are grounds for thinking that not
inconsiderable variations are likely to be met with in other species,
and it is not at present easy to assign to some of the developmental
features their true value. We have no knowledge of the early
development of the Ornithodelphia or Marsupialia.
The ovum on leaving the ovary is received by the fimbriated extremity
of the Fallopian tube, down which it slowly travels. It is still
invested by the zona radiata, and in the rabbit an albuminous envelope
is formed around it in its passage downwards. Impregnation takes place
in the upper part of the Fallopian tube, and is shortly followed by
the segmentation, which is remarkable amongst the Amniota for being
complete.
Although this process (the details of which have been made known by
the brilliant researches of Ed. van Beneden) has already been shortly
dealt with as it occurs in the rabbit (Vol. II. p. 98) it will be
convenient to describe it again with somewhat greater detail.
The ovum first divides into two nearly equal spheres, of which one is
slightly larger and more transparent than the other. The larger sphere
and its products will be spoken of as the epiblastic spheres, and the
smaller one and its products as the hypoblastic spheres, in accordance
with their different destinations.
Both the spheres are soon divided into two, and each of the four so
formed into two again; and thus a stage with eight spheres ensues. At
the moment of their first separation these spheres are spherical, and
arranged in two layers, one of them formed of the four epiblastic
spheres, and the other of the four hypoblastic. This position is not
long retained, but one of the hypoblastic spheres passes to the
centre; and the whole ovum again takes a spherical form.
In the next phase of segmentation each of the four epiblastic spheres
divides into two, and the ovum thus becomes constituted of twelve
spheres, eight epiblastic and four hypoblastic. The epiblastic spheres
have now become markedly smaller than the hypoblastic.
The four hypoblastic spheres next divide, giving rise, together with
the eight epiblastic spheres, to sixteen spheres in all; which are
nearly uniform in size. Of the eight hypoblastic spheres four soon
pass to the centre, while the eight superficial epiblastic spheres
form a kind of cup partially enclosing the hypoblastic spheres. The
epiblastic spheres now divide in their turn, giving rise to sixteen
spheres which largely enclose the hypoblastic spheres. The
segmentation of both epiblastic and hypoblastic spheres continues, and
in the course of it the epiblastic spheres spread further and further
over the hypoblastic, so that at the close of segmentation the
hypoblastic spheres constitute a central solid mass almost entirely
surrounded by the epiblastic spheres. In a small circular area however
the hypoblastic spheres remain for some time exposed at the surface
(fig. 134 A).
The whole process of segmentation is completed in the rabbit about
seventy hours after impregnation. At its close the epiblast cells, as
they may now be called, are clear, and have an irregularly cubical
form; while the hypoblast cells are polygonal and granular, and
somewhat larger than the epiblast cells.
The opening in the epiblastic layer where the hypoblast cells are
exposed on the surface may for convenience be called with Van Beneden
the blastopore, though it is highly improbable that it in any way
corresponds with the blastopore of other vertebrate ova[76].
[76] It is stated by Bischoff that shortly after impregnation,
and before the commencement of the segmentation, the ova of the
rabbit and guinea-pig are covered with cilia and exhibit the
phenomenon of rotation. This has not been noticed by other
observers.
[FIG. 134. OPTICAL SECTIONS OF A RABBIT'S OVUM AT TWO STAGES CLOSELY
FOLLOWING UPON THE SEGMENTATION. (After E. van Beneden.)
_ep._ epiblast; _hy._ primary hypoblast; _bp._ Van Beneden's
blastopore. The shading of the epiblast and hypoblast is
diagrammatic.]
After its segmentation the ovum passes into the uterus. The epiblast
cells soon grow over the blastopore and thus form a complete
superficial layer. A series of changes next take place which result in
the formation of what has been called the blastodermic vesicle. To Ed.
van Beneden we owe the fullest account of these changes; to Hensen and
Kölliker however we are also indebted for valuable observations,
especially on the later stages in the development of this vesicle.
The succeeding changes commence with the appearance of a narrow cavity
between the epiblast and hypoblast, which extends so as completely to
separate these two layers except in the region adjoining the original
site of the blastopore (fig. 134 B)[77]. The cavity so formed rapidly
enlarges, and with it the ovum also; which soon takes the form of a
thin-walled vesicle with a large central cavity. This vesicle is the
blastodermic vesicle. The greater part of its walls are formed of a
single row of flattened epiblast cells; while the hypoblast cells form
a small lens-shaped mass attached to the inner side of the epiblast
cells (fig. 135).
[77] Van Beneden regards it as probable that the blastopore is
situated somewhat excentrically in relation to the area of
attachment of the hypoblastic mass to the epiblast.
In the Vespertilionidæ Van Beneden and Julin have shewn that the ovum
undergoes at the close of segmentation changes of a more or less
similar nature to those in the rabbit; the blastopore would however
appear to be wider, and to persist even after the cavity of the
blastodermic vesicle has commenced to be developed.
[FIG. 135. RABBIT'S OVUM BETWEEN 70-90 HOURS AFTER IMPREGNATION.
(After E. van Beneden.)
_bv._ cavity of blastodermic vesicle (yolk-sack); _ep._ epiblast;
_hy._ primitive hypoblast; _Zp._ mucous envelope (zona pellucida).]
Although by this stage, which occurs in the rabbit between seventy and
ninety hours after impregnation, the blastodermic vesicle has by no
means attained its greatest dimensions, it has nevertheless grown from
about 0.09 mm.--the size of the ovum at the close of segmentation--to
about 0.28. It is enclosed by a membrane formed from the zona radiata
and the mucous layer around it. The blastodermic vesicle continues to
enlarge rapidly, and during the process the hypoblastic mass undergoes
important changes. It spreads out on the inner side of the epiblast
and at the same time loses its lens-like form and becomes flattened.
The central part of it remains however thicker, and is constituted of
two rows of cells, while the peripheral part, the outer boundary of
which is irregular, is formed of an imperfect layer of amoeboid cells
which continually spread further and further within the epiblast. The
central thickening of the hypoblast forms an opaque circular spot on
the blastoderm, which constitutes the commencement of the embryonic
area.
The history of the stages immediately following, from about the
commencement of the fifth day to the seventh day, when a primitive
streak makes its appearance, is imperfectly understood, and has been
interpreted very differently by Van Beneden (No. 171) on the one hand
and by Kölliker (184), Rauber (187) and Lieberkühn (186) on the other.
I have myself in conjunction with my pupil, Mr Heape, also conducted
some investigations on these stages, which have unfortunately not as
yet led me to a completely satisfactory reconciliation of the opposing
views.
Van Beneden states that about five days after impregnation the
hypoblast cells in the embryonic area become divided into two distinct
strata, an upper stratum of small cells adjoining the epiblast and a
lower stratum of flattened cells which form the true hypoblast. At the
edge of the embryonic area the hypoblast is continuous with a
peripheral ring of the amoeboid cells of the earlier stage, which now
form, except at the edge of the ring, a continuous layer of flattened
cells in contact with the epiblast. During the sixth day the flattened
epiblast cells are believed by Van Beneden to become columnar. The
embryonic area gradually extends itself, and as it does so becomes
oval. A central lighter portion next becomes apparent, which gradually
spreads, till eventually the darker part of the embryonic area forms a
crescent at the posterior part of the now somewhat pyriform embryonic
area. The lighter part is formed of columnar epiblast and hypoblast
only, while in the darker area a layer of the mesoblast, derived from
the intermediate layer of the fifth day, is also found. In this darker
area the primitive streak originates early on the seventh day.
Kölliker, following the lines originally laid down by Rauber, has
arrived at very different results. He starts from the three-layered
condition described by Van Beneden for the fifth day, but does not
give any investigations of his own as to the origin of the middle
layer. He holds the outer layer to be a provisional layer of
protective cells, forming part of the wall of the original vesicle,
the middle layer he regards as the true epiblast and the inner layer
as the hypoblast.
During the sixth day he finds that the cells of the outer layer
gradually cease to form a continuous layer and finally disappear;
while the cells of the middle layer become columnar, and form the
columnar epiblast present in the embryonic area at the end of the
sixth day. The mesoblast first takes its origin in the region and on
the formation of the primitive streak.
The investigations of Heape and myself do not extend to the first
formation of the intermediate layer found on the fifth day. We find on
the sixth day in germinal vesicles of about 2.2-2.5 millimetres in
diameter with embryonic areas of about .8 mm. that the embryonic area
(fig. 136) is throughout composed of:
(1) A layer of flattened hypoblast cells;
(2) A somewhat irregular layer of more columnar elements, in some
places only a single row deep and in other places two or more
rows deep.
(3) Flat elements on the surface, which do not, however, form
a continuous layer, and are intimately attached to the columnar
cells below.
Our results as to the structure of the blastoderm at this stage
closely correspond therefore with those of Kölliker, but on one
important point we have arrived at a different conclusion. Kölliker
states that he has never found the flattened elements in the act of
becoming columnar. We believe that we have in many instances been able
to trace them in the act of undergoing this change, and have attempted
to shew this in our figure.
Our next oldest embryonic areas were somewhat pyriform measuring about
1.19 mm. in length and .85 in breadth. Of these we have several, some
from a rabbit in which we also met with younger still nearly circular
areas. All of them had a distinctly marked posterior opacity forming a
commencing primitive streak, though decidedly less advanced than in
the blastoderm represented in fig. 140. In the younger specimens the
epiblast in front of the primitive streak was formed of a single row
of columnar cells (fig. 138 A), no mesoblast was present and the
hypoblast formed a layer of flattened cells. In the region immediately
in front of the primitive streak, an irregular layer of mesoblast
cells was interposed between the epiblast and hypoblast. In the
anterior part of the primitive streak itself (fig. 138 B) there was a
layer of mesoblast with a considerable lateral extension, while in the
median line there was a distinct mesoblastic proliferation of epiblast
cells. In the posterior sections the lateral extension of the
mesoblast was less, but the mesoblast cells formed a thicker cord in
the axial line.
Owing to the unsatisfactory character of our data the following
attempt to fill in the history of the fifth and sixth days must be
regarded as tentative[78]. At the commencement of the fifth day the
central thickening, of what has been called above the primitive
hypoblast, becomes divided into two layers: the lower of these is
continuous with the peripheral hypoblast and is formed of flattened
cells, while the upper one is formed of small rounded elements. The
superficial epiblast again is formed of flattened cells.
[78] The attempt made below to frame a consecutive history out of
the contradictory data at my disposal is not entirely
satisfactory. Should Kölliker's view turn out to be quite
correct, the origin of the middle layer of the fifth day, which
Kölliker believes to become the permanent epiblast, will have to
be worked out again, in order to determine whether it really
comes, as it is stated by Van Beneden to do, from the primitive
hypoblast.
During the fifth day remarkable changes take place in the epiblast of
the embryonic area. It is probable that its constituent cells increase
in number and become one by one columnar; and that in the process they
press against the layer of rounded elements below them, so that the
two layers cease to be distinguishable, and the _whole_ embryonic area
acquires in section the characters represented in fig. 136[79].
Towards the end of the sixth day the embryonic area becomes oval, but
the changes which next take place are not understood. In the front
part of the area only two layers of cells are found, (1) an hypoblast,
and (2) an epiblast of columnar cells probably derived from the
flattened epiblast cells of the earlier stages. In the posterior part
of the blastoderm a middle layer is present (Van Beneden) in addition
to the two other layers; and this layer probably originates from the
middle layer which extended throughout the area at the beginning of
the fifth day, and then became fused with the epiblast. The middle
layer does not give rise to the whole of the eventual mesoblast, but
only to part of it. From its origin it may be called the hypoblastic
mesoblast, and it is probably equivalent to the hypoblastic mesoblast
already described in the chick (pp. 154 and 155). The stage just
described has only been met with by Van Beneden[80].
[79] The section figured may perhaps hardly appear to justify
this view; the examination of a larger number of sections is,
however, more favourable to it, but it must be admitted that the
interpretation is by no means thoroughly satisfactory.
[80] Kölliker does not believe in the existence of this stage,
having never met with it himself. It appears to me, however, more
probable that Kölliker has failed to obtain it, than that Van
Beneden has been guilty of such an extraordinary blunder as to
have described a stage which has no existence.
[FIG. 136. SECTION THROUGH THE NEARLY CIRCULAR EMBRYONIC AREA OF A
RABBIT'S OVUM OF SIX DAYS, NINE HOURS AND .8 MM. IN DIAMETER.
The section shews the peculiar character of the upper layer with a
certain number of superficial flattened cells; and represents about
half the breadth of the area.]
A diagrammatic view of the whole blastodermic vesicle at about the
beginning of the seventh day is given in fig. 137. The embryonic area
is represented in white. The line _ge_ in B shews the extension of the
hypoblast round the inner side of the vesicle. The blastodermic
vesicle is therefore formed of three areas, (1) the embryonic area
with three layers: this area is placed where the blastopore was
originally situated. (2) The ring around the embryonic area where the
walls of the vesicle are formed of epiblast and hypoblast. (3) The
area beyond this again where the vesicle is formed of epiblast
only[81].
[81] Schäfer describes the blastodermic vesicle of the cat as
being throughout in a bilaminar condition before the formation of
a definite primitive streak or of the mesoblast.
[FIG. 137. VIEWS OF THE BLASTODERMIC VESICLE OF A RABBIT ON THE
SEVENTH DAY WITHOUT THE ZONA. A. from above, B. from the side. (From
Kölliker.)
_ag._ embryonic area; _ge._ boundary of the hypoblast.]
The changes which next take place begin with the formation of a
primitive streak, homologous with, and in most respects similar to,
the primitive streak in Birds. The formation of the streak is preceded
by that of a clear spot near the middle of the blastoderm, forming the
nodal point of Hensen. This spot subsequently constitutes the front
end of the primitive streak.
The history of the primitive streak was first worked out in a
satisfactory manner by Hensen (No. 182), from whom however I differ in
admitting the existence of a certain part of the mesoblast before its
appearance.
Early on the seventh day the embryonic area becomes pyriform, and at
its posterior and narrower end a primitive streak makes its
appearance, which is due to a proliferation of rounded cells from the
epiblast. At the time when this proliferation commences the layer of
hypoblastic mesoblast is present, especially just in front of, and at
the sides of, the anterior part of the streak; but no mesoblast is
found in the anterior part of the embryonic area. These features are
shewn in fig. 138 A and B. The mesoblast derived from the
proliferation of the epiblast soon joins the mesoblast already
present; though in many sections it seems possible to trace a
separation between the two parts (fig. 139 B) of the mesoblast.
[FIG. 138. TWO SECTIONS THROUGH OVAL BLASTODERMS OF A RABBIT ON THE
SEVENTH DAY. THE LENGTH OF THE AREA WAS ABOUT 1.2 MM. AND ITS
BREADTH ABOUT .86 MM.
A. Through the region of the blastoderm in front of the primitive
streak; B. through the front part of the primitive streak; _ep._
epiblast; _m._ mesoblast; _hy._ hypoblast; _pr._ primitive streak.]
[FIG. 139. TWO TRANSVERSE SECTIONS THROUGH THE EMBRYONIC AREA OF AN
EMBRYO RABBIT OF SEVEN DAYS.
The embryo has nearly the structure represented in fig. 140.
A. is taken through the anterior part of the embryonic area. It
represents about half the breadth of the area, and there is no trace
of a medullary groove or of the mesoblast.
B. Is taken through the posterior part of the primitive streak.
_ep._ epiblast; _hy._ hypoblast.]
During the seventh day the primitive streak becomes a more pronounced
structure, the mesoblast in its neighbourhood increases in quantity,
while an axial groove--the primitive groove--is formed on its upper
surface. The mesoblastic layer in front of the primitive streak
becomes thicker, and, in the two-layered region in front, the epiblast
becomes several rows deep (fig. 139 A).
In the part of the embryonic area in front of the primitive streak
there arise during the eighth day two folds bounding a shallow median
groove, which meet in front, but diverge behind, and enclose between
them the foremost end of the primitive streak (fig. 141). These folds
are the medullary folds and they constitute the first definite traces
of the embryo. The medullary plate bounded by them rapidly grows in
length, the primitive streak always remaining at its hinder end. While
the lateral epiblast is formed of several rows of cells, that of the
medullary plate is at first formed of but a single row (fig. 142,
_mg_). The mesoblast, which appears to grow forward from the primitive
streak, is stated to be at first a continuous sheet between the
epiblast and hypoblast (Hensen). The evidence on this point does not
however appear to me to be quite conclusive. In any case, as soon as
ever the medullary groove is formed, the mesoblast becomes divided,
exactly as in Lacerta and Elasmobranchii, into two independent lateral
plates, which are not continuous across the middle line (fig. 142,
_me_). The hypoblast cells are flattened laterally, but become
columnar beneath the medullary plate (fig. 142).
[FIG. 140. EMBRYONIC AREA OF AN EIGHT DAYS' RABBIT. (After
Kölliker.)
_arg._ embryonic area; _pr._ primitive streak.]
In tracing the changes which take place in the relations of the
layers, in passing from the region of the embryo to that of the
primitive streak, it will be convenient to follow the account given by
Schäfer for the guinea-pig (No. 190), which on this point is far
fuller and more satisfactory than that of other observers. In doing so
I shall leave out of consideration the fact (fully dealt with later in
this chapter) that the layers in the guinea-pig are inverted. Fig. 143
represents a series of sections through this part in the guinea-pig.
The anterior section (D) passes through the medullary groove near its
hinder end. The commencement of the primitive streak is marked by a
slight prominence on the floor of the medullary groove between the two
diverging medullary folds (fig. 143 C, _ae_). Where this prominence
becomes first apparent the epiblast and hypoblast are united together.
The mesoblast plates at the two sides remain in the meantime quite
free. Slightly further back, but before the primitive groove is
reached, the epiblast and hypoblast are connected together by a cord
of cells (fig. 143 B. _f_), which in the section next following
becomes detached from the hypoblast and forms a solid keel projecting
from the epiblast. In the following section the hitherto independent
mesoblast plates become united with this keel (fig. 143 A); and in the
posterior sections, through the part of the primitive streak with the
primitive groove, the epiblast and mesoblast continue to be united in
the axial line, but the hypoblast remains distinct. These peculiar
relations may shortly be described by saying that in the axial line
the hypoblast becomes _united with the epiblast at the posterior end
of the embryo_; and that the cells which connect the hypoblast and
epiblast are posteriorly continuous with the fused epiblast and
mesoblast of the primitive streak, the hypoblast in the region of the
primitive streak having become distinct from the other layers.
[FIG. 141. EMBRYONIC AREA OF A SEVEN DAYS' EMBRYO RABBIT. (From
Kölliker.)
_o._ place of future area vasculosa; _rf._ medullary groove; _pr._
primitive streak; _ag._ embryonic area.]
[FIG. 142. TRANSVERSE SECTION THROUGH AN EMBRYO RABBIT OF EIGHT
DAYS.
_ep._ epiblast; _me._ mesoblast; _hy._ hypoblast; _mg._ medullary
groove.]
[FIG. 143. A SERIES OF TRANSVERSE SECTIONS THROUGH THE JUNCTION OF
THE PRIMITIVE STREAK AND MEDULLARY GROOVE OF A YOUNG GUINEA-PIG.
(After Schäfer.)
A. is the posterior section.
_e._ epiblast; _m._ mesoblast; _h._ hypoblast; _ae._ axial epiblast
of the primitive streak; _ah._ axial hypoblast attached in B. and C.
to the epiblast at the rudimentary blastopore; _mg._ medullary
groove; _f._ rudimentary blastopore.]
The peculiar relations just described, which hold also for the rabbit,
receive their full explanation by a comparison of the Mammal with the
Bird and the Lizard, but before entering into this comparison, it will
be well to describe the next stage in the rabbit, which is in many
respects very instructive. In this stage the thickened axial portion
of the hypoblast in the region of the embryo becomes separated from
the lateral part as the notochord. Very shortly after the formation of
the notochord, the hypoblast grows in from the two sides, and becomes
quite continuous across the middle line. The formation of the
notochord takes place from before backwards; and at the hinder end of
the embryo the notochord is continued into the mass of cells which
forms the axis of the primitive streak, becoming therefore at this
point continuous with the epiblast. The notochord in fact behaves
exactly as did the axial hypoblast in the earlier stage.
In comparison with Lacerta (pp. 203-205) it is obvious that the axial
hypoblast and the notochord derived from it have exactly the same
relations in Mammalia and Lacertilia. In both they are continued at
the hind end of the embryo into the epiblast; and close to where they
join it, the mesoblast and epiblast fuse together to form the
primitive streak. The difference between the two types consists in the
fact that in Reptilia there is formed a passage connecting the neural
and alimentary canals, the front wall of which is constituted by the
cells which form the above junction between the notochord and
epiblast; and that in Mammalia this passage--which is only a
rudimentary structure in Reptilia--has either been overlooked or else
is absent. In any case the axial junction of the epiblast and
hypoblast in Mammalia is shewn by the above comparison with Lacertilia
to represent the dorsal lip of the true vertebrate blastopore. The
presence of this blastopore seems to render it clear that the
blastopore discovered by Ed. van Beneden cannot have the meaning he
assigned to it in comparing it with the blastopore of the frog.
Kölliker adduces the fact that the notochord is continuous with the
axial cells of the primitive streak as an argument against its
hypoblastic origin. The above comparison with Lacertilia altogether
deprives this argument of any force.
At the stage we have now reached the three layers are definitely
established. The epiblast (on the view adopted above) clearly
originates from epiblastic segmentation cells. The hypoblast without
doubt originates from the hypoblastic segmentation spheres which give
rise to the lenticular mass within the epiblast on the appearance of
the cavity of the blastodermic vesicle; while, though the history of
the mesoblast is still obscure, part of it appears to originate from
the hypoblastic mass, and part is undoubtedly formed from the epiblast
of the primitive streak.
While these changes have been taking place the rudiments of a vascular
area become formed, and it is very possible that part of the
hypoblastic mesoblast passes in between the epiblast and hypoblast,
immediately around the embryonic area, to give rise to the area
vasculosa. From Hensen's observation it seems at any rate clear that
the mesoblast of the vascular area arises independently of the
primitive streak: an observation which is borne out by the analogy of
Birds.
_General growth of the Embryo._
We have seen that the blastodermic vesicle becomes divided at an early
stage of development into an embryonic area, and a non-embryonic
portion. The embryonic area gives rise to the whole of the body of the
embryo, while the non-embryonic part forms an appendage, known as the
umbilical vesicle, which becomes gradually folded off from the embryo,
and has precisely the relations of the yolk-sack of the Sauropsida. It
is almost certain that the Placentalia are descended from ancestors,
the embryos of which had large yolk-sacks, but that the yolk has
become reduced in quantity owing to the nutriment received from the
wall of the uterus taking the place of that originally supplied by the
yolk. A rudiment of the yolk-sack being retained in the umbilical
vesicle, this structure may be called indifferently umbilical vesicle
or yolk-sack.
The yolk which fills the yolk-sack in Birds is replaced in Mammals by
a coagulable fluid; while the gradual extension of the hypoblast round
the wall of the blastodermic vesicle, which has already been
described, is of the same nature as the growth of the hypoblast round
the yolk-sack in Birds.
The whole embryonic area would seem to be employed in the formation of
the body of the embryo. Its long axis has no very definite relation to
that of the blastodermic vesicle. The first external trace of the
embryo to appear is the medullary plate, bounded by the medullary
folds, and occupying at first the anterior half of the embryonic area
(fig. 141). The two medullary folds diverge behind and enclose the
front end of the primitive streak. As the embryo elongates, the
medullary folds nearly meet behind and so cut off the front portion of
the primitive streak, which then appears as a projection in the hind
end of the medullary groove. In an embryo rabbit, eight days after
impregnation, the medullary groove is about 1.80 mm. in length. At
this stage a division may be clearly seen in the lateral plates of
mesoblast into a vertebral zone adjoining the embryo and a more
peripheral lateral zone; and in the vertebral zone indications of two
somites, about 0.37 mm. from the hinder end of the embryo, become
apparent. The foremost of these somites marks the junction, or very
nearly so, of the cephalic region and trunk. The small size of the
latter as compared with the former is very striking, but is
characteristic of Vertebrates generally. The trunk gradually elongates
relatively to the head, by the addition behind of fresh somites. The
embryo has not yet begun to be folded off from the yolk-sack. In a
slightly older embryo of nine days there appears (Hensen, Kölliker)
round the embryonic area a delicate clear ring which is narrower in
front than behind (fig. 144 A, _ap_). This ring is regarded by these
authors as representing the peripheral part of the area pellucida of
Birds, which does not become converted into the body of the embryo.
Outside the area pellucida, an area vasculosa has become very well
defined. In the embryo itself (fig. 144 A) the disproportion between
head and trunk is less marked than before; the medullary plate dilates
anteriorly to form a spatula-shaped cephalic enlargement; and three or
four somites are established. In the lateral parts of the mesoblast of
the head there may be seen on each side a tube-like structure (_hz_).
Each of these is part of the heart, which arises as two independent
tubes. The remains of the primitive streak (_pr_) are still present
behind the medullary groove.
In somewhat older embryos (fig. 144 B) with about eight somites, in
which the trunk considerably exceeds the head in length, the first
distinct traces of the folding-off of the head end of the embryo
become apparent, and somewhat later a fold also appears at the hind
end. In the formation of the hind end of the embryo the primitive
streak gives rise to a tail swelling and to part of the ventral wall
of the postanal gut. In the region of the head the rudiments of the
heart (_h_) are far more definite. The medullary groove is still open
for its whole length, but in the head it exhibits a series of
well-marked dilatations. The foremost of these (_vh_) is the rudiment
of the fore-brain, from the sides of which there project the two optic
vesicles (_ab_); the next is the mid-brain (_mh_), and the last is the
hind-brain (_hh_), which is again divided into smaller lobes by
successive constrictions. The medullary groove behind the region of
the somites dilates into an embryonic sinus rhomboidalis like that of
the Bird. Traces of the amnion (_af_) are now apparent both in front
of and behind the embryo.
[FIG. 144. EMBRYO RABBITS OF ABOUT NINE DAYS FROM THE DORSAL SIDE.
(From Kölliker.)
A. magnified 22 times, and B. 21 times.
_ap._ area pellucida; _rf._ medullary groove; _h´._ medullary plate
in the region of the future fore-brain; _h´´._ medullary plate in the
region of the future mid-brain; _vh._ fore-brain; _ab._ optic
vesicle; _mh._ mid-brain; _hh._ and _h´´._ hind-brain; _uw._
mesoblastic somite; _stz._ vertebral zone; _pz._ lateral zone; _hz._
and _h._ heart; _ph._ pericardial section of body cavity; _vo._
vitelline vein; _af._ amnion fold.]
The structure of the head and the formation of the heart at this age
are illustrated in fig. 145. The widely-open medullary groove (_rf_)
is shewn in the centre. Below it the hypoblast is thickened to form
the notochord _dd´_; and at the sides are seen the two tubes, which,
on the folding-in of the foregut, give rise to the unpaired heart.
Each of these is formed of an outer muscular tube of splanchnic
mesoblast (_ahh_), not quite closed towards the hypoblast, and an
inner epithelioid layer (_ihh_); and is placed in a special section of
the body cavity (_ph_), which afterwards forms the pericardial cavity.
[FIG. 145. TRANSVERSE SECTION THROUGH THE HEAD OF A RABBIT OF THE
SAME AGE AS FIG. 144 B. (From Kölliker.)
B. is a more highly magnified representation of part of A.
_rf._ medullary groove; _mp._ medullary plate; _rw._ medullary fold;
_h._ epiblast; _dd._ hypoblast; _dd´._ notochordal thickening of
hypoblast; _sp._ undivided mesoblast; _hp._ somatic mesoblast;
_dfp._ splanchnic mesoblast; _ph._ pericardial section of body
cavity; _ahh._ muscular wall of heart; _ihh._ epithelioid layer of
heart; _mes._ lateral undivided mesoblast; _sw._ fold of hypoblast
which will form the ventral wall of the pharynx; _sr._ commencing
throat.]
Before the ninth day is completed great external changes are usually
effected. The medullary groove becomes closed for its whole length
with the exception of a small posterior portion. The closure
commences, as in Birds, in the region of the mid-brain. Anteriorly the
folding-off of the embryo proceeds so far that the head becomes quite
free, and a considerable portion of the throat, ending blindly in
front, becomes established. In the course of this folding the, at
first widely separated, halves of the heart are brought together,
coalesce on the ventral side of the throat, and so give rise to a
median undivided heart. The fold at the tail end of the embryo
progresses considerably, and during its advance the allantois is
formed in the same way as in Birds. The somites increase in number to
about twelve. The amniotic folds nearly meet above the embryo.
[FIG. 146. ADVANCED EMBRYO OF A RABBIT (ABOUT TWELVE DAYS)[82].
_mb_. mid-brain; _th._ thalamencephalon; _ce._ cerebral hemisphere;
_op._ eye; _iv.v._ fourth ventricle; _mx._ maxillary process; _md._
mandibular arch; _hy._ hyoid arch; _fl._ fore-limb; _hl._ hind-limb;
_um._ umbilical stalk.]
[82] This figure was drawn for me by my pupil, Mr Weldon.
The later stages in the development proceed in the main in the same
manner as in the Bird. The cranial flexure soon becomes very marked,
the mid-brain forming the end of the long axis of the embryo (fig.
146). The sense organs have the usual development. Under the
fore-brain appears an epiblastic involution giving rise both to the
mouth and to the pituitary body. Behind the mouth are three
well-marked pairs of visceral arches. The first of these is the
mandibular arch (fig. 146, _md_), which meets its fellow in the middle
line, and forms the posterior boundary of the mouth. It sends forward
on each side a superior maxillary process (_mx_) which partially forms
the anterior margin of the mouth. Behind the mandibular arch are
present a well-developed hyoid (_hy_) and a first branchial arch (not
shewn in fig. 146). There are four clefts, as in other Amniota, but
the fourth is not bounded behind by a definite arch. Only the first of
these clefts persists as the tympanic cavity and Eustachian tube.
At the time when the cranial flexure appears, the body also develops a
sharp flexure immediately behind the head, which is thus bent forwards
upon the posterior straight part of the body (fig. 146). The amount of
this flexure varies somewhat in different forms. It is very marked in
the dog (Bischoff). At a later period, and in some species even before
the stage figured, the tail end of the body also becomes bent (fig.
146), so that the whole dorsal side assumes a convex curvature, and
the head and tail become closely approximated. In most cases the
embryo, on the development of the tail, assumes a more or less
definite spiral curvature (fig. 146); which however never becomes
nearly so marked a feature as it commonly is in Lacertilia and
Ophidia. With the more complete development of the lower wall of the
body the ventral flexure partially disappears, but remains more or
less persistent till near the close of intra-uterine life. The limbs
are formed as simple buds in the same manner as in Birds. The buds of
the hind-limbs are directed somewhat forwards, and those of the
fore-limb backwards.
_Embryonic membranes and yolk-sack._
The early stages in the development of the embryonic membranes are
nearly the same as in Aves; but during the later stages in the
Placentalia the allantois enters into peculiar relations with the
uterine walls, and the two, together with the interposed portion of
the subzonal membrane or false amnion, give rise to a very
characteristic Mammalian organ--the placenta--into the structure of
which it will be necessary to enter at some length. The embryonic
membranes vary so considerably in the different forms that it will be
advantageous to commence with a description of their development in an
ideal case.
We may commence with a blastodermic vesicle, closely invested by the
delicate remnant of the zona radiata, at the stage in which the
medullary groove is already established. Around the embryonic area a
layer of mesoblast would have extended for a certain distance; so as
to give rise to an area vasculosa, in which however the blood-vessels
would not have become definitely established. Such a vesicle is
represented diagrammatically in fig. 147, 1. Somewhat later the embryo
begins to be folded off, first in front and then behind (fig. 147, 2).
These folds result in a constriction separating the embryo and the
yolk-sack (_ds_), or as it is known in Mammalian embryology, the
umbilical vesicle. The splitting of the mesoblast into a splanchnic
and a somatic layer has taken place, and at the front and hind end of
the embryo a fold (_ks_) of the somatic mesoblast and epiblast begins
to rise up and grow over the head and tail of the embryo. These two
folds form the commencement of the amnion. The head and tail folds of
the amnion are continued round the two sides of the embryo, till they
meet and unite into a continuous fold. This fold grows gradually
upwards, but before it has completely enveloped the embryo, the
blood-vessels of the area vasculosa become fully developed. They are
arranged in a manner not very different from that in the chick.
The following is a brief account of their arrangement in the Rabbit:--
The outer boundary of the area, which is continually
extending further and further round the umbilical vesicle,
is marked by a venous sinus terminalis (fig. 147, _st_).
The area is not, as in the chick, a nearly complete circle,
but is in front divided by a deep indentation extending
inwards to the level of the heart. In consequence of this
indentation the sinus terminalis ends in front in two
branches, which bend inwards and fall directly into the
main vitelline veins. The blood is brought from the dorsal
aortæ by a series of lateral vitelline arteries, and not by
a single pair as in the chick. These arteries break up into
a more deeply situated arterial network, from which the
blood is continued partly into the sinus terminalis, and
partly into a superficial venous network. The hinder end of
the heart is continued into two vitelline veins, each of
which divides into an anterior and a posterior branch. The
anterior branch is a limb of the sinus terminalis, and the
posterior and smaller branch is continued towards the hind
part of the sinus, near which it ends. On its way it
receives, on its outer side, numerous branches from the venous
network, which connect by their anastomoses the posterior branch
of the vitelline vein and the sinus terminalis.
[FIG. 147. FIVE DIAGRAMMATIC FIGURES ILLUSTRATING THE FORMATION OF
THE FOETAL MEMBRANES OF A MAMMAL. (From Kölliker.)
In 1, 2, 3, 4 the embryo is represented in longitudinal section.
1. Ovum with zona pellucida, blastodermic vesicle, and embryonic
area.
2. Ovum with commencing formation of umbilical vesicle and amnion.
3. Ovum with amnion about to close, and commencing allantois.
4. Ovum with villous subzonal membrane, larger allantois, and mouth
and anus.
5. Ovum in which the mesoblast of the allantois has extended round
the inner surface of the subzonal membrane and united with it to
form the chorion. The cavity of the allantois is aborted. This fig.
is a diagram of an early human ovum.
_d._ zona radiata; _d´._ processes of zona; _sh._ subzonal membrane;
_ch._ chorion; _ch.z._ chorionic villi; _am._ amnion; _ks._
head-fold of amnion; _ss._ tail-fold of amnion; _a._ epiblast of
embryo; _a´._ epiblast of non-embryonic part of the blastodermic
vesicle; _m._ embryonic mesoblast; _m´._ non-embryonic mesoblast;
_df._ area vasculosa; _st._ sinus terminalis; _dd._ embryonic
hypoblast; _i._ non-embryonic hypoblast; _kh._ cavity of
blastodermic vesicle, the greater part of which becomes the cavity
of the umbilical vesicle _ds._; _dg._ stalk of umbilical vesicle;
_al._ allantois; _e._ embryo; _r._ space between chorion and amnion
containing albuminous fluid; _vl._ ventral body wall; _hh._
pericardial cavity.]
While the above changes have been taking place the whole blastodermic
vesicle, still enclosed in the zona, has become attached to the walls
of the uterus. In the case of the typical uterus with two tubular
horns, the position of each embryo, when there are several, is marked
by a swelling in the walls of the uterus, preparatory to the changes
which take place on the formation of the placenta. In the region of
each swelling the zona around the blastodermic vesicle is closely
embraced, in a ring-like fashion, by the epithelium of the uterine
wall. The whole vesicle assumes an oval form, and it lies in the
uterus with its two ends free. The embryonic area is placed close to
the mesometric attachment of the uterus. In many cases peculiar
processes or villi grow out from the ovum (fig. 147, 4, _sz_), which
fit into the folds of the uterine epithelium. The nature of these
processes requires further elucidation, but in some instances they
appear to proceed from the zona (the Rabbit) and in other instances
from the subzonal membrane (the Dog). In any case the attachment
between the blastodermic vesicle and the uterine wall becomes so close
at the time when the body of the embryo is first formed out of the
embryonic area, that it is hardly possible to separate them without
laceration; and at this period--from the 8th to the 9th day in the
Rabbit--it requires the greatest care to remove the ovum from the
uterus without injury. It will be understood of course that the
attachment above described is at first purely superficial and not
vascular.
Shortly after the establishment of the circulation of the yolk-sack
the folds of the amnion meet and coalesce above the embryo (fig. 147,
3 and 4, _am_). After this the inner or true amnion becomes severed
from the outer or false amnion, though the two sometimes remain
connected by a narrow stalk. Between the true and false amnion is a
continuation of the body cavity. The true amnion consists of a layer
of epiblastic epithelium and generally also of somatic mesoblast,
while the false amnion consists, as a rule, of epiblast only; though
it is possible that in some cases (the Rabbit?) the mesoblast may be
continued along its inner face.
[FIG. 147*. DIAGRAM OF THE FOETAL MEMBRANES OF A MAMMAL. (From
Turner.)
Structures which either are or have been at an earlier period of
development continuous with each other are represented by the same
character of shading.
_pc._ zona with villi; _sz._ subzonal membrane; _E._ epiblast of
embryo; _am._ amnion; _AC._ amniotic cavity; _M._ mesoblast of
embryo; _H._ hypoblast of embryo; _UV._ umbilical vesicle; _al._
allantois; _ALC._ allantoic cavity.]
Before the two limbs of the amnion are completely severed, the
epiblast of the umbilical vesicle becomes separated from the mesoblast
and hypoblast of the vesicle (fig. 147, 3), and, together with the
false amnion (_sh_), with which it is continuous, forms a complete
lining for the inner face of the zona radiata. The space between this
membrane and the umbilical vesicle with the attached embryo is
obviously continuous with the body cavity (_vide_ figs. 147, 4 and
147*). To this membrane Turner has given the appropriate name of
subzonal membrane: by Von Baer it was called the serous envelope. It
soon fuses with the zona radiata, or at any rate the zona ceases to be
distinguishable.
While the above changes are taking place in the amnion, the allantois
grows out from the hind gut as a vesicle lined by hypoblast, but
covered externally by a layer of splanchnic mesoblast (fig. 147, 3 and
4, _al_)[83]. The allantois soon becomes a flat sack, projecting into
the now largely developed space between the subzonal membrane and the
amnion, on the dorsal side of the embryo (fig. 147*, _ALC_). In some
cases it extends so as to cover the whole inner surface of the
subzonal membrane; in other cases again its extension is much more
limited. Its lumen may be retained or may become nearly or wholly
aborted. A fusion takes place between the subzonal membrane and the
adjoining mesoblastic wall of the allantois, and the two together give
rise to a secondary membrane round the ovum, known as the chorion.
Since however the allantois does not always come in contact with the
whole inner surface of the subzonal membrane, the term chorion is apt
to be somewhat vague; and in the rabbit, for instance, a considerable
part of the so-called chorion is formed by a fusion of the wall of the
yolk-sack with the subzonal membrane (fig. 148). The placental region
of the chorion may in such cases be distinguished as the true chorion,
from the remaining part which will be called the false chorion.
[83] The hypoblastic element in the allantois is sometimes very
much reduced, so that the allantois may be mainly formed of a
vascular layer of mesoblast.
The mesoblast of the allantois, especially that part of it which
assists in forming the chorion, becomes highly vascular; the blood
being brought to it by two allantoic arteries continued from the
terminal bifurcation of the dorsal aorta, and returned to the body by
one, or rarely two, allantoic veins, which join the vitelline veins
from the yolk-sack. From the outer surface of the true chorion (fig.
147, 5, _d_, 148) villi grow out and fit into crypts or depressions
which have in the meantime made their appearance in the walls of the
uterus[84]. The villi of the chorion are covered by an epithelium
derived from the subzonal membrane, and are provided with a connective
tissue core containing an artery and vein and a capillary plexus
connecting them. In most cases they assume a more or less arborescent
form, and have a distribution on the surface of the chorion varying
characteristically in different species. The walls of the crypts into
which the villi are fitted also become highly vascular, and a
nutritive fluid passes from the maternal vessels of the placenta to
the foetal vessels by a process of diffusion; while there is probably
also a secretion by the epithelial lining of the walls of the crypts,
which becomes absorbed by the vessels of the foetal villi. The above
maternal and foetal structures constitute together the organ known as
the placenta. The maternal portion consists essentially of the
vascular crypts in the uterine walls, and the foetal portion of more
or less arborescent villi of the true chorion fitting into these
crypts.
[84] These crypts have no connection with the openings of glands
in the walls of the uterus. They are believed by Ercolani to be
formed to a large extent by a regeneration of the lining tissue
of the uterine walls.
While the placenta is being developed, the folding-off of the embryo
from the yolk-sack becomes more complete; and the yolk-sack remains
connected with the ileal region of the intestine by a narrow stalk,
the vitelline duct (fig. 147, 4 and 5 and fig. 147*), consisting of
the same tissues as the yolk-sack, viz. hypoblast and splanchnic
mesoblast. While the true splanchnic stalk of the yolk-sack is
becoming narrow, a somatic stalk connecting the amnion with the walls
of the embryo is also formed, and closely envelops the stalk both of
the allantois and the yolk-sack. The somatic stalk together with its
contents is known as the umbilical cord. The mesoblast of the
somatopleuric layer of the cord develops into a kind of gelatinous
tissue, which cements together the whole of the contents. The
allantoic arteries in the cord wind in a spiral manner round the
allantoic vein. The yolk-sack in many cases atrophies completely
before the close of intra-uterine life, but in other cases it is only
removed with the other embryonic membranes at birth. The
intra-embryonic portion of the allantoic stalk gives rise to two
structures, viz. to (1) the urinary bladder formed by a dilatation of
its proximal extremity, and to (2) a cord known as the urachus
connecting the bladder with the wall of the body at the umbilicus. The
urachus, in cases where the cavity of the allantois persists till
birth, remains as an open passage connecting the intra- and
extra-embryonic parts of the allantois. In other cases it gradually
closes, and becomes nearly solid before birth, though a delicate but
interrupted lumen would appear to persist in it. It eventually gives
rise to the ligamentum vesicæ medium.
At birth the foetal membranes, including the foetal portion of the
placenta, are shed; but in many forms the interlocking of the foetal
villi with the uterine crypts is so close that the uterine mucous
membrane is carried away with the foetal part of the placenta. It thus
comes about that in some placentæ the maternal and foetal parts simply
separate from each other at birth, and in others the two remain
intimately locked together, and both are shed together as the
afterbirth. These two forms of placenta are distinguished as
non-deciduate and deciduate, but it has been shewn by Ercolani and
Turner that no sharp line can be drawn between the two types;
moreover, a larger part of the uterine mucous membrane than that
forming the maternal part of the placenta is often shed in the
deciduate Mammalia, and in the non-deciduate Mammalia it is probable
that the mucous membrane (not including vascular parts) of the
maternal placenta either peels or is absorbed.
_Comparative history of the Mammalian foetal membranes._
Two groups of Mammalia--the Monotremata and the Marsupialia--are
believed not to be provided with a true placenta.
The nature of the foetal membranes in the Monotremata is not known.
Ova, presumably in an early stage of development, have been found free
in the uterus of Ornithorhyncus by Owen. The lining membrane of the
uterus was thickened and highly vascular. The females in which these
were found were killed early in October[85].
[85] The following is Owen's account of the young after birth
(_Comp. Anat. of Vertebrates_, Vol. III. p. 717):
"On the eighth of December Dr Bennet discovered in the
subterranean nest of Ornithorhyncus three living young, naked,
not quite two inches in length." On the 12th of August, 1864, "a
female Echidna hystrix was captured ... having a young one with
its head buried in a mammary or marsupial fossa. This young one
was naked, of a bright red colour, and one inch two lines in
length."
Marsupialia. Our knowledge of the foetal membranes of the Marsupialia
is almost entirely due to Owen. In Macropus major he found that birth
took place thirty-eight days after impregnation. A foetus at the
twentieth day of gestation measured eight lines from the mouth to the
root of the tail. The foetus was enveloped in a large subzonal
membrane, with folds fitting into uterine furrows, but _not adhering
to the uterus, and without villi_. The embryo was enveloped in an
amnion reflected over the stalk of the yolk-sack, which was attached
by a filamentary pedicle to near the end of the ileum. The yolk-sack
was large and vascular, and was connected with the foetal vascular
system by a vitelline artery and two veins. The yolk-sack was
partially adherent, especially at one part, to the subzonal membrane.
No allantois was observed. In a somewhat older foetus of ten lines in
length there was a small allantois supplied by two allantoic arteries
and one vein. The allantois was quite free and not attached to the
subzonal membrane. The yolk-sack was more closely attached to the
subzonal membrane than in the younger embryo[86].
[86] Owen quotes in the _Anatomy of Vertebrates_, Vol. III. p.
721, a description from Rengger of the development of Didelphis
azaræ, which would seem to imply that a vascular adhesion arises
between the uterine walls and the subzonal membrane, but the
description is too vague to be of any value in determining the
nature of the foetal membranes.
All Mammalia, other than the Monotremata and Marsupialia, have a true
allantoic placenta. The placenta presents a great variety of forms,
and it will perhaps be most convenient first to treat these varieties
in succession, and then to give a general exposition of their mutual
affinities[87].
[87] Numerous contributions to our knowledge of the various types
of placenta have been made during the last few years, amongst
which those of Turner and Ercolani may be singled out, both from
the variety of forms with which they deal, and the important
light they have thrown on the structure of the placenta.
Amongst the existing Mammals provided with a true placenta, the most
primitive type is probably retained by those forms in which the
placental part of the chorion is confined to a comparatively
restricted area on the dorsal side of the embryo; while the false
chorion is formed by the vascular yolk-sack fusing with the remainder
of the subzonal membrane. In all the existing forms with this
arrangement of foetal membranes, the placenta is deciduate. This,
however, was probably not the case in more primitive forms from which
these are descended[88]. The placenta would appear from Ercolani's
description to be simpler in the mole (Talpa) than in other species.
The Insectivora, Cheiroptera, and Rodentia are the groups with this
type of placenta; and since the rabbit, amongst the latter, has been
more fully worked out than other species, we may take it first.
[88] _Vide_ Ercolani, No. 197, and Harting, No. 201, and also Von
Baer, _Entwicklungsgeschichte_ table on p. 225, part I., where
the importance of the limited area of attachment of the allantois
as compared with the yolk-sack is distinctly recognised.
The Rabbit. In the pregnant female Rabbit several ova are generally
found in each horn of the uterus. The general condition of the
egg-membranes at the time of their full development is shewn in fig.
148.
[FIG. 148. DIAGRAMMATIC LONGITUDINAL SECTION OF A RABBIT'S OVUM AT
AN ADVANCED STAGE OF PREGNANCY. (From Kölliker after Bischoff.)
_e._ embryo; _a._ amnion; _a._ urachus; _al._ allantois with
blood-vessels; _sh._ subzonal membrane; _pl._ placental villi; _fd._
vascular layer of yolk-sack; _ed._ hypoblastic layer of yolk-sack;
_ed´._ inner portion of hypoblast, and _ed´´._ outer portion of
hypoblast lining the compressed cavity of the yolk-sack; _ds._
cavity of yolk-sack; _st._ sinus terminalis; _r._ space filled with
fluid between the amnion, the allantois and the yolk-sack.]
The embryo is surrounded by the amnion, which is comparatively small.
The yolk-sack (_ds_) is large and attached to the embryo by a long
stalk. It has the form of a flattened sack closely applied to about
two-thirds of the surface of the subzonal membrane. The outer wall of
this sack, adjoining the subzonal membrane, is formed of hypoblast
only; but the inner wall is covered by the mesoblast of the area
vasculosa, as indicated by the thick black line (_fd_). The vascular
area is bordered by the sinus terminalis (_st_). In an earlier stage
of development the yolk-sack had not the compressed form represented
in the figure. It is, however, remarkable that the vascular area never
extends over the whole yolk-sack; but the inner vascular wall of the
yolk-sack fuses with the outer, and with the subzonal membrane, and so
forms a false chorion, which receives its blood supply from the
yolk-sack. This part of the chorion does not develop vascular villi.
The allantois (_al_) is a simple vascular sack with a large cavity.
Part of its wall is applied to the subzonal membrane, and gives rise
to the true chorion, from which there project numerous vascular villi.
These fit into corresponding uterine crypts. It seems probable, from
Bischoff's and Kölliker's observations, that the subzonal membrane in
the area of the placenta becomes attached to the uterine wall, by
means of villi, even before its fusion with the allantois. In the
later periods of gestation the intermingling of the maternal and
foetal parts of the placenta becomes very close, and the placenta is
truly deciduate. The cavity of the allantois persists till birth.
Between the yolk-sack, the allantois, and the embryo, there is left a
large cavity filled with an albuminous fluid.
The Hare does not materially differ in the arrangement of its foetal
membranes from the Rabbit.
[FIG. 149. SECTION THROUGH THE PLACENTA AND ADJACENT PARTS OF A RAT
ONE INCH AND A QUARTER LONG. (From Huxley.)
_a._ uterine vein; _b_. uterine wall; _c._ cavernous portion of
uterine wall; _d._ deciduous portion of uterus with cavernous
structure; _i._ large vein passing to the foetal portion of the
placenta; _f._ false chorion supplied by vitelline vessels; _k._
vitelline vessel; _l._ allantoic vessel; _g._ boundary of true
placenta; _e_, _m_, _m_, _e_. line of junction of the deciduate and
non-deciduate parts of the uterine wall.]
In the Rat (Mus decumanus) (fig. 149) the sack of the allantois
completely atrophies before the close of foetal life[89], and there is
developed, at the junction of the maternal part of the placenta and
the unaltered mucous membrane of the uterus, a fold of the mucous
membrane which completely encapsules the whole chorion, and forms a
separate chamber for it, distinct from the general lumen of the
uterus. Folds of this nature, which are specially developed in Man and
Apes, are known as a decidua reflexa. The decidua reflexa of the Rat
is reduced to extreme tenuity, or even vanishes before the close of
gestation.
[89] This is denied by Nasse; _vide_ Kölliker, No. 183, p. 361.
Guinea-pig. The development of the Guinea-pig is dealt with elsewhere,
but, so far as its peculiarities permit a comparison with the Rabbit,
the agreement between the two types appears to be fairly close.
The blastodermic vesicle of the Guinea-pig becomes completely
enveloped in a capsule of the uterine wall (decidua reflexa) (fig.
150). The epithelium of the blastodermic vesicle in contact with the
uterine wall is not epiblastic, but corresponds with the hypoblast of
the yolk-sack of other forms, and the mesoblast of the greater part of
the inner side of this becomes richly vascular (_yk_); the vascular
area being bounded by a sinus terminalis.
[FIG. 150. DIAGRAMMATIC LONGITUDINAL SECTION OF AN OVUM OF A
GUINEA-PIG AND THE ADJACENT UTERINE WALLS AT AN ADVANCED STAGE OF
PREGNANCY. (After Bischoff.)
_yk._ yolk-sack (umbilical vesicle) formed of an external
hypoblastic layer (shaded) and an internal mesoblastic vascular
layer (black). At the end of this layer is placed the sinus
terminalis; _all._ allantois; _pl._ placenta.
The external shaded parts are the uterine walls.]
The blastodermic vesicle is so situated within its uterine capsule
that the embryo is attached to the part of it adjoining the free side
of the uterus. From the opposite side of the uterus, viz. that to
which the mesometrium is attached, there grow into the wall of the
blastodermic vesicle numerous vascular processes of the uterine wall,
which establish at this point an organic connection between the two
(_pl_). The blood-vessels of the blastodermic vesicle (yolk-sack) stop
short immediately around the area of attachment to the uterus; but at
a late period the allantois grows towards, and fuses with this area.
The blood-vessels of the allantois and of the uterus become
intertwined, and a disc-like placenta more or less similar to that in
the Rabbit becomes formed (_pl_). The cavity of the allantois, if
developed, vanishes completely.
In all the Rodentia the placenta appears to be situated on the
mesometric side of the uterus.
Insectivora. In the Mole (Talpa) and the Shrew (Sorex), the foetal
membranes are in the main similar to those in the rabbit, and a
deciduate discoidal placenta is always present. It may be situated
anywhere in the circumference of the uterine tube. The allantoic
cavity persists (Owen), but the allantois only covers the placental
area of the chorion. The yolk-sack is persistent, and fuses with the
non-allantoic part of the subzonal membrane; which is rendered
vascular by its blood-vessels. There would seem to be (Owen) a small
decidua reflexa. A similar arrangement is found in the Hedgehog
(Erinaceus Europæus) (Rolleston), in which the placenta occupies the
typical dorsal position. It is not clear from Rolleston's description
whether the yolk-sack persists till the close of foetal life, but it
seems probable that it does so. There is a considerable reflexa which
does not, however, cover the whole chorion. In the Tenrec (Centetes)
the yolk-sack and non-placental part of the chorion are described by
Rolleston as being absent, but it seems not impossible that this may
have been owing to the bad state of preservation of the specimen. The
amnion is large. In the Cheiroptera (_Vespertilio_ and _Pteropus_),
the yolk-sack is large, and coalesces with part of the chorion. The
large yolk-sack has been observed in Pteropus by Rolleston, and in
Vespertilio by Owen. The allantoic vessels supply the placenta only.
The Cheiroptera are usually uniparous.
Simiadæ and Anthropidæ. The foetal membranes of Apes and Man, though
in their origin unlike those of the Rodentia and Insectivora, are in
their ultimate form similar to them, and may be conveniently dealt
with here. The early stages in the development of these membranes in
the human embryo have not been satisfactorily observed; but it is
known that the ovum, shortly after its entrance into the uterus,
becomes attached to the uterine wall, which in the meantime has
undergone considerable preparatory changes. A fold of the uterine wall
appears to grow round the blastodermic vesicle, and to form a complete
capsule for it, but the exact mode of formation of this capsule is a
matter of inference and not of observation. During the first fortnight
of pregnancy villi grow out, according to Allen Thomson over its whole
surface, but according to Reichert in a ring-like fashion round the
edge of the somewhat flattened ovum, and attach it to the uterus. The
further history of the early stages is extremely obscure, and to a
large extent a matter of speculation: what is known with reference to
it will be found in a special section, but I shall here take up the
history at about the fourth week.
At this stage a complete chorion has become formed, and is probably
derived from a growth of the mesoblast of the allantois (unaccompanied
by the hypoblast) round the whole inner surface of the subzonal
membrane. From the whole surface of the chorion there project branched
vascular processes, covered by an epithelium. The allantois is without
a cavity, but a hypoblastic epithelium is present in the allantoic
stalk, through which it does not, however, form a continuous tube. The
blood-vessels of the chorion are derived from the usual allantoic
arteries and vein. The general condition of the embryo and of its
membranes at this period is shewn diagrammatically in fig. 147, 5.
Around the embryo is seen the amnion, already separated by a
considerable interval from the embryo. The yolk-sack is shewn at _ds_.
Relatively to the other parts it is considerably smaller than it was
at an earlier stage. The allantoic stalk is shewn at _al_. Both it and
the stalk of the yolk-sack are enveloped by the amnion (_am_). The
chorion with its vascular processes surrounds the whole embryo.
It may be noted that the condition of the chorion at this stage is
very similar to that of the normal diffused type of placenta,
described in the sequel.
While the above changes are taking place in the embryonic membranes,
the blastodermic vesicle greatly increases in size, and forms a
considerable projection from the upper wall of the uterus. Three
regions of the uterine wall, in relation to the blastodermic vesicle,
are usually distinguished; and since the superficial parts of all of
these are thrown off with the afterbirth, each of them is called a
decidua. They are represented at a somewhat later stage in fig. 151.
There is (1) the part of the wall reflected over the blastodermic
vesicle, called the decidua reflexa (_dr_); (2) the part of the wall
forming the area round which the reflexa is inserted, called the
decidua serotina (_ds_); (3) the general wall of the uterus, not
related to the embryo, called the decidua vera (_du_).
The decidua reflexa and serotina together envelop the chorion, the
processes of which fit into crypts in them. At this period both of
them are highly and nearly uniformly vascular. The general cavity of
the uterus is to a large extent obliterated by the ovum, but still
persists as a space filled with mucus, between the decidua reflexa and
the decidua vera.
[FIG. 151. DIAGRAMMATIC SECTION OF PREGNANT HUMAN UTERUS WITH
CONTAINED FOETUS. (From Huxley after Longet.)
_al._ allantoic stalk; _nb._ umbilical vesicle; _am._ amnion; _ch._
chorion; _ds._ decidua serotina; _du._ decidua vera; _dr._ decidua
reflexa; _l_ Fallopian tube; _c._ cervix uteri; _u._ uterus; z.
foetal villi of true placenta; _z´._ villi of non-placental part of
chorion.]
The changes which ensue from this period onwards are fully known. The
amnion continues to dilate (its cavity being intensely filled with
amniotic fluid) till it comes very close to the chorion (fig. 151,
_am_); from which, however, it remains separated by a layer of
gelatinous tissue. The villi of the chorion in the region covered by
the decidua reflexa, gradually cease to be vascular, and partially
atrophy, but in the region in contact with the decidua serotina
increase and become more vascular and more arborescent (fig. 151,
_z_). The former region becomes known as the chorion læve, and the
latter as the chorion frondosum. _The chorion frondosum, together with
the decidua serotina, gives rise to the placenta._
Although the vascular supply is cut off from the chorion læve, the
processes on its surface do not completely abort. It becomes, as the
time of birth approaches, more and more closely united with the
reflexa, till the union between the two is so close that their exact
boundaries cannot be made out. The umbilical vesicle (fig. 151, _nb_),
although it becomes greatly reduced in size and flattened, persists in
a recognisable form till the time of birth.
As the embryo enlarges, the space between the decidua vera and decidua
reflexa becomes reduced, and finally the two parts unite together. The
decidua vera is mainly characterised by the presence of peculiar
roundish cells in its subepithelial tissue, and by the disappearance
of a distinct lining of epithelial cells. During the whole of
pregnancy it remains highly vascular. The decidua reflexa, on the
disappearance of the vessels in the chorion læve, becomes
non-vascular. Its tissue undergoes changes in the main similar to
those of the decidua vera, and as has been already mentioned, it fuses
on the one hand with the chorion, and on the other with the decidua
vera. The membrane resulting from its fusion with the latter structure
becomes thinner and thinner as pregnancy advances, and is reduced to a
thin layer at the time of birth.
The placenta has a somewhat discoidal form, with a slightly convex
uterine surface and a concave embryonic surface. At its edge it is
continuous both with the decidua reflexa and decidua vera. Near the
centre of the embryonic surface is implanted the umbilical cord. As
has already been mentioned, the placenta is formed of the decidua
serotina and the foetal villi of the chorion frondosum. The foetal and
maternal tissues are far more closely united (fig. 152) than in the
forms described above. The villi of the chorion, which were originally
comparatively simple, become more and more complicated, and assume an
extremely arborescent form. Each of them contains a vein and an
artery, which subdivide to enter the complicated ramifications; and
are connected together by a rich anastomosis. The villi are formed
mainly of connective tissue, but are covered by an epithelial layer
generally believed to be derived from the subzonal membrane; but, as
was first stated by Goodsir, and has since been more fully shewn by
Ercolani and Turner, this epithelial layer is really a part of the
cellular decidua serotina of the uterine wall, which has become
adherent to the villi in the development of the placenta (fig. 161,
_g_). The placenta is divided into a number of lobes, usually called
cotyledons, by septa which pass towards the chorion. These septa,
which belong to the serotina, lie between the arborescent villi of the
chorion. The cotyledons themselves consist of a network of tissue
permeated by large vascular spaces, formed by the dilatation of the
maternal blood-vessels of the serotina, into which the ramifications
of the foetal villi project. In these spaces they partly float freely,
and partly are attached to delicate trabeculæ of the maternal tissue
(fig. 161, _G_). They are, of course, separated from the maternal
blood by the uterine epithelial layer before mentioned. The blood is
brought to the maternal part of the placenta by spirally coiled
arteries, which do not divide into capillaries, but open into the
large blood-spaces already spoken of. From these spaces there pass off
oblique utero-placental veins, which pierce the serotina, and form a
system of large venous sinuses in the adjoining uterine wall (fig.
152, _F_), and eventually fall into the general uterine venous system.
At birth the whole placenta, together with the fused decidua vera, and
reflexa, with which it is continuous, is shed; and the blood-vessels
thus ruptured are closed by the contraction of the uterine wall.
[FIG. 152. SECTION OF THE HUMAN UTERUS AND PLACENTA AT THE THIRTIETH
WEEK OF PREGNANCY. (From Huxley after Ecker.)
_A._ umbilical cord; _B._ chorion; _C._ foetal villi separated by
processes of the decidua serotina, _D_; _E_, _F_, _G_. walls of
uterus.]
The foetal membranes and the placenta of the Simiadæ (Turner, No. 225)
are in most respects closely similar to those in Man; but the placenta
is, in most cases, divided into two lobes, though in the Chimpanzee,
Cynocephalus, and the Apes of the New World, it appears to be single.
The types of deciduate placenta so far described, are usually
classified by anatomists as discoidal placentæ, although it must be
borne in mind that they differ very widely. In the Rodentia,
Insectivora, and Cheiroptera there is a (usually) dorsal placenta,
which is co-extensive with the area of contact between the allantois
and the subzonal membrane, while the yolk-sack adheres to a large part
of the subzonal membrane. In Apes and Man the allantois spreads over
the whole inner surface of the subzonal membrane; the placenta is on
the ventral side of the embryo, and occupies only a small part of the
surface of the allantois. The placenta of Apes and Man might be called
metadiscoidal, in order to distinguish it from the primitive discoidal
placenta of the Rodentia and Insectivora.
In the Armadilloes (Dasypus) the placenta is truly discoidal and
deciduate (Owen and Kölliker). Alf. Milne Edwards states that in
Dasypus novemcinctus the placenta is zonary, and both Kölliker and he
found four embryos in the uterus, each with its own amnion, but the
placenta of all four united together; and all four enclosed in a
common chorion. A reflexa does not appear to be present. In the Sloths
the placenta approaches the discoidal type (Turner, No. 218). It
occupies in Cholæpus Hoffmanni about four-fifths of the surface of the
chorion, and is composed of about thirty-four discoid lobes. It is
truly deciduate, and the maternal capillaries are replaced by a system
of sinuses (fig. 161). The amnion is close to the inner surface of the
chorion. A dome-shaped placenta is also found amongst the Edentata in
Myrmecophaga and Tamandua (Milne Edwards, No. 208).
Zonary Placenta. Another form of deciduate placenta is known as the
zonary. This form of placenta occupies a broad zone of the chorion,
leaving the two poles free. It is found in the Carnivora, Hyrax,
Elephas, and Orycteropus.
It is easy to understand how the zonary placenta may be derived from
the primitive arrangement of the membranes (_vide_ p. 240) by the
extension of a _discoidal_ placental area to a _zonary_ area, but it
is possible that some of the types of zonary placenta may have been
evolved from the concentration of a diffused placenta (_vide_ p. 261)
to a zonary area. The absence of the placenta at the extreme poles of
the chorion is explained by the fact of their not being covered by a
reflection of the uterine mucous membrane. In the later periods of
pregnancy the placental area becomes, however, in most forms much more
restricted than the area of contact between the uterus and chorion.
In the Dog[90], which may be taken as type, there is a large vascular
yolk-sack formed in the usual way, which does not however fuse with
the chorion. It extends at first quite to the end of the citron-shaped
ovum, and persists till birth. The allantois first grows out on the
dorsal side of the embryo, where it coalesces with the subzonal
membrane, over a small discoidal area.
[90] _Vide_ Bischoff, No. 175.
Before the fusion of the allantois with the subzonal membrane, there
grow out from the whole surface of the external covering of the ovum,
except the poles, numerous non-vascular villi, which fit into uterine
crypts. When the allantois adheres to the subzonal membrane vascular
processes grow out from it into these villi. The vascular villi so
formed are of course at first confined to the disc-shaped area of
adhesion between the allantois and the subzonal membrane; _and there
is thus formed a rudimentary discoidal placenta_, closely resembling
that of the Rodentia. The view previously stated, that the zonary
placenta is derived from the discoidal one, receives from this fact a
strong support.
The cavity of the allantois is large, and its inner part is in contact
with the amnion. The area of adhesion between the outer part of the
allantois and subzonal membrane gradually spreads over the whole
interior of the subzonal membrane, and vascular villi are formed over
the whole area of adhesion except at the two extreme poles of the egg.
The last part to be covered is the ventral side where the yolk-sack
adjoins the subzonal membrane.
During the extension of the allantois its cavity persists, and its
inner part covers not only the amnion, but also the yolk-sack. It
adheres to the amnion and supplies it with blood-vessels (Bischoff).
With the full growth of the allantois there is formed a broad
placental zone, with numerous branched villi, fitting into
corresponding pits which become developed in the uterine walls. The
maternal and foetal structures become closely interlocked and highly
vascular; and at birth a large part of the maternal part is carried
away with the placenta; some of it however still remains attached to
the muscular wall of the uterus. The villi of the chorion do not fit
into uterine glands. The zone of the placenta diminishes greatly in
proportion to the chorion as the latter elongates, and at the full
time the breadth of the zone is not more than about one-fifth of the
whole length of the chorion.
At the edge of the placental zone there is a very small portion of the
uterine mucous membrane reflected over the non-placental part of the
chorion, which forms a small reflexa analogous with the reflexa in
Man.
The Carnivora generally closely resemble the Dog, but in the Cat the
whole of the maternal part of the placenta is carried away with the
foetal parts, so that the placenta is more completely deciduate than
in the Dog. In the Grey Seal (_Halichoerus gryphus_, Turner, No. 219)
the general arrangement of the foetal membranes is the same as in the
other groups of the Carnivora, but there is a considerable reflexa
developed at the edge of the placenta. The foetal part of the placenta
is divided by a series of primary fissures which give off secondary
and tertiary fissures. Into the fissures there pass vascular laminæ of
the uterine wall. The general surface of the foetal part of the
placenta between the fissures is covered by a greyish membrane formed
of the coalesced terminations of the foetal villi.
The structure of the placenta in Hyrax is stated by Turner (No. 221)
to be very similar to that in the Felidæ. The allantoic sack is large,
and covers the whole surface of the subzonal membrane. The amnion is
also large, but the yolk-sack would seem to disappear at an early
stage, instead of persisting, as in the Carnivora, till the close of
foetal life.
The Elephant (Owen, Turner, Chapman) is provided with a zonary
deciduate placenta, though a villous patch is present near each pole
of the chorion.
Turner (No. 220) has shewn that in Orycteropus there is present a
zonary placenta, which differs however in several particulars from the
normal zonary placenta of the Carnivora; and it is even doubtful
whether it is truly deciduate. There is a single embryo, which fills
up the body of the uterus and also projects into only one of the
horns. The placenta forms a broad median zone, leaving the two poles
free. The breadth of the zone is considerably greater than is usual in
Carnivora, one-half or more of the whole longitudinal diameter of the
chorion being occupied by the placenta. The chorionic villi are
arborescent, and diffusely scattered, and though the maternal and
foetal parts are closely interwoven, it has not been ascertained
whether the adhesion between them is sufficient to cause the maternal
subepithelial tissue to be carried away with the foetal part of the
placenta at birth. The allantois is adherent to the whole chorion, the
non-placental parts of which are vascular. In the umbilical cord a
remnant of the allantoic vesicle was present in the embryos observed
by Turner, but in the absence of a large allantoic cavity the Cape
Ant-eater differs greatly from the Carnivora. The amnion and allantois
were in contact, but no yolk sack was observed.
Non-deciduate placenta. The remaining Mammalia are characterized by a
non-deciduate placenta; or at least by a placenta in which only parts
of the maternal epithelium and no vascular maternal structures are
carried away at parturition. The non-deciduate placentæ are divided
into two groups: (1) The polycotyledonary placenta, characteristic of
the true Ruminantia (Cervidæ, Antilopidæ, Bovidæ, Camelopardalidæ);
(2) the diffused placenta found in the other non-deciduate Mammalia,
viz. the Perissodactyla, the Suidæ, the Hippopotamidæ, the Tylopoda,
the Tragulidæ, the Sirenia, the Cetacea, Manis amongst the Edentata,
and the Lemuridæ. The polycotyledonary form is the most
differentiated; and is probably a modification of the diffused form.
The diffused non-deciduate placenta is very easily derived from the
primitive type (p. 240) by an extension of the allantoic portion of
the chorion; and the exclusion of the yolk-sack from any participation
in forming the chorion.
The possession in common of a diffused type of placenta is by no means
to be regarded as a necessary proof of affinity between two groups,
and there are often, even amongst animals possessing a diffused form
of placenta, considerable differences in the general arrangement of
the embryonic membranes.
Ungulata. Although the Ungulata include forms with both cotyledonary
and diffused placentæ, the general arrangement of the embryonic
membranes is so similar throughout the group, that it will be
convenient to commence with a description of them, which will fairly
apply both to the Ruminantia and to the other forms.
The blastodermic vesicle during the early stages of development lies
freely in the uterus; and no non-vascular villi, similar to those of
the Dog or the Rabbit, are formed before the appearance of the
allantois. The blastodermic vesicle has at first the usual spherical
form, but it grows out at an early period, and with prodigious
rapidity, into two immensely long horns; which in cases where there is
only one embryo are eventually prolonged for the whole length of the
two horns of the uterus. The embryonic area is formed in the usual
way, and its long axis is placed at right angles to that of the
vesicle. On the formation of an amnion there is formed the usual
subzonal membrane, which soon becomes separated by a considerable
space from the yolk-sack (fig. 153). The yolk-sack is, however,
continued into two elongated processes (_yk_), which pass to the two
extremities of the subzonal membrane. It is supplied with the normal
blood-vessels. As soon as the allantois appears (fig. 153 _all_), it
grows out into a right and a left process, which rapidly fill the
whole free space within the subzonal membrane and in many cases,
_e.g._ the Pig (Von Baer), break through the ends of the membrane,
from which they project as the diverticula allantoidis. The cavity of
the allantois remains large, but the lining of hypoblast becomes
separated from the mesoblast, owing to the more rapid growth of the
latter. The mesoblast of the allantois applies itself externally to
the subzonal membrane to form the chorion[91], and internally to the
amnion, the cavity of which remains very small. The chorionic portion
of the allantoic mesoblast is very vascular, and that applied to the
amnion also becomes vascular in the later developmental periods.
[91] According to Bischoff the subzonal membrane atrophies,
leaving the allantoic mesoblast to constitute the whole chorion.
[FIG. 153. EMBRYO AND FOETAL MEMBRANES OF A YOUNG EMBRYO ROE-DEER.
(After Bischoff.)
_yk._ yolk-sack; _all._ allantois just sprouting as a bilobed sack.]
The horns of the yolk-sack gradually atrophy, and the whole yolk-sack
disappears some time before birth.
Where two or more embryos are present in the uterus, the chorions of
the several embryos may unite where they are in contact.
From the chorion there grow out numerous vascular villi, which fit
into corresponding pits in the uterine walls. According to the
distribution of these villi, the allantois is either diffused or
polycotyledonary.
[FIG. 154. PORTION OF THE INJECTED CHORION OF A PIG, SLIGHTLY
MAGNIFIED. (From Turner.)
The figure shews a minute circular spot (_b_) (enclosed by a
vascular ring) from which villous ridges (_r_) radiate.]
[FIG. 155. SURFACE-VIEW OF THE INJECTED UTERINE MUCOSA OF A GRAVID
PIG. (From Turner.)
The fig. shews a circular non-vascular spot where a gland opens
(_g_) surrounded by numerous vascular crypts (_cr_).]
The pig presents the simplest type of diffused placenta. The villi of
the surface of the chorion cover a broad zone, leaving only the two
poles free; their arrangement differs therefore from that in a zonary
placenta in the greater breadth of the zone covered by them. The villi
have the form of simple papillæ, arranged on a series of ridges, which
are highly vascular as compared with the intervening valleys. If an
injected chorion is examined (fig. 154), certain clear non-vascular
spots are to be seen (_b_), from which the ridges of villi radiate.
The surface of the uterus adapts itself exactly to the elevations of
the chorion; and the furrows which receive the chorionic ridges are
highly vascular (fig. 155). On the other hand, there are non-vascular
circular depressions corresponding to the non-vascular areas on the
chorion; and in these areas, and in these alone, the glands of the
uterus open (fig. 155 _g_) (Turner). The maternal and foetal parts of
the placenta in the pig separate with very great ease.
[FIG. 156. VERTICAL SECTION THROUGH THE INJECTED PLACENTA OF A MARE.
(From Turner.)
_ch._ chorion with its villi partly _in situ_ and partly drawn out
of the crypts (_cr_); _E._ loose epithelial cells which formed the
lining of the crypt; _g._ uterine glands; _v._ blood-vessels.]
In the mare (Turner), the foetal villi are arranged in a less definite
zonary band than in the pig, though still absent for a very small area
at both poles of the chorion, and also opposite the os uteri. The
filiform villi, though to the naked eye uniformly scattered, are, when
magnified, found to be clustered together in minute cotyledons, which
fit into corresponding uterine crypts (fig. 156). Surrounding the
uterine crypts are reticulate ridges on which are placed the openings
of the uterine glands. The remaining Ungulata with diffused placentæ
do not differ in any important particulars from those already
described.
The polycotyledonary form of placenta is found in the Ruminantia
alone. Its essential character consists in the foetal villi not being
uniformly distributed, but collected into patches or cotyledons which
form as it were so many small placentæ (fig. 157). The foetal villi of
these patches fit into corresponding pits in thickened patches of the
wall of the uterus (figs. 158 and 159). In many cases (Turner), the
interlocking of the maternal and foetal structures is so close that
large parts of the maternal epithelium are carried away when the
foetal villi are separated from the uterus. The glands of the uterus
open in the intervals between the cotyledons. The character of the
cotyledons differs greatly in different types. The maternal parts are
cup-shaped in the sheep, and mushroom-shaped in the cow. There are
from 60-100 in the cow and sheep, but only about five or six in the
Roe-deer. In the Giraffe there are, in addition to larger and smaller
cotyledons, rows and clusters of short villi, so that the placenta is
more or less intermediate between the polycotyledonary and diffused
types (Turner). A similarly intermediate type of placenta is found in
Cervus mexicanus (Turner).
[FIG. 157. UTERUS OF A COW IN THE MIDDLE OF PREGNANCY LAID OPEN.
(From Huxley after Colin.)
_V._ vagina; _U._ uterus; _Ch._ chorion; _C^1._ uterine cotyledons;
_C^2._ foetal cotyledons.]
[FIG. 158. COTYLEDON OF A COW, THE FOETAL AND MATERNAL PARTS HALF
SEPARATED. (From Huxley after Colin.)
_u._ uterus; _Ch._ chorion; _C^1._ maternal part of cotyledon;
_C^2._ foetal part.]
[FIG. 159. SEMI-DIAGRAMMATIC VERTICAL SECTION THROUGH A PORTION OF A
MATERNAL COTYLEDON OF A SHEEP. (From Turner.)
_cr._ crypts; _e._ epithelial lining of crypts; _v._ veins and _c._
curling arteries of subepithelial connective tissue.]
The groups not belonging to the Ungulata which are characterized by
the possession of a diffused placenta are the Sirenia, the Cetacea,
Manis, and the Lemuridæ.
Sirenia. Of the Sirenia, the placentation of the Dugong is known from
some observations of Harting (No. 201).
It is provided with a diffuse and non-deciduate placenta; with the
villi generally scattered except at the poles. The umbilical vesicle
vanishes early.
Cetacea. In the Cetacea, if we may generalize from Turner's
observations on Orca Gladiator and the Narwhal, and those of Anderson
(No. 191) on Platanista and Orcella, the blastodermic vesicle is very
much elongated, and prolonged unsymmetrically into two horns. The
mesoblast (fig. 160) of the allantois would appear to grow round the
whole inner surface of the subzonal membrane, but the cavity of the
allantois only persists as a widish sack on the ventral aspect of the
embryo (_al_). The amnion (_am_) is enormous, and is dorsally in
apposition with, and apparently coalesces with the chorion, and
ventrally covers the inner wall of the persistent allantoic sack. The
chorion, except for a small area at the two poles and opposite the os
uteri, is nearly uniformly covered with villi, which are more numerous
than in fig. 160. In the large size of the amnion, and small
dimensions of the persistent allantoic sack, the Cetacea differ
considerably from the Ungulata.
[FIG. 160. DIAGRAM OF THE FOETAL MEMBRANES IN ORCA GLADIATOR. (From
Turner.)
_ch._ chorion; _am._ amnion; _al._ allantois; _E._ embryo.]
Manis. Manis amongst the Edentata presents a type of diffused
placenta[92]. The villi are arranged in ridges which radiate from a
non-villous longitudinal strip on the concave surface of the chorion.
[92] The observations on this head were made by Sharpey, and are
quoted by Huxley (No. 202) and with additional observations by
Turner in his Memoir on the placentation of the Sloths. Anderson
(No. 191) has also recently confirmed Sharpey's account of the
diffused character of the placenta of Manis.
Manis presents us with the third type of placenta found amongst the
Edentata. On this subject, I may quote the following sentence from
Turner (_Journal of Anat. and Phys._, vol. X., p. 706).
"The Armadilloes (Dasypus), according to Professor Owen, possess a
single, thin, oblong, disc-shaped placenta; a specimen, probably
Dasypus gymnurus, recently described by Kölliker[93], had a
transversely oval placenta, which occupied the upper 2/3rds of the
uterus. In Manis, as Dr Sharpey has shewn, the placenta is diffused
over the surfaces of the chorion and uterine mucosa. In Myrmecophaga
and Tamandua, as MM. Milne Edwards have pointed out, the placenta is
set on the chorion in a dome-like manner. In the Sloths, as I have
elsewhere described, the placenta is dome-like in its general form,
and consists of a number of aggregated, discoid lobes. In Orycteropus,
as I have now shewn, the placenta is broadly zonular."
[93] _Entwicklungsgeschichte des Menschen_, _etc._, 2nd ed., p.
362. Leipzig, 1876.
Lemuridæ. The Lemurs in spite of their affinities with the Primates
and Insectivora have, as has been shewn by Milne Edwards and Turner,
an apparently very different form of placenta. There is only one
embryo, which occupies the body and one of the cornua of the uterus.
The yolk-sack disappears early, and the allantois (Turner) bulges out
into a right and left lobe, which meet above the back of the embryo.
The cavity of the allantois persists, and the mesoblast of the outer
wall fuses with the subzonal membrane (the hypoblastic epithelium
remaining distinct) to give rise to the chorion.
On the surface of the chorion are numerous vascular villi, which fit
into uterine crypts. They are generally distributed, though absent at
the two ends of the chorion and opposite the os uteri. Their
distribution accords with Turner's diffused type. Patches bare of
villi correspond with smooth areas on the surface of the uterine
mucosa in which numerous utricular glands open. There is no reflexa.
Although the Lemurian type of placenta undoubtedly differs from that
of the Primates, it must be borne in mind that the placenta of the
Primates may easily be conceived to be derived from a Lemurian form of
placenta. It will be remembered that in Man, before the true placenta
becomes developed, there is a condition with simple vascular villi
scattered over the chorion. It seems very probable that this is a
repetition of the condition of the placenta of the ancestors of the
Primates which has probably been more or less retained by the Lemurs.
It was mentioned above that the resemblance between the metadiscoidal
placenta of Man and that of the Cheiroptera, Insectivora and Rodentia
is rather physiological than morphological.
_Comparative histology of the Placenta._
It does not fall within the province of this work to treat from a
histological standpoint the changes which take place in the uterine
walls during pregnancy. It will, however, be convenient to place
before the reader a short statement of the relations between the
maternal and foetal tissues in the different varieties of placenta.
This subject has been admirably dealt with by Turner (No. 222), from
whose paper fig. 161 illustrating this subject is taken.
The simplest known condition of the placenta is that found in the pig
(B). The papilla-like foetal villi fit into the maternal crypts. The
villi (_v_) are formed of a connective tissue cone with capillaries,
and are covered by a layer of very flat epithelium (_e_) derived from
the subzonal membrane. The maternal crypts are lined by the uterine
epithelium (_e´_), immediately below which is a capillary flexus. The
maternal and foetal vessels are here separated by a double epithelial
layer. The same general arrangement holds good in the diffused
placentæ of other forms, and in the polycotyledonary placenta of the
Ruminantia, but the foetal villi (C) in the latter acquire an
arborescent form. The maternal vessels retain the form of capillaries.
In the deciduate placenta a considerably more complicated arrangement
is usually found. In the typical zonary placenta of the fox and cat (D
and E), the maternal tissue is broken up into a complete trabecular
mesh-work, and in the interior of the trabeculæ there run dilated
maternal capillaries (_d´_). The trabeculæ are covered by a more or
less columnar uterine epithelium (_e´_), and are in contact on every
side with foetal villi. The capillaries of the foetal villi preserve
their normal size, and the villi are covered by a flat epithelial
layer (_e_).
In the sloth (F) the maternal capillaries become still more dilated,
and the epithelium covering them is formed of very flat polygonal
cells.
[FIG. 161. DIAGRAMMATIC REPRESENTATIONS OF THE MINUTE STRUCTURE OF
THE PLACENTA. (From Turner.)
_F._ the foetal; _M._ the maternal placenta; _e._ epithelium of
chorion; _e´._ epithelium of maternal placenta; _d._ foetal
blood-vessels; _d´._ maternal blood-vessels; _v._ villus.
A. Placenta in its most generalized form.
B. Structure of placenta of a Pig.
C. Structure of placenta of a Cow.
D. Structure of placenta of a Fox.
E. Structure of placenta of a Cat.
F. Structure of placenta of a Sloth. On the right side of the figure
the flat maternal epithelial cells are shewn _in situ_. On the
left side they are removed, and the dilated maternal vessel with
its blood-corpuscles is exposed.
G. Structure of Human placenta. In addition to the letters already
referred to _ds_, _ds_. represents the decidua serotina of the
placenta; _t_, _t_. trabeculæ of serotina passing to the foetal
villi; _ca._ curling artery; _up._ utero-placental vein; _x._ a
prolongation of maternal tissue on the exterior of th villus
outside the cellular layer _e´_, which may represent either the
endothelium of the maternal blood-vessel or delicate connective
tissue belonging to the serotina, or both. The layer _e´_
represents maternal cells derived from the serotina. The layer of
foetal epithelium cannot be seen on the villi of the fully-formed
human placenta.]
In the human placenta (G), as in that of Apes, the greatest
modification is found in that the maternal vessels have completely
lost their capillary form, and have become expanded into large freely
communicating sinuses (_d´_). In these sinuses the foetal villi hang
for the most part freely, though occasionally attached to their walls
(_t_). In the late stages of foetal life there is only one epithelial
layer (_e´_) between the maternal and foetal vessels, which closely
invests the foetal villi, but, as shewn by Turner and Ercolani, is
part of the uterine tissue. In the foetal villi the vessels retain
their capillary form.
_Evolution of the Placenta._
From Owen's observations on the Marsupials it is clear that the
yolk-sack in this group plays an important, if not the most important
part, in absorbing the maternal nutriment destined for the foetus. The
fact that in Marsupials both the yolk-sack and the allantois are
functional in rendering the chorion vascular makes it _à priori_
probable that this was also the case in the primitive types of the
Placentalia, and this deduction is supported by the fact that in the
Rodentia, Insectivora and Cheiroptera this peculiarity of the foetal
membranes is actually found. In the primitive Placentalia there was
probably present a _discoidal_ allantoic region of the chorion, from
which simple foetal villi, like those of the pig (fig. 161 B),
projected into uterine crypts; but it is not certain how far the
umbilical part of the chorion, which was no doubt vascular, may also
have been villous. From such a primitive type of foetal membranes
divergences in various directions have given rise to the types of
foetal membranes now existing.
In a general way it may be laid down that variations in any direction
which tended to increase the absorbing capacities of the chorion would
be advantageous. There are two obvious ways in which this might be
done, viz. (1) by increasing the complexity of the foetal villi and
maternal crypts over a limited area, (2) by increasing the area of the
part of the chorion covered by placental villi. Various combinations
of the two processes would also of course be advantageous.
The most fundamental change which has taken place in all the existing
Placentalia is the exclusion of the umbilical vesicle from any
important function in the nutrition of the foetus.
The arrangement of the foetal parts in the Rodentia, Insectivora and
Cheiroptera may be directly derived from the primitive form by
supposing the villi of the discoidal placental area to have become
more complex, so as to form a _deciduate_ discoidal placenta; while
the yolk-sack still plays a part, though physiologically an
unimportant part, in rendering the chorion vascular.
In the Carnivora again we have to start from the discoidal placenta,
as shewn by the fact that the allantoic region of the placenta is at
first discoidal (p. 248). A zonary _deciduate_ placenta indicates an
increase both in area and in complexity. The relative diminution of
the breadth of the placental zone in late foetal life in the zonary
placenta of the Carnivora is probably due to its being on the whole
advantageous to secure the nutrition of the foetus by insuring a more
intimate relation between the foetal and maternal parts, than by
increasing their area of contact. The reason of this is not obvious,
but as mentioned below, there are other cases where it can be shewn
that a diminution in the area of the placenta has taken place,
accompanied by an increase in the complexity of its villi.
The second type of differentiation from the primitive form of
discoidal placenta is illustrated by the Lemuridæ, the Suidæ, and
Manis. In all these cases the area of the placental villi appears to
have increased so as to cover nearly the whole subzonal membrane,
without the villi increasing to any great extent in complexity. From
the diffused placenta covering the whole surface of the chorion,
differentiations appear to have taken place in various directions. The
_metadiscoidal_ placenta of Man and Apes, from its mode of ontogeny
(p. 248), is clearly derived from a diffused placenta--very probably
similar to that of Lemurs--by a concentration of the foetal villi,
which are originally spread over the whole chorion, to a disc-shaped
area, and by an increase in their arborescence.
The polycotyledonary forms of placenta are due to similar
concentrations of the foetal villi of an originally diffused placenta.
In the Edentata we have a group with very varying types of placenta.
Very probably these may all be differentiations within the group
itself from a diffused placenta, such as that found in Manis. The
zonary placenta of Orycteropus is capable of being easily derived from
that of Manis, by the disappearance of the foetal villi at the two
poles of the ovum. The small size of the umbilical vesicle in
Orycteropus indicates that its discoidal placenta is not, like that in
Carnivora, directly derived from a type with both allantoic and
umbilical vascularization of the chorion. The discoidal and
dome-shaped placentæ of the Armadilloes, Myrmecophaga, and the Sloths
may easily have been formed from a diffused placenta, just as the
discoidal placenta of the Simiadæ and Anthropidæ appears to have been
formed from a diffused placenta like that of the Lemuridæ.
The presence of zonary placentæ in Hyrax and Elephas does not
necessarily afford any proof of affinity of these types with the
Carnivora. A zonary placenta may quite easily be derived from a
diffused placenta; and the presence of two villous patches at the
poles of the chorion in Elephas indicates that this was very probably
the case with the placenta of this form.
Although it is clear from the above considerations that the placenta
is capable of being used to some extent in classification, yet at the
same time the striking resemblances which can exist between such
essentially different forms of placenta, as for instance those of Man
and the Rodentia, are likely to prevent it being employed, except in
conjunction with other characters.
_Special types of development._
The Guinea-pig, Cavia cobaya. Many years ago Bischoff (No. 176) shewed
that the development of the guinea-pig was strikingly different from
that of other Mammalia. His statements, which were at first received
with some doubt, have been in the main fully confirmed by Hensen (No.
182) and Schäfer (No. 190), but we are still as far as ever from
explaining the mystery of the phenomenon.
The ovum, enclosed by the zona radiata, passes into the Fallopian tube
and undergoes a segmentation which has not been studied with great
detail. On the close of segmentation, about six days after
impregnation, it assumes (Hensen) a vesicular form not unlike that of
other Mammalia. To the inner side of one wall of this vesicle is
attached a mass of granular cells similar to the hypoblastic mass in
the blastodermic vesicle of the rabbit. The egg still lies freely in
the uterus, and is invested by its zona radiata. The changes which
next take place are in spite of Bischoff's, Reichert's (No. 188) and
Hensen's observations still involved in great obscurity. It is
certain, however, that during the course of the seventh day a
ring-like thickening of the uterine mucous membrane, on the free side
of the uterus, gives rise to a kind of diverticulum of the uterine
cavity, in which the ovum becomes lodged. Opposite the diverticulum
the mucous membrane of the mesometric side of the uterus also becomes
thickened, and this thickening very soon (shortly after the seventh
day) unites with the wall of the diverticulum, and completely shuts
off the ovum in a closed capsule.
The history of the ovum during the earlier period of its inclusion in
the diverticulum of the uterine wall is not satisfactorily elucidated.
There appears in the diverticulum during the eighth and succeeding
days a cylindrical body, one end of which is attached to the uterine
walls at the mouth of the diverticulum. The opposite end of the
cylinder is free, and contains a solid body.
With reference to the nature of this cylinder two views have been put
forward. Reichert and Hensen regard it as an outgrowth of the uterine
wall, while the body within its free apex is regarded as the ovum.
Bischoff and Schäfer maintain that the cylinder itself is the ovum
attached to the uterine wall. The observations of the latter authors,
and especially those of Schäfer, appear to me to speak for the
correctness of their view[94].
[94] Schäfer's and Hensen's statements are in more or less direct
contradiction as to the structure of the ovum after the formation
of the embryo; and it is not possible to decide between the two
views about the ovum till these points of difference have been
cleared up.
The cylinder gradually elongates up to the twelfth day. Before this
period it becomes attached by its base to the mesometric thickening of
the uterus, and enters into vascular connection with it. During its
elongation it becomes hollow, and is filled with a fluid not
coagulable in alcohol, while the body within its apex remains
unaltered till the tenth day.
[FIG. 162. DIAGRAMMATIC LONGITUDINAL SECTION THROUGH THE EMBRYO OF A
GUINEA-PIG WITH ITS MEMBRANES. (After Schäfer.)
_e._ epiblast; _h._ hypoblast; _m´._ amniotic mesoblast; _m´´._
splanchnic mesoblast; _am._ amnion; _ev._ cavity of amnion; _all._
allantois; _f._ rudimentary blastopore; _mc._ cavity of vesicle
continuous with body cavity; _mm._ mucous membrane of uterus;
_m´m´._ parts where vascular uterine tissue perforates hypoblast of
blastodermic vesicle; _vt._ uterine vascular tissue; _l._ limits of
uterine tissue.]
On this day a cavity develops in the interior of this body which at
the same time enlarges itself. The greater part of its wall next
attaches itself to the free end of the cylinder, and becomes
considerably thickened. The remainder of the wall adjoining the cavity
of the cylinder becomes a comparatively thin membrane. At the free end
of the cylinder there appears on the thirteenth day an embryonic area
similar to that of other Mammalia. It is at first round but soon
becomes pyriform, and in it there appear a primitive streak and
groove; and on their appearance it becomes obvious _that the outer
layer of the cylinder is the hypoblast[95], instead of, as in all
other Mammalia, the epiblast; and that the epiblast is formed by the
wall of the inner vesicle, i.e. the original solid body placed at the
end of the cylinder_. Thus the dorsal surface of the embryo is turned
inwards, and the ventral surface outwards, and the ordinary position
of the layers is completely inverted.
[95] According to Hensen the hypoblast grows round the inside of
the wall of the cylinder from the body which he regards as the
ovum. The original wall of the cylinder persists as a very thin
layer separated from the hypoblast by a membrane.
The previously cylindrical egg next assumes a spherical form, and the
mesoblast arises in connection with the primitive streak in the manner
already described. A splanchnic layer of mesoblast attaches itself to
the inner side of the outer hypoblastic wall of the egg, a somatic
layer to the epiblast of the inner vesicle, and a mass of mesoblast
grows out into the cavity of the larger vesicle forming the
commencement of the allantois. The general structure of the ovum at
this stage is represented on fig. 162, copied from Schäfer; and the
condition of the whole ovum will best be understood by a description
of this figure.
It is seen to consist of two vesicles, (1) an outer larger one
(_h_)--the original egg-cylinder--united to the mesometric wall of the
uterus by a vascular connection at _m´m´_, and (2) an inner smaller
one (_ev_)--the originally solid body at the free end of the
egg-cylinder. The outer vesicle is formed of (1) an external lining of
columnar hypoblast (_h_) which is either pierced or invaginated at the
area of vascular connection with the uterus, and (2) of an inner layer
of splanchnic mesoblast (_m´´_) which covers without a break the
vascular uterine growth. At the upper pole of the ovum is placed the
smaller epiblastic vesicle, and where the two vesicles come together
is situated the embryonic area with the primitive streak (_f_), and
the medullary plate seen in longitudinal section. The thinner wall of
the inner vesicle is formed of epiblast and somatic mesoblast, and
covers over the dorsal face of the embryo just like the amnion. It is
in fact usually spoken of as the amnion. The large cavity of the outer
vesicle is continuous with the body cavity, and into it projects the
solid mesoblastic allantois (_all_), so far without hypoblast[96].
[96] Hensen states that the hypoblast never grows into the
allantois; while Bischoff, though not very precise on the point,
implies that it does; he states however that it soon disappears.
The outer vesicle corresponds exactly with the yolk-sack, and its
mesoblastic layer receives the ordinary vascular supply.
The embryo becomes folded off from the yolk-sack in the usual way, but
comes to lie _not outside_ it as in the ordinary form, but _in its
interior_, and is connected with it by an umbilical stalk. The
yolk-sack forms the substitute for part of the subzonal membrane of
other Mammalia. The so-called amnion appears to me from its
development and position rather to correspond with the non-embryonic
part of the epiblastic wall (true subzonal membrane) of the
blastodermic vesicle of the ordinary mammalian forms than with the
true amnion; and a true amnion would seem not to be developed.
The allantois meets the yolk-sack on about the seventeenth day at the
region of its vascular connection with the uterine wall, and gives
rise to the placenta. A diagrammatic representation of the structure
of the embryo at this stage is given in fig. 163.
The peculiar inversion of the layers in the Guinea-pig has naturally
excited the curiosity of embryologists, but as yet no satisfactory
explanation has been offered of it.
At the time when the ovum first becomes fixed it will be remembered
that it resembles the early blastodermic vesicle of the Rabbit, and it
is natural to suppose that the apparently hypoblastic mass attached to
the inner wall of the vesicle becomes the solid body at the end of the
egg-cylinder. This appears to be Bischoff's view, but, as shewn above,
the solid mass is really the epiblast! Is it conceivable that the
hypoblast in one species becomes the epiblast in a closely allied
species? To my mind it is not conceivable, and I am reduced to the
hypothesis, put forward by Hensen, that in the course of the
attachment of the ovum to the wall of the uterus a rupture of walls of
the blastodermic vesicle takes place, and that they become completely
turned inside out. It must be admitted, however, that in the present
state of our knowledge of the development of the ovum on the seventh
and eighth days it is not possible to frame a satisfactory explanation
how such an inversion can take place.
[FIG. 163. DIAGRAMMATIC LONGITUDINAL SECTION OF AN OVUM OF A
GUINEA-PIG AND THE ADJACENT UTERINE WALLS AT AN ADVANCED STAGE OF
PREGNANCY. (After Bischoff.)
_yk._ inverted yolk-sack (umbilical vesicle) formed of an external
hypoblastic layer (shaded) and an internal vascular layer (black).
At the end of this layer is placed the sinus terminalis; _all._
allantois; _pl._ placenta.
The external shaded parts are the uterine walls.]
The Human Embryo. Our knowledge as to the early development of the
human embryo is in an unsatisfactory state. The positive facts we know
are comparatively few, and it is not possible to construct from them a
history of the development which is capable of satisfactory comparison
with that in other forms, unless all the early embryos known are to be
regarded as abnormal. The most remarkable feature in the development,
which was first clearly brought to light by Allen Thomson in 1839, is
the very early appearance of branched villi. In the last few years
several ova, even younger than those described by Allen Thomson, have
been met with, which exhibit this peculiarity.
The best-preserved of these ova is one described by Reichert (No.
237). This ovum, though probably not more than thirteen days old, was
completely enclosed by a decidua reflexa. It had (fig. 164 A and B) a
flattened oval form, measuring in its two diameters 5.5 mm. and 3.5
mm. The edge was covered with branched villi, while in the centre of
each of the flattened surfaces there was a spot free from villi. On
the surface adjoining the uterine wall was a darker area (_e_) formed
of two layers of cells, which is interpreted by Reichert as the
embryonic area, while the membrane forming the remainder of the ovum,
including the branched villi, was stated by Reichert to be composed of
a single row of epithelial cells.
Whether or no Reichert is correct in identifying his darker spot as
the embryonic area, it is fairly certain from the later observations
of Beigel and Löwe (No. 228), Ahlfeld (No. 227), and Kollmann (No.
234) on ova nearly as young as that of Reichert, that the wall of very
young ova has a more complicated structure than Reichert is willing to
admit. These authors do not however agree amongst themselves, but from
Kollmann's description, which appears to me the most satisfactory, it
is probable that it is composed of an outer epithelial layer, and an
inner layer of connective tissue, and that the connective tissue
extends at a very early period into the villi; so that the latter are
not hollow, as Reichert supposed them to be.
[FIG. 164. THE HUMAN OVA DURING EARLY STAGES OF DEVELOPMENT. (From
Quain's _Anatomy_.)
A. and B. Front and side view of an ovum figured by Reichert,
supposed to be about thirteen days. _e._ embryonic area.
C. An ovum of about four or five weeks shewing the general structure
of the ovum before the formation of the placenta. Part of the wall
of the ovum is removed to shew the embryo _in situ_. (After Allen
Thomson.)]
The villi, which at first leave the flattened poles free, seem soon to
extend first over one of the flat sides, and finally over the whole
ovum (fig. 164 C).
Unless the two-layered region of Reichert's ovum is the embryonic
area, nothing which can clearly be identified as an embryo has been
detected in these early ova. In an ovum described by Breus (No. 228),
and in one described long ago by Wharton-Jones a mass found in the
interior of the egg may perhaps be interpreted (His) as the remains of
the yolk. It is, however, very probable that all the early ova so far
discovered are more or less pathological.
The youngest ovum with a distinct embryo is one described by His (No.
232). This ovum, which is diagrammatically represented in fig. 168 in
longitudinal section, had the form of an oval vesicle completely
covered by villi, and about 8.5 mm. and 5.5 mm. in its two diameters,
and flatter on one side than on the other. An embryo with a yolk-sack
was attached to the inner side of the flatter wall of the vesicle by a
stalk, which must be regarded as the allantoic stalk[97], and the
embryo and yolk-sack filled up but a very small part of the whole
cavity of the vesicle.
[97] Allen Thomson informs me that he is very confident that such
a form of attachment between the hind end of the embryo and the
wall of the vesicle, as that described and figured by His in this
embryo, did not exist in any of the younger embryos examined by
him.
The embryo, which was probably not quite normal (fig. 165 A), was very
imperfectly developed; a medullary plate was hardly indicated, and,
though the mesoblast was unsegmented, the head fold, separating the
embryo from the yolk-sack (_um_), was already indicated. The amnion
(_am_) was completely formed, and vitelline vessels had made their
appearance.
[FIG. 165. THREE EARLY HUMAN EMBRYOS. (Copied from His.)
A. An early embryo described by His from the side. _am._ amnion;
_um._ umbilical vesicle; _ch._ chorion, to which the embryo is
attached by a stalk.
B. Embryo described by Allen Thomson about 12-14 days. _um._
umbilical vesicle; _md._ medullary groove.
C. Young embryo described by His. _um._ umbilical vesicle.]
Two embryos described by Allen Thomson (No. 239) are but slightly
older than the above embryos of His. Both of them probably belong to
the first fortnight of pregnancy. In both cases the embryo was more or
less folded off from the yolk-sack, and in one of them the medullary
groove was still widely open, except in the region of the neck (fig.
165 B). The allantoic stalk, if present, was not clearly made out, and
the condition of the amnion was also not fully studied. The smaller of
the two ova was just 6 mm. in its largest diameter, and was nearly
completely covered with simple villi, more developed on one side than
on the other.
In a somewhat later period, about the stage of a chick at the end of
the second day, the medullary folds are completely closed, the region
of the brain already marked, and the cranial flexure commencing. The
mesoblast is divided up into numerous somites, and the mandibular and
first two branchial arches are indicated. The embryo is still but
incompletely folded off from the yolk-sack below.
In a still older stage the cranial flexure becomes still more
pronounced, placing the mid-brain at the end of the long axis of the
body. The body also begins to be ventrally curved (fig. 165 C).
Externally human embryos at this age are characterised by the small
size of the anterior end of the head.
[FIG. 166. TWO VIEWS OF A HUMAN EMBRYO OF BETWEEN THE THIRD AND
FOURTH WEEK.
A. Side view. (From Kölliker; after Allen Thomson.) _a._ amnion;
_b._ umbilical vesicle; _c._ mandibular arch; _e._ hyoid arch;
_f._ commencing anterior limb; _g._ primitive auditory vesicle;
_h._ eye; _i._ heart.
B. Dorsal view to shew the attachment of the dilated allantoic stalk
to the chorion. (From a sketch by Allen Thomson.) _am._ amnion;
_all._ allantois; _ys._ yolk-sack.]
The flexure goes on gradually increasing, and in the third week of
pregnancy in embryos of about 4 mm. the limbs make their appearance.
The embryo at this stage (fig. 166), which is about equivalent to that
of a chick on the fourth day, resembles in almost every respect the
normal embryos of the Amniota. The cranial flexure is as pronounced as
usual, and the cerebral region has now fully the normal size. The
whole body soon becomes flexed ventrally, and also somewhat spirally.
The yolk-sack (_b_) forms a small spherical appendage with a long wide
stalk, and the embryo (B) is attached by an allantoic stalk with a
slight swelling (_all_), probably indicating the presence of a small
hypoblastic diverticulum, to the inner face of the chorion.
A remarkable exception to the embryos generally observed is afforded
by an embryo which has been described by Krause (No. 235). In this
embryo, which probably belongs to the third week of pregnancy, the
limbs were just commencing to be indicated, and the embryo was
completely covered by an amnion, but instead of being attached to the
chorion by an allantoic cord, it was quite free, and was provided with
a small spherical sack-like allantois, very similar to that of a
fourth-day chick, projected from its hind end.
[FIG. 167. FIGURES SHEWING THE EARLY CHANGES IN THE FORM OF THE
HUMAN HEAD. (From Quain's _Anatomy_.)
A. Head of an embryo of about four weeks. (After Allen Thomson.)
B. Head of an embryo of about six weeks. (After Ecker.)
C. Head of an embryo of about nine weeks.
1. mandibular arch; 1´. persistent part of hyomandibular cleft; _a._
auditory vesicle.]
No details are given as to the structure of the chorion or the
presence of villi upon it. The presence of such an allantois at this
stage in a human embryo is so unlike what is usually found that
Krause's statements have been received with considerable scepticism.
His even holds that the embryo is a chick embryo, and not a human one;
while Kölliker regards Krause's allantois as a pathological structure.
The significance to be attached to this embryo is dealt with below.
A detailed history of the further development of the human embryo does
not fall within the province of this work; while the later changes in
the embryonic membranes have already been dealt with (pp. 244-248).
For the changes which take place on the formation of the face I may
refer the reader to fig. 167.
The most obscure point connected with the early history of the human
ovum concerns the first formation of the allantois, and the nature of
the villi covering the surface of the ovum. The villi, if really
formed of mesoblast covered by epiblast, have the true structure of
chorionic villi; and can hardly be compared to the early villi of the
dog which are derived from the subzonal membrane, and still less to
those of the rabbit formed from the zona radiata.
Unless all the early ova so far described are pathological, it seems
to follow that the mesoblast of the chorion is formed before the
embryo is definitely established, and even if the pathological
character of these ova is admitted, it is nevertheless probable
(leaving Krause's embryo out of account), as shewn by the early
embryos of Allen Thomson and His, that it is formed before the closure
of the medullary groove. In order to meet this difficulty His supposes
that the embryo never separates from the blastodermic vesicle, but
that the allantoic stalk of the youngest embryo (fig. 168) represents
the persistent attachment between the two[98]. His' view has a good
deal to be said for it. I would venture, however, to suggest that
Reichert's embryonic area is probably not in the two-layered stage,
but that a mesoblast has already become established, and that it has
grown round the inner face of the blastodermic vesicle from the
(apparent) posterior end of the primitive streak. This growth I regard
as _a precocious formation of the mesoblast of the allantois_--an
exaggeration of the early formation of the allantoic mesoblast which
is characteristic of the Guinea-pig (_vide_ p. 264). This mesoblast,
together with the epiblast, forms a true chorion, so that in fig. 168,
and probably also in fig. 164 A and B, a true chorion has already
become established. The stalk connecting the embryo with the chorion
in His' earliest embryo (fig. 168) is therefore a true allantoic stalk
into which the hypoblastic allantoic diverticulum grows in for some
distance. How the yolk-sack (umbilical vesicle) is formed is not
clear. Perhaps, as suggested by His, it arises from the conversion of
a solid mass of primitive hypoblast directly into a yolk-sack. The
amnion is probably formed as a fold over the head end of the embryo in
the manner indicated in His' diagram (fig. 168 _Am_).
[98] For a fuller explanation of His' views I must refer the
reader to his Memoir (No. 232), pp. 170, 171, and to the diagrams
contained in it.
[FIG. 168. DIAGRAMMATIC LONGITUDINAL SECTION OF THE OVUM TO WHICH
THE EMBRYO (FIG. 165 A) BELONGED. (After His.)
_Am._ amnion; _Nb._ umbilical vesicle.]
These speculations have so far left Krause's embryo out of account.
How is this embryo to be treated? Krause maintains that all the other
embryos shewing an allantoic stalk at an early age are pathological.
This, though not impossible, appears to me, to say the least of it,
improbable; especially when it is borne in mind that embryos, which
have every appearance of being normal, of about the same age and
younger than Krause's, have been frequently observed, and have always
been found attached to the chorion by an allantoic stalk.
We are thus provisionally reduced to suppose either that the structure
figured by Krause is not the allantois, or that it is a very abnormal
allantois. It is perhaps just possible that it may be an abnormally
developed hypoblastic vesicle of the allantois artificially detached
from the mesoblastic layer,--the latter having given rise to the
chorion at an earlier date.
BIBLIOGRAPHY.
_General._
(168) K. E. von Baer. _Ueb. Entwicklungsgeschichte d. Thiere._
Königsberg, 1828-1837.
(169) Barry. "Researches on Embryology." First Series. _Philosophical
Transactions_, 1838, Part II. Second Series, Ibid. 1839, Part II.
Third Series, Ibid. 1840.
(170) Ed. van Beneden. _La maturation de l'oeuf, la fécondation et les
premières phases du développement embryonaire d. Mammifères._
Bruxelles, 1875.
(171) Ed. van Beneden. "Recherches sur l'embryologie des Mammifères."
_Archives de Biologie_, Vol. I. 1880.
(172) Ed. v. Beneden and Ch. Julin. "Observations sur la maturation
etc. de l'oeuf chez les Cheiroptères." _Archives de Biologie_, Vol. I.
1880.
(173) Th. L. W. Bischoff. _Entwicklungsgeschichte d. Säugethiere u.
des Menschen._ Leipzig, 1842.
(174) Th. L. W. Bischoff. _Entwicklungsgeschichte des Kanincheneies._
Braunschweig, 1842.
(175) Th. L. W. Bischoff. _Entwicklungsgeschichte des Hundeeies._
Braunschweig, 1845.
(176) Th. L. W. Bischoff. _Entwicklungsgeschichte des
Meerschweinchens._ Giessen, 1852.
(177) Th. L. W. Bischoff. _Entwicklungsgeschichte des Rehes._ Giessen,
1854.
(178) Th. L. W. Bischoff. "Neue Beobachtungen z. Entwicklungsgesch.
des Meerschweinchens." _Abh. d. bayr. Akad._, Cl. II. Vol. X. 1866.
(179) Th. L. W. Bischoff. _Historisch-kritische Bemerkungen z. d.
neuesten Mittheilungen üb. d. erste Entwick. d. Säugethiereier._
München, 1877.
(180) M. Coste. _Embryogénie comparée._ Paris, 1837.
(181) E. Haeckel. _Anthropogenie, Entwicklungsgeschichte des
Menschen._ Leipzig, 1874.
(182) V. Hensen. "Beobachtungen üb. d. Befrucht. u. Entwick. d.
Kaninchens u. Meerschweinchens." _Zeit. f. Anat. u. Entwick._, Vol. I.
1876.
(183) A. Kölliker. _Entwicklungsgeschichte d. Menschen u. d. höheren
Thiere._ Leipzig, 1879.
(184) A. Kölliker. "Die Entwick. d. Keimblätter des Kaninchens."
_Zoologischer Anzeiger_, Nos. 61, 62, Vol. III. 1880.
(185) N. Lieberkühn. _Ueber d. Keimblätter d. Säugethiere.
Doctor-Jubelfeier d. Herrn. H. Nasse._ Marburg, 1879.
(186) N. Lieberkühn. "Z. Lehre von d. Keimblättern d. Säugethiere."
_Sitz. d. Gesell. z. Beförd d. gesam. Naturwiss._ Marburg, No. 3.
1880.
(187) Rauber. "Die erste Entwicklung d. Kaninchens." _Sitzungsber. d.
naturfor. Gesell. z. Leipzig._ 1875.
(188) C. B. Reichert. "Entwicklung des Meerschweinchens." _Abh. der.
Berl. Akad._ 1862.
(189) E. A. Schäfer. "Description of a Mammalian ovum in an early
condition of development." _Proc. Roy. Soc._, No. 168. 1876.
(190) E. A. Schäfer. "A contribution to the history of development of
the guinea-pig." _Journal of Anat. and Phys._, Vol. X. and XI. 1876
and 1877.
_Foetal Membranes and Placenta._
(191) John Anderson. _Anatomical and Zoological Researches in Western
Yunnan._ London, 1878.
(192) K. E. von Baer. _Untersuchungen über die Gefässverbindung
zwischen Mutter und Frucht_, 1828.
(193) C. G. Carus. _Tabulae anatomiam comparativam illustrantes._
1831, 1840.
(194) H. C. Chapman. "The placenta and generative apparatus of the
Elephant." _Journ. Acad. Nat. Sc._, Philadelphia. Vol. VIII. 1880.
(195) C. Creighton. "On the formation of the placenta in the
guinea-pig." _Journal of Anat. and Phys._, Vol. XII. 1878.
(196) Ecker. _Icones Physiologicae._ 1852-1859.
(197) G. B. Ercolani. _The utricular glands of the uterus_, etc.,
translated from the Italian under the direction of H. O. Marcy.
Boston, 1880. Contains translations of memoirs published in the _Mem.
dell'Accad. d. Scienze d. Bologna_, and additional matter written
specially for the translation.
(198) G. B. Ercolani. _Nuove ricerche sulla placenta nei pesci
cartilaginosi e nei mammiferi._ Bologna, 1880.
(199) Eschricht. _De organis quae respirationi et nutritioni foetus
Mammalium inserviunt._ Hafniae, 1837.
(200) A. H. Garrod and W. Turner. "The gravid uterus and placenta of
Hyomoschus aquaticus." _Proc. Zool. Soc._, London, 1878.
(201) P. Harting. _Het ei en de placenta van Halicore Dugong. Inaug.
diss._ Utrecht. "On the ovum and placenta of the Dugong." Abstract by
Prof. Turner. _Journal of Anat. and Phys._, Vol. XIII.
(202) Th. H. Huxley. _The Elements of Comparative Anatomy._ London,
1864.
(203) A. Kölliker. "Ueber die Placenta der Gattung Tragulus." _Verh.
der Würzb. phys.-med. Gesellschaft_, Bd. X.
(204) C. D. Meigs. "On the reproduction of the Opossum (Didelphis
Virginiana)." _Amer. Phil. Soc. Trans._, Vol. X. 1853.
(205) H. Milne-Edwards. "Sur la Classification Naturelle." _Ann.
Sciences Nat._, Sér. 3, Vol. I. 1844.
(206) Alf. Milne-Edwards. "Recherches sur la famille des Chevrotains."
_Ann. des Sciences Nat._, Séries V., Vol. II. 1864.
(207) Alf. Milne-Edwards. "Observations sur quelques points de
l'Embryologie des Lemuriens, etc." _Ann. Sci. Nat._, Sér. V., Vol. XV.
1872.
(208) Alf. Milne-Edwards. "Sur la conformation du placenta chez le
Tamandua." _Ann. des Sci. Nat._, XV. 1872.
(209) Alf. Milne-Edwards. "Recherches s. l. enveloppes foetales du
Tatou à neuf bandes." _Ann. Sci. Nat._, Sér. VI., Vol. VIII. 1878.
(210) R. Owen. "On the generation of Marsupial animals, with a
description of the impregnated uterus of the Kangaroo." _Phil.
Trans._, 1834.
(211) R. Owen. "Description of the membranes of the uterine foetus of
the Kangaroo." _Mag. Nat. Hist._, Vol. I. 1837.
(212) R. Owen. "On the existence of an Allantois in a foetal Kangaroo
(Macropus major)." _Zool. Soc. Proc._, v. 1837.
(213) R. Owen. "Description of the foetal membranes and placenta of
the Elephant." _Phil. Trans._, 1857.
(214) R. Owen. _On the Anatomy of Vertebrates_, Vol. III. London,
1868.
(215) G. Rolleston. "Placental structure of the Tenrec, etc."
_Transactions of the Zoological Society_, Vol. V. 1866.
(216) W. Turner. "Observations on the structure of the human
placenta." _Journal of Anat. and Phys._, Vol. VII. 1868.
(217) W. Turner. "On the placentation of the Cetacea." _Trans. Roy.
Soc. Edinb._, Vol. XXVI. 1872.
(218) W. Turner. "On the placentation of Sloths (Choloepus
Hoffmanni)." _Trans. of R. Society of Edinburgh_, Vol. XXVII. 1875.
(219) W. Turner. "On the placentation of Seals (Halichoerus gryphus)."
_Trans. of R. Society of Edinburgh_, Vol. XXVII. 1875.
(220) W. Turner. "On the placentation of the Cape Ant-eater
(Orycteropus capensis)." _Journal of Anat. and Phys._, Vol. X. 1876.
(221) W. Turner. _Lectures on the Anatomy of the Placenta._ First
Series. Edinburgh, 1876.
(222) W. Turner. "Some general observations on the placenta, with
special reference to the theory of Evolution." _Journal of Anat. and
Phys._, Vol. XI. 1877.
(223) W. Turner. "On the placentation of the Lemurs." _Phil. Trans._,
Vol. 166, p. 2. 1877.
(224) W. Turner. "On the placentation of Apes." _Phil. Trans._, 1878.
(225) W. Turner. "The cotyledonary and diffused placenta of the
Mexican deer (Cervus Americanus)." _Journal of Anat. and Phys._, Vol.
XIII. 1879.
_Human Embryo._
(226) Fried. Ahlfeld. "Beschreibung eines sehr kleinen menschlichen
Eies." _Archiv f. Gynaekologie_, Bd. XIII. 1878.
(227) Herm. Beigel und Ludwig Loewe. "Beschreibung eines menschlichen
Eichens aus der zweiten bis dritten Woche der Schwangerschaft."
_Archiv f. Gynaekologie_, Bd. XII. 1877.
(228) K. Breus. "Ueber ein menschliches Ei aus der zweiten Woche der
Gravidität." _Wiener medicinische Wochenschrift_, 1877.
(229) M. Coste. _Histoire générale et particulière du développement
des corps organisés_, 1847-59.
(230) A. Ecker. _Icones Physiologicae._ Leipzig, 1851-1859.
(231) V. Hensen. "Beitrag z. Morphologie d. Körperform u. d. Gehirns
d. menschlichen Embryos." _Archiv f. Anat. u. Phys._, 1877.
(232) W. His. _Anatomie menschlicher Embryonen_, Part I. _Embryonen d.
ersten Monats._ Leipzig, 1880.
(233) J. Kollmann. "Die menschlichen Eier von 6 MM. Grösse." _Archiv
f. Anat. und Phys._, 1879.
(234) W. Krause. "Ueber d. Allantois d. Menschen." _Archiv f. Anat.
und Phys._, 1875.
(235) W. Krause. "Ueber zwei frühzeitige menschliche Embryonen."
_Zeit. f. wiss. Zool._, Vol. XXXV. 1880.
(236) L. Loewe. "Im Sachen der Eihäute jüngster menschlicher Eier."
_Archiv für Gynaekologie_, Bd. XIV. 1879.
(237) C. B. Reichert. "Beschreibung einer frühzeitigen menschlichen
Frucht im bläschenformigen Bildungszustande (sackformiger Keim von
Baer) nebst vergleichenden Untersuchungen über die bläschenformigen
Früchte der Säugethiere und des Menschen." _Abhandlungen der königl.
Akad. d. Wiss. zu Berlin_, 1873.
(238) Allen Thomson. "Contributions to the history of the structure of
the human ovum and embryo before the third week after conception; with
a description of some early ova." _Edinburgh Med. Surg. Journal_, Vol.
LII. 1839.
CHAPTER XI.
COMPARISON OF THE FORMATION OF THE GERMINAL LAYERS AND OF THE EARLY
STAGES IN THE DEVELOPMENT OF VERTEBRATES.
Although the preceding chapters of this volume contain a fairly
detailed account of the early developmental stages of different groups
of the Chordata, it will nevertheless be advantageous to give at this
place a short comparative review of the whole subject.
In this review only the most important points will be dwelt upon, and
the reader is referred for the details of the processes to the
sections on the development of the individual groups.
The subject may conveniently be treated under three heads.
(1) The formation of the gastrula and behaviour of the blastopore:
together with the origin of the hypoblast.
(2) The mesoblast and notochord.
(3) The epiblast.
At the close of the chapter is a short summary of the organs derived
from the several layers, together with some remarks on the growth in
length of the vertebrate embryo, and some suggestions as to the origin
of the allantois and amnion.
Formation of the gastrula. Amphioxus is the type in which the
developmental phenomena are least interfered with by the presence of
food-yolk.
In this form the segmentation results in a uniform, or nearly uniform,
blastosphere, one wall of which soon becomes thickened and
invaginated, giving rise to the hypoblast; while the larva takes the
form of a gastrula, with an archenteric cavity opening by a
blastopore. The blastopore rapidly narrows, while the embryo assumes
an elongated cylindrical form with the blastopore at its hinder
extremity (fig. 169 A). The blastopore now passes to the dorsal
surface, and by the flattening of this surface a medullary plate is
formed extending forwards from the blastopore (fig. 169 B). On the
formation of the medullary groove and its conversion into a canal, the
blastopore opens into this canal, and gives rise to a neurenteric
passage, leading from the neural canal into the alimentary tract (fig.
169 C and E). At a later period this canal closes, and the neural and
alimentary canals become separated.
[FIG. 169. EMBRYOS OF AMPHIOXUS. (After Kowalevsky.)
The parts in black with white lines are epiblastic; the shaded parts
are hypoblastic.
A. Gastrula stage in optical section.
B. Slightly later stage after the neural plate _np_ has become
differentiated, seen as a transparent object from the dorsal side.
C. Lateral view of a slightly older larva in optical section.
D. Dorsal view of an older larva with the neural canal completely
closed except for a small pore (_no_) in front.
E. Older larva seen as a transparent object from the side.
_bl._ blastopore (which becomes in D the neurenteric canal); _ne._
neurenteric canal; _np._ neural or medullary plate; _no._ anterior
opening of neural canal; _ch._ notochord; _so´_, _so´´_. first and
second mesoblastic somites.]
Such is the simple history of the layers in Amphioxus. In the simplest
types of Ascidians the series of phenomena is almost the same, but the
blastopore assumes a more definitely dorsal position.
Here also the blastopore lies at the hinder end of the medullary
groove, and on the closure of the groove becomes converted into a
neurenteric passage.
[FIG. 170. DIAGRAMMATIC LONGITUDINAL SECTIONS THROUGH THE EMBRYO OF
BOMBINATOR AT TWO STAGES, TO SHEW THE FORMATION OF THE GERMINAL
LAYERS. (Modified from Götte.)
_ep._ epiblast; _m._ dorsal mesoblast; _m´._ ventral mesoblast;
_hy._ hypoblast; _yk._ yolk; _x._ point of junction of the epiblast
and hypoblast at the dorsal side of the blastopore; _al._
mesenteron; _sg._ segmentation cavity.]
In the true Vertebrates the types which most approach Amphioxus are
the Amphibia, Acipenser and Petromyzon. We may take the first of these
as typical (though Petromyzon is perhaps still more so) and fig. 170 A
B C D represents four diagrammatic longitudinal vertical sections
through a form belonging to this group (Bombinator). The food-yolk is
here concentrated in what I shall call the lower pole of the egg,
which becomes the ventral aspect of the future embryo. The part of the
egg containing the stored-up food-yolk is, as has already been
explained in the chapter on segmentation (Vol. II. pp. 94 and 95), to
be regarded as equivalent to part of those eggs which do not contain
food-yolk; a fact which requires to be borne in mind in any attempt to
deal comparatively with the formation of the layers in the Vertebrata.
It may be laid down as a general law, which holds very accurately for
the Vertebrata, that in eggs in which the distribution of food-yolk is
not uniform, the size of the cells resulting from segmentation is
proportional to the quantity of food-material they contain. In
accordance with this law the cells of the Amphibian ovum are of
unequal size even at the close of segmentation. They may roughly be
divided into two categories, viz. the smaller cells of the upper pole
and the larger of the lower (fig. 170 A). The segmentation cavity
(_sg_) lies between the two, but is unsymmetrically placed near the
upper pole of the egg, owing to the large bulk of the ventrally placed
yolk-segments. In the inequality of the cells at the close of
segmentation the Amphibia stand in contrast with Amphioxus. The upper
cells are mainly destined to form the epiblast, and the lower the
hypoblast and mesoblast.
The next change which takes place is an invagination, the earliest
traces of which are observable in fig. 170 A. The invagination is not
however so simple as in Amphioxus. Owing in fact to the presence of
the food-yolk it is a mixture of invagination by epibole and by
embole.
At the point marked _x_ in fig. 170 A, which corresponds with the
future hind end of the embryo, and is placed on the equatorial line
marking the junction of the large and small cells, there takes place a
normal invagination, which gives rise solely to the hypoblast of the
dorsal wall of the alimentary tract and to part of the dorsal
mesoblast. The invaginated layer grows inwards from the point _x_
along what becomes the dorsal side of the embryo; and between it and
the yolk-cells below is formed a slit-like space (fig. 170 B and C).
This space is the mesenteron. It is even better shewn in fig. 171
representing the process of invagination in Petromyzon. The point _x_
in fig. 170 where epiblast, mesoblast and hypoblast are continuous, is
homologous with the dorsal lip of the blastopore in Amphioxus. In the
course of the invagination the segmentation cavity, as in Amphioxus,
becomes obliterated.
While the above invagination has been taking place, the epiblast cells
have been simply growing in an epibolic fashion round the yolk; and by
the stage represented in fig. 170 C and D the exposed surface of yolk
has become greatly diminished; and an obvious blastopore is thus
established. Along the line of the growth a layer of mesoblast cells
(_m´_), continuous at the sides with the invaginated mesoblast layer,
has become differentiated from the small cells (fig. 170 A)
intermediate between the epiblast cells and the yolk.
Owing to the nature of the above process of invagination the
mesenteron is at first only provided with an epithelial wall on its
dorsal side, its ventral wall being formed of yolk-cells (fig. 170).
At a later period some of the yolk-cells become transformed into the
epithelial cells of the ventral wall, while the remainder become
enclosed in the alimentary cavity and employed as pabulum. The whole
of the yolk-cells, after the separation of the mesoblast, are however
morphologically part of the hypoblast.
The final fate of the blastopore is nearly the same as in Amphioxus.
It gradually narrows, and the yolk-cells which at first plug it up
disappear (fig. 170 C and D). The neural groove, which becomes formed
on the dorsal surface of the embryo, is continued forwards from the
point _x_ in fig. 170 C. On the conversion of this groove into a canal
the canal freely opens behind into the blastopore; and a condition is
reached in which the blastopore still opens to the exterior and also
into the neural canal fig. 170 D. In a later stage (fig. 172) the
external opening of the blastopore becomes closed by the medullary
folds meeting behind it, but the passage connecting the neural and
alimentary canals is left. There is one small difference between the
Frog and Amphioxus in the relation of the neural canal to the
blastopore. In both types the medullary folds embrace and meet behind
it, so that it comes to occupy a position at the hind extremity of the
medullary groove. In Amphioxus the closure of the medullary folds
commences behind, so that the external opening of the blastopore is
obliterated simultaneously with the commencing formation of the
medullary canal; but in the Frog the closure of the medullary folds
commences anteriorly and proceeds backwards, so that the obliteration
of the external opening of the blastopore is a late event in the
formation of the medullary canal.
[FIG. 171. LONGITUDINAL VERTICAL SECTION THROUGH AN EMBRYO OF
PETROMYZON OF 136 HOURS.
_me._ mesoblast; _yk._ yolk-cells; _al._ alimentary tract; _bl._
blastopore; _s.c._ segmentation cavity.]
The anus is formed (_vide_ fig. 172) some way in front of the
blastopore, and a postanal gut, continuous with the neurenteric canal,
is thus established. Both the postanal gut and the neurenteric canal
eventually disappear.
[FIG. 172. LONGITUDINAL SECTION THROUGH AN ADVANCED EMBRYO OF
BOMBINATOR. (After Götte.)
_m._ mouth; _an._ anus; _l._ liver; _ne._ neurenteric canal; _mc._
medullary canal; _ch._ notochord; _pn._ pineal gland.]
The two other types classed above with the Amphibia, viz. Petromyzon
and Acipenser, agree sufficiently closely with them to require no
special mention; but with reference to both types it may be pointed
out that the ovum contains relatively more food-yolk than that of the
Amphibian type just described, and that this leads amongst other
things to the lower layer cells extending up the sides of the
segmentation cavity, and assisting in forming its roof.
The next type to be considered is that of Elasmobranchii. The yolk in
the ovum of these forms is enormously bulky, and the segmentation is
in consequence a partial one. At first sight the differences between
their development and that of Amphibia would appear to be very great.
In order fully to bridge over the gulf which separates them I have
given three diagrammatic longitudinal sections of an ideal form
intermediate between Amphibia and Elasmobranchii, which differs
however mainly from the latter in the smaller amount of food-yolk; and
by their aid I trust it will be made clear that the differences
between the Amphibia and Elasmobranchii are of an insignificant
character. In fig. 174 A B C are represented three diagrammatic
longitudinal sections of Elasmobranch embryos, and in fig. 173 A B C
three longitudinal sections of the ideal intermediate form. The
diagrams correspond with the Amphibian diagrams already described
(fig. 170). In the first stage figured there is present in all of
these forms a segmentation cavity (_sg_) situated not centrally but
near the surface of the egg. The roof of the cavity is thin, being
composed in the Amphibian embryo of epiblast alone, and in the
Elasmobranch of epiblast and _lower layer cells_. The floor of the
cavity is formed of so-called yolk, which forms the main mass of the
embryo. In Amphibia the yolk is segmented. In Elasmobranchii there is
at first a layer of primitive hypoblast cells separating the
segmentation cavity from the yolk proper; this however soon
disappears, and an unsegmented yolk with _free nuclei_ fills the place
of the segmented yolk of the Amphibia. The small cells at the sides of
the segmentation cavity in Amphibia correspond exactly in function and
position with the lower layer cells of the Elasmobranch blastoderm.
The relation of the yolk to the blastoderm in the Elasmobranch embryo
at this stage of development very well suits the view of its homology
with the yolk-cells of the Amphibian embryo. The only essential
difference between the two embryos arises from the roof of the
segmentation cavity being formed in the Elasmobranch embryo of lower
layer cells, which are absent in the Amphibian embryo. This difference
no doubt depends upon the greater quantity of yolk in the Elasmobranch
ovum, and a similar distribution of the lower layer cells is found in
Acipenser and in Petromyzon.
[FIG. 173. THREE DIAGRAMMATIC LONGITUDINAL SECTIONS THROUGH AN IDEAL
TYPE OF VERTEBRATE EMBRYO INTERMEDIATE IN THE MODE OF FORMATION OF
ITS LAYERS BETWEEN AMPHIBIA OR PETROMYZON AND ELASMOBRANCHII.
_sg._ segmentation cavity; _ep._ epiblast; _m._ mesoblast; _hy._
hypoblast; _nc._ neural canal; _al._ mesenteron; _n._ nuclei of the
yolk.]
In the next stage for the Elasmobranch (fig. 173 and 174 B) and for
the Amphibian (fig. 170 C) or better still Petromyzon (fig. 171) the
agreement between the three types is again very close. For a small arc
(_x_) of the edge of the blastoderm the epiblast and hypoblast become
continuous, while at all other parts the epiblast, accompanied by
lower layer cells, grows round the yolk or round the large cells which
correspond to it. The yolk-cells of the Amphibian embryo form a
comparatively small mass, and are therefore rapidly enveloped; while
in the case of the Elasmobranch embryo, owing to the greater mass of
the yolk, the same process occupies a long period. The portion of the
blastoderm, where epiblast and hypoblast become continuous, forms the
dorsal lip of an opening--the blastopore--which leads into the
alimentary cavity. This cavity has the same relation in all the three
cases. It is lined dorsally by lower layer cells, and ventrally by
yolk-cells or what corresponds with yolk-cells; a large part of the
ventral epithelium of the alimentary canal being in both cases
eventually derived from the yolk. In Amphibia this epithelium is
formed directly from the existing cells, while in Elasmobranchii it is
derived from cells formed around the nuclei of the yolk.
As in the earlier stage, so in the present one, the anatomical
relations of the yolk to the blastoderm in the one case
(Elasmobranchii) are nearly identical with those of the yolk-cells to
the blastoderm in the other (Amphibia).
The main features in which the two embryos differ, during the stage
under consideration, arise from the same cause as the solitary point
of difference during the preceding stage.
In Amphibia the alimentary cavity is formed coincidently with a true
ingrowth of cells from the point where epiblast and hypoblast become
continuous; and from this ingrowth the dorsal wall of the alimentary
cavity is formed. The same ingrowth causes the obliteration of the
segmentation cavity.
In Elasmobranchs, owing probably to the larger bulk of the lower layer
cells, the primitive hypoblast cells arrange themselves in their final
position during segmentation, and no room is left for a true
invagination; but instead of this there is formed a simple space
between the blastoderm and the yolk. The homology of this space with
the primitive invagination cavity is nevertheless proved by the
survival of a number of features belonging to the ancestral condition
in which a true invagination was present. Amongst the more important
of these are the following:--(1) The continuity of epiblast and
hypoblast at the dorsal lip of the blastopore. (2) The continuous
conversion of primitive hypoblast cells into permanent hypoblast,
which gradually extends inwards towards the segmentation cavity, and
exactly represents the course of the invagination whereby in Amphibia
the dorsal wall of the alimentary cavity is formed. (3) The
obliteration of the segmentation cavity during the period when the
pseudo-invagination is occurring.
In the next stage there appear more important differences between the
two types than in the preceding stages, though here again the points
of resemblance predominate.
Figs. 170 D and 174 C represent longitudinal sections through embryos
after the closure of the medullary canal. The neurenteric canal is
established; and in front and behind the epithelium of the ventral
wall of the mesenteron has begun to be formed.
The mesoblast is represented as having grown in between the medullary
canal and the superjacent epiblast.
There are at this stage two points in which the embryo Elasmobranch
differs from the corresponding Amphibian embryo. (1) In the formation
of the neurenteric canal, there is no free passage leading into the
mesenteron from the exterior as in Amphibia (fig. 170 D). (2) The
whole yolk is not enclosed by the epiblast, and therefore part of the
blastopore is still open.
The difference between Amphibia and Elasmobranchii in the first of
these points is due to the fact that in Elasmobranchii, as in
Amphioxus, the neural canal becomes first closed behind; and
simultaneously with its closure the lateral parts of the lips of the
blastopore, which are continuous with the medullary folds, meet
together and shut in the hindmost part of the alimentary tract.
The second point is of some importance for understanding the relations
of the formation of the layers in the amniotic and the non-amniotic
Vertebrates. Owing to its large size the whole of the yolk in
Elasmobranchii is not enclosed by the epiblast at the time when the
neurenteric canal is established; in other words a small posterior and
dorsal portion of the blastopore is shut off in the formation of the
neurenteric canal. The remaining ventral portion becomes closed at a
later period. Its closure takes place in a linear fashion, commencing
at the hind end of the embryo, and proceeding apparently backwards;
though, as this part eventually becomes folded in to form the ventral
wall of the embryo, the closure of it really travels forwards. The
process causes however the embryo to cease to lie at the edge of the
blastoderm, and while situated at some distance from the edge, to be
connected with it by a linear streak, representing the coalesced lips
of the blastopore. The above process is diagrammatically represented
in fig. 175 B; while as it actually occurs it is shewn in fig. 30, p.
63. The whole closure of the blastopore in Elasmobranchii is
altogether unlike what takes place in Amphibia, where the blastopore
remains as a circular opening which gradually narrows till it becomes
completely enveloped in the medullary folds (fig. 175 A).
[FIG. 174. DIAGRAMMATIC LONGITUDINAL SECTIONS OF AN ELASMOBRANCH
EMBRYO.
_Epiblast_ without shading. _Mesoblast_ black with clear outlines to
the cells. _Lower layer cells_ and _hypoblast_ with simple shading.
_ep._ epiblast; _m._ mesoblast; _al._ alimentary cavity; _sg._
segmentation cavity; _nc._ neural canal; _ch._ notochord; _x._ point
where epiblast and hypoblast become continuous at the posterior end
of the embryo; _n._ nuclei of yolk.
A. Section of young blastoderm, with the segmentation cavity
enclosed in the lower layer cells (primitive hypoblast).
B. Older blastoderm with embryo in which hypoblast and mesoblast are
distinctly formed, and in which the alimentary cavity has
appeared. The segmentation cavity is still represented, though by
this stage it has in reality disappeared.
C. Older blastoderm with embryo in which the neural canal is formed,
and is continuous posteriorly with the alimentary canal. The
notochord, though shaded like mesoblast, belongs properly to the
hypoblast.]
On the formation of the neurenteric canal the body of the embryo
Elasmobranch becomes gradually folded off from the yolk, which, owing
to its great size, forms a large sack appended to the ventral side of
the body. The part of the somatopleure, which grows round it, is to be
regarded as a modified portion of the ventral wall of the body. The
splanchnopleure also envelops it, so that, morphologically speaking,
the yolk lies within the mesenteron.
The Teleostei, so far as the first formation of the layers is
concerned, resemble in all essential features the Elasmobranchii, but
the neurenteric canal is apparently not developed (?), owing to the
obliteration of the neural canal; and the roof of the segmentation
cavity is formed of epiblast only.
* * * * *
In the preceding pages I have attempted to shew that the Amphibia,
Acipenser, Petromyzon, the Elasmobranchii and the Teleostei agree very
closely in the mode of formation of the gastrula. The unsymmetrical
gastrula or pseudo-gastrula which is common to them all is, I believe,
to be explained by the form of the vertebrate body. In Amphioxus,
where the small amount of food-yolk present is distributed uniformly,
there is no reason why the invagination and resulting gastrula should
not be symmetrical. In true Vertebrates, where more food-yolk is
present, the shape and structure of the body render it necessary for
the food-yolk to be stored away on the ventral side of the alimentary
canal. It is this fact which causes the asymmetry of the gastrula,
since it is not possible for the part of the ovum, which will become
the ventral wall of the alimentary tract, and which is loaded with
food-yolk, to be invaginated in the same fashion as the dorsal wall.
Sauropsida. The comparison of the different types of the Ichthyopsida
is fairly simple, but the comparison of the Sauropsida with the
Ichthyopsida is a far more difficult matter. In all the Sauropsida
there is a large food-yolk, and the segmentation agrees closely with
that in the Elasmobranchii. It might have been anticipated that the
resemblance would continue in the subsequent development. This however
is far from being the case. The medullary plate, instead of lying at
the edge of the blastoderm, lies in the centre, and its formation is
preceded by that of a peculiar structure, the primitive streak, which,
on the formation of the medullary plate, is found to lie at the hinder
end of the latter and to connect it with the edge of the blastoderm.
[FIG. 175. DIAGRAMS ILLUSTRATING THE POSITION OF THE BLASTOPORE, AND
THE RELATION OF THE EMBRYO TO THE YOLK IN VARIOUS MEROBLASTIC
VERTEBRATE OVA.
A. Type of Frog. B. Elasmobranch type. C. Amniotic Vertebrate.
_mg._ medullary plate; _ne._ neurenteric canal; _bl._ portion of
blastopore adjoining the neurenteric canal. In B this part of the
blastopore is formed by the edges of the blastoderm meeting and
forming a linear streak behind the embryo; and in C it forms the
structure known as the primitive streak. _yk._ part of the yolk not
yet enclosed by the blastoderm.]
The possibility of a comparison between the Sauropsida and the
Elasmobranchii depends upon the explanation being possible of (1) the
position of the embryo near the centre of the blastoderm, and (2) the
nature of the primitive streak.
The answers to these two questions are, according to my view,
intimately bound together.
I consider that the embryos of the Sauropsida have come to occupy a
central position in the blastoderm owing to the abbreviation of a
process similar to that by which, in Elasmobranchii, the embryo is
removed from the edge of the blastoderm; and that the primitive streak
represents the linear streak connecting the Elasmobranch embryo with
the edge of the blastoderm after it has become removed from its
previous peripheral position, as well as the true neurenteric part of
the Elasmobranch blastopore.
This view of the nature of the primitive streak, which is
diagrammatically illustrated in fig. 175, will be rendered more clear
by a brief review of the early developmental processes in the
Sauropsida.
After segmentation the blastoderm becomes divided, as in
Elasmobranchii, into two layers. It is doubtful whether there is any
true representative of the segmentation cavity. The first structure to
appear in the blastoderm is a linear streak placed at the hind end of
the blastoderm, known as the primitive streak (figs. 175 C, _bl_ and
176, _pr_). At the front end of the primitive streak the epiblast and
hypoblast become continuous, just as they do at the dorsal lip of the
blastopore in Elasmobranchii. Continued back from this point is a
streak of fused mesoblast and epiblast to the under side of which a
linear thin layer of hypoblast is more or less definitely attached.
A further structure, best developed in the Lacertilia, appears in the
form of a circular passage perforating the blastoderm at the front end
of the primitive streak (fig. 176, _ne_). This passage is bounded
anteriorly by the layer of cells forming the continuation of the
hypoblast into the epiblast.
In the next stage the medullary plate becomes formed in front of the
primitive streak (fig. 175 C), and the medullary folds are continued
backwards so as to enclose the upper opening of the passage through
the blastoderm. On the closure of the medullary canal (fig. 177) this
passage leads from the medullary canal into the alimentary tract, and
is therefore the neurenteric canal; and a postanal gut also becomes
formed. The latter part of the above description applies especially to
the Lizard: but in Chelonia and most Birds distinct remnants (_vide_
pp. 162-164) of the neurenteric canal are developed.
On the hypothesis that the Sauropsidan embryos have come to occupy
their central position, owing to an abbreviation of a process
analogous to the linear closing of the blastopore behind the embryos
of Elasmobranchii, all the appearances above described receive a
satisfactory explanation. The passage at the front end of the
primitive streak is the dorsal part of the blastopore, which in
Elasmobranchii becomes converted into the neurenteric canal. The
remainder of the primitive streak represents, in a rudimentary form,
the linear streak in Elasmobranchii, formed by the coalesced edges of
the blastoderm, which connects the hinder end of the embryo with the
still open yolk blastopore. That it is in later stages not continued
to the edge of the blastoderm, as in Elasmobranchii, is due to its
being a rudimentary organ. The more or less complete fusion of the
layers in the primitive streak is simply to be explained by this
structure representing the coalesced edges of the blastopore; and the
growth outwards from it of the mesoblast is probably a remnant of a
primitive dorsal invagination of the mesoblast and hypoblast like that
in the Frog.
[FIG. 176. DIAGRAMMATIC LONGITUDINAL SECTION OF AN EMBRYO OF
LACERTA.
_pp._ body cavity; _am._ amnion; _ne._ neurenteric canal; _ch._
notochord; _hy._ hypoblast; _ep._ epiblast; _pr._ primitive streak.
In the primitive streak all the layers are partially fused.]
The final enclosure of the yolk in the Sauropsida takes place at the
pole of the yolk-sack opposite the embryo, so that the blastopore is
formed of three parts, (1) the neurenteric canal, (2) the primitive
streak behind this, (3) the blastopore at the pole of the yolk-sack
opposite the embryo.
Mammalia. The features of the development of the placental Mammalia
receive their most satisfactory explanation on the hypothesis that
their ancestors were provided with a large-yolked ovum like that of
the Sauropsida. The food-yolk must be supposed to have ceased to be
developed on the establishment of a maternal nutrition through the
uterus.
On this hypothesis all the developmental phenomena subsequently to the
formation of the blastodermic vesicle receive a satisfactory
explanation.
[FIG. 177. DIAGRAMMATIC LONGITUDINAL SECTION THROUGH THE POSTERIOR
END OF AN EMBRYO BIRD AT THE TIME OF THE FORMATION OF THE ALLANTOIS.
_ep._ epiblast; _Sp.c._ spinal canal; _ch._ notochord; _n.e._
neurenteric canal; _hy._ hypoblast; _p.a.g._ postanal gut; _pr._
remains of primitive streak folded in on the ventral side; _al._
allantois; _me._ mesoblast; _an._ point where anus will be formed;
_p.c._ perivisceral cavity; _am._ amnion; _so._ somatopleure; _sp._
splanchnopleure.]
The whole of the blastodermic vesicle, except the embryonic area,
represents the yolk-sack, and the growth of the hypoblast and then of
the mesoblast round its inner wall represents the corresponding
growths in the Sauropsida. As in the Sauropsida it becomes constricted
off from the embryo, and the splanchnopleuric stalk of the sack opens
into the ileum in the usual way.
[FIG. 178. OPTICAL SECTIONS OF A RABBIT'S OVUM AT TWO STAGES CLOSELY
FOLLOWING UPON THE SEGMENTATION. (After E. van Beneden.)
_ep._ epiblast; _hy._ primary hypoblast; _bp._ Van Beneden's
so-called blastopore. The shading of the epiblast and hypoblast is
diagrammatic.]
In the formation of the embryo out of the embryonic area the phenomena
which distinguish the Sauropsida from the Ichthyopsida are repeated.
The embryo lies in the centre of the area; and before it is formed
there appears a primitive streak, from which there grows out the
greater part of the mesoblast. At the front end of the primitive
streak the hypoblast and epiblast become continuous, though a
perforated neurenteric blastopore has not yet been detected.
All these Sauropsidan features are so obvious that they need not be
insisted on further. The embryonic evidence of the common origin of
Mammalia and Sauropsida, both as concerns the formation of the layers
and of the embryonic membranes, is as clear as it can be. The only
difficulty about the early development of Mammalia is presented by the
epibolic gastrula and the formation of the blastodermic vesicle (figs.
178 and 179). That the segmentation is a complete one is no doubt a
direct consequence of the reduction of the food-yolk, but the growth
of the epiblast cells round the hypoblast and the final enclosure of
the latter, which I have spoken of as giving rise to the epibolic
gastrula, are not so easily explained.
[FIG. 179. RABBIT'S OVUM BETWEEN 70-90 HOURS AFTER IMPREGNATION.
(After E. van Beneden.)
_bv._ cavity of blastodermic vesicle (yolk-sack); _ep._ epiblast;
_hy._ primitive hypoblast; _Zp._ mucous envelope.]
It might have been supposed that this process was equivalent to the
growth of the blastoderm round the yolk in the Sauropsida, but then
the blastopore ought to be situated at the pole of the egg opposite to
the embryonic area, while, according to Van Beneden, the embryonic
area corresponds approximately to the blastopore.
Van Beneden regards the Mammalian blastopore as equivalent to that in
the Amphibia, but if the position previously adopted about the
primitive streak is to be maintained, Van Beneden's view must be
abandoned. No satisfactory phylogenetic explanation of the Mammalian
gastrula by epibole has in my opinion as yet been offered.
The formation of the blastodermic vesicle may perhaps be explained on
the view that in the Proto-mammalia the yolk-sack was large, and that
its blood-vessels took the place of the placenta of higher forms. On
this view a reduction in the bulk of the _ovarian ovum_ might easily
have taken place at the same time that the presence of _a large
yolk-sack_ was still necessary for the purpose of affording surface of
contact with the uterus.
_The formation of the Mesoblast and of the Notochord._
[FIG. 180. SECTIONS OF AN AMPHIOXUS EMBRYO AT THREE STAGES.
(After Kowalevsky.)
A. Section at gastrula stage.
B. Section of an embryo slightly younger than that represented in
fig. 169 D.
C. Section through the anterior part of an embryo at the stage
represented in fig. 169 E.
_np._ neural plate; _nc._ neural canal; _mes._ archenteron in A and
B, and mesenteron in C; _ch._ notochord; _so._ mesoblastic somite.]
Amphioxus. The mesoblast originates in Amphioxus, as in several
primitive invertebrate types, from a pair of lateral diverticula,
constricted off from the archenteron (fig. 180). Their formation
commences at the front end of the body and is thence carried
backwards, and each diverticulum contains a prolongation of the cavity
of the archenteron. After their separation from the archenteron the
dorsal parts of these diverticula become divided by transverse septa
into successive somites, the cavities of which eventually disappear;
while the walls become mainly converted into the muscle-plates, but
also into the tissue around the notochord which corresponds with the
vertebral tissue of the higher Chordata.
The ventral part of each diverticulum, which is prolonged so as to
meet its fellow in the middle ventral line, does not become divided
into somites, but contains a continuous cavity, which becomes the body
cavity of the adult. The inner layer of this part forms the splanchnic
mesoblast, and the outer layer the somatic mesoblast.
The notochord would almost appear to arise as a third median and
dorsal diverticulum of the archenteron (fig. 180 _ch_). At any rate it
arises as a central fold of the wall of this cavity, which is
gradually constricted off from before backwards.
Urochorda. In simple Ascidians the above processes undergo a slight
modification, which is mainly due (1) to a general simplification of
the organization, and (2) to the non-continuation of the notochord
into the trunk.
[FIG. 181. TRANSVERSE OPTICAL SECTION OF THE TAIL OF AN EMBRYO OF
PHALLUSIA MAMMILLATA. (After Kowalevsky.)
The section is from an embryo of the same age as fig. 8 IV.
_ch._ notochord; _n.c._ neural canal; _me._ mesoblast; _al´._
hypoblast of tail.]
The whole dorsal wall of the posterior part of the archenteron is
converted into the notochord (fig. 181 _ch_), and the lateral walls
into the mesoblast (_me_); so that the original lumen of the posterior
part of the archenteron ceases to be bounded by hypoblast cells, and
disappears as such. Part of the ventral wall remains as a solid cord
of cells (_al´_) The anterior part of the archenteron in front of the
notochord passes wholly into the permanent alimentary tract.
The derivation of the mesoblast from the lateral walls of the
posterior part of the archenteron is clearly comparable with the
analogous process in Amphioxus.
Vertebrata. In turning from Amphioxus to the true Vertebrata we find
no form in which diverticula of the primitive alimentary tract give
rise to the mesoblast. There is reason to think that the type
presented by the Elasmobranchii in the formation of the mesoblast is
as primitive as that of any other group. In this group the mesoblast
is formed, nearly coincidently with the hypoblast of the dorsal wall
of the mesenteron, as two lateral sheets, one on each side of the
middle line (fig. 182 _m_). These two sheets are at first solid
masses; and their differentiation commences in front and is continued
backwards. After their formation the notochord arises from the axial
portion of the hypoblast (which had no share in giving rise to the two
mesoblast plates) as a solid thickening (fig. 183 _ch´_), which is
separated from it as a circular rod. Its differentiation, like that of
the mesoblastic plates, commences in front. The mesoblast plates
subsequently become divided for their whole length into two layers,
between which a cavity is developed (fig. 184). The dorsal parts of
the plates become divided by transverse partitions into somites, and
these somites with their contained cavities are next separated from
the more ventral parts of the plates (fig. 185 _mp_). In the somites
the cavities become eventually obliterated, and from their inner sides
plates of tissue for the vertebral bodies (fig. 186 _Vr_) are
separated; while the outer parts, consisting of two sheets, containing
the remains of the original cavity, form the muscle-plates (_mp_).
[FIG. 182. TWO TRANSVERSE SECTIONS OF AN EMBRYO PRISTIURUS OF THE
SAME AGE AS FIG. 17.
A. Anterior section.
B. Posterior section.
_mg._ medullary groove; _ep._ epiblast; _hy._ hypoblast; _n.al._
cells formed round the nuclei of the yolk which have entered the
hypoblast; _m._ mesoblast.
The sections shew the origin of the mesoblast.]
[FIG. 183. THREE SECTIONS OF A PRISTIURUS EMBRYO SLIGHTLY OLDER THAN
FIG. 28 B.
The sections shew the development of the notochord.
_Ch._ notochord; _Ch´._ developing notochord; _mg._ medullary
groove; _lp._ lateral plate of mesoblast; _ep._ epiblast; _hy._
hypoblast.]
[FIG. 184. TRANSVERSE SECTION THROUGH THE TAIL-REGION OF A
PRISTIURUS EMBRYO OF THE SAME AGE AS FIG. 28 E.
_df._ dorsal fin; _sp.c._ spinal cord; _pp._ body cavity; _sp._
splanchnic layer of mesoblast; _so._ somatic layer of mesoblast;
_mp´._ commencing differentiation of muscles; _ch._ notochord; _x._
subnotochordal rod arising as an outgrowth of the dorsal wall of the
alimentary tract; _al._ alimentary tract.]
The undivided ventral portion gives rise to the general somatic and
splanchnic mesoblast (fig. 185), and the cavity between its two layers
constitutes the body cavity. The originally separate halves of the
body cavity eventually meet and unite in the ventral median line
throughout the greater part of the body, though in the tail they
remain distinct and are finally obliterated. Dorsally they are
separated by the mesentery. From the mesoblast at the junction of the
dorsal and ventral parts of the primitive plates is formed the
urinogenital system.
That the above mode of origin of the mesoblast and notochord is to be
regarded as a modification of that observable in Amphioxus seems
probable from the following considerations:--
In the first place, the mesoblast is split off from the hypoblast not
as a single mass but as a pair of distinct masses, comparable with the
paired diverticula in Amphioxus. Secondly, the body cavity, when it
appears in the mesoblast plates, _does not arise as a single cavity,
but as a pair of cavities, one for each plate of mesoblast_; and these
cavities remain permanently distinct in some parts of the body, and
nowhere unite till a comparatively late period. Thirdly, the primitive
body cavity of the embryo is not confined to the region in which a
body cavity exists in the adult, _but extends to the summit of the
muscle-plates_, at first separating parts which become completely
fused in the adult to form the great lateral muscles of the body.
[FIG. 185. SECTION THROUGH THE TRUNK OF A SCYLLIUM EMBRYO SLIGHTLY
YOUNGER THAN 28 F.
_sp.c._ spinal canal; _W._ white matter of spinal cord; _pr._
posterior nerve-roots; _ch._ notochord; _x._ subnotochordal rod;
_ao._ aorta; _mp._ muscle-plate; _mp´._ inner layer of muscle-plate
already converted into muscles; _Vr._ rudiment of vertebral body;
_st._ segmental tube; _sd._ segmental duct; _sp.v._ spiral valve;
_v._ subintestinal vein; _p.o._ primitive generative cells.]
It is difficult to understand how the body cavity could thus extend
into the muscle-plates on the supposition that it represents a
primitive split in the mesoblast between the wall of the gut and the
body-wall; but its extension to this part is quite intelligible, on
the hypothesis that it represents the cavities of two diverticula of
the alimentary tract, from the muscular walls of which the voluntary
muscular system has been derived; and it may be pointed out that the
derivation of part of the muscular system from what is apparently
splanchnic mesoblast is easily explained on the above hypothesis, but
not, so far as I see, on any other.
Such are the main features, presented by the mesoblast in
Elasmobranchii, which favour the view of its having originally formed
the walls of the alimentary diverticula. Against this view of its
nature are the facts (1) of the mesoblast plates being at first solid,
and (2) of the body cavity as a consequence of this never
communicating with the alimentary canal. These points, in view of our
knowledge of embryological modifications, cannot be regarded as great
difficulties in my hypothesis. We have many examples of organs, which,
though in most cases arising as involutions, yet appear in other cases
as solid ingrowths. Such examples are afforded by the optic vesicle,
auditory vesicle, and probably also by the central nervous system of
Osseous Fishes. In most Vertebrates these organs are formed as hollow
involutions from the exterior; in Osseous Fishes, however, as solid
involutions, in which a cavity is secondarily established.
[FIG. 186. HORIZONTAL SECTION THROUGH THE TRUNK OF AN EMBRYO OF
SCYLLIUM CONSIDERABLY YOUNGER THAN 28 F.
The section is taken at the level of the notochord, and shews the
separation of the cells to form the vertebral bodies from the
muscle-plates.
_ch._ notochord; _ep._ epiblast; _Vr._ rudiment of vertebral body;
_mp._ muscle-plate; _mp´._ portion of muscle-plate already
differentiated into longitudinal muscles.]
There are strong grounds for thinking that in all Vertebrates the
mesoblast plates on each side of the notochord originate
independently, much as in Elasmobranchii, and that the notochord is
derived from the axial hypoblast; but there are some difficulties in
the application of this general statement to all cases. In Amphibia,
Ganoids, and Petromyzon, where the dorsal hypoblast is formed by a
process of invagination as in Amphioxus, the dorsal mesoblast also
owes its origin to this invagination, in that the indifferent
invaginated layer becomes divided into hypoblast and mesoblast.
Amongst these forms the mesoblast sheet, when separated from the
hypoblast, is certainly _not_ continuous across the middle line in
Petromyzon (Calberla) and the Newt (Scott and Osborn), and doubtfully
so in the other forms. It arises, in fact, as in Elasmobranchii, as
two independent plates. The fact of these plates originating from an
invaginated layer can only be regarded in the light of an
approximation to the primitive type found in Amphioxus.
In Petromyzon and the Newt the whole axial plate of dorsal hypoblast
becomes separated off from the rest of the hypoblast as the notochord,
and this mode of origin for the notochord resembles more closely that
in Amphioxus than the mode of origin in Elasmobranchii.
In Teleostei, there is reason to think that the processes in the
formation of the mesoblast accord closely with what has been described
as typical for the Ichthyopsida, but there are still some points
involved in obscurity.
[FIG. 187. TRANSVERSE SECTION THROUGH AN EMBRYO RABBIT OF EIGHT
DAYS.
_ep._ epiblast; _me._ mesoblast; _hy._ hypoblast; _mg._ medullary
groove.]
Leaving the Ichthyopsida, we may pass to the consideration of the
Sauropsida and Mammalia. In both of these types there is evidence to
shew that a part of the mesoblast is formed _in situ_ at the same time
as the hypoblast, from the lower strata of segmentation spheres. This
mesoblast is absent in the front part of the area pellucida, and on
the formation of the primitive streak (blastopore), an outgrowth of
mesoblast arises from it as in Amphibia, etc. From this region the
mesoblast spreads as a continuous sheet to the sides and posterior
part of the blastoderm. In the region of the embryo, its exact
behaviour has not in some cases been quite satisfactorily made out.
There are reasons for thinking that it appears as two sheets _not
united_ in the axial line in both Lacertilia (fig. 126) and Mammalia
(fig. 187), and this to some extent holds true for Aves (_vide_ p.
156). In Lacertilia (fig. 188) and Mammalia, the axial hypoblast
becomes wholly converted into the notochord, which at the posterior
end of the body is continued into the epiblast at the dorsal lip of
the blastopore; while in Birds the notochord is formed by a very
similar (fig. 189 _ch_) process.
The above processes in the formation of the mesoblast are for the most
part easily explained by a comparison with the lower types. The
outgrowth of the mesoblast from the sides of the primitive streak is a
rudiment of the dorsal invagination of hypoblast and mesoblast found
in Amphibia; and the apparent outgrowth of the mesoblast from the
epiblast in the primitive streak is no more to be taken as a proof of
the epiblastic origin of the mesoblast, than the continuity of the
epiblast with the invaginated hypoblast and mesoblast at the lips of
the blastopore in the Frog of the derivation of these layers from the
epiblast in this type.
[FIG. 188. DIAGRAMMATIC LONGITUDINAL SECTION THROUGH AN EMBRYO
LIZARD TO SHEW THE RELATIONS OF THE NEURENTERIC CANAL (_ne_) AND OF
THE PRIMITIVE STREAK (_pr_).
_am._ amnion; _ep._ epiblast; _hy._ hypoblast; _ch._ notochord;
_pp._ body cavity; _ne._ neurenteric canal; _pr._ primitive streak.]
[FIG. 189. TRANSVERSE SECTION THROUGH THE EMBRYONIC REGION OF THE
BLASTODERM OF A CHICK AT THE TIME OF THE FORMATION OF THE NOTOCHORD,
BUT BEFORE THE APPEARANCE OF THE MEDULLARY GROOVE.
_ep._ epiblast; _hy._ hypoblast; _ch._ notochord; _me._ mesoblast;
_n._ nuclei in the yolk of the germinal wall _yk._]
The division of the mesoblast into two plates along the dorsal line of
the embryo, and the formation of the notochord from the axial
hypoblast, are intelligible without further explanation. The
appearance of part of the mesoblast before the formation of the
primitive streak is a process of the same nature as the
differentiation of hypoblast and mesoblast in Elasmobranchii without
an invagination.
In the Sauropsida, some of the mesoblast of the vascular area would
appear to be formed _in situ_ out of the germinal wall, by a process
of cell-formation similar to that which takes place in the yolk
adjoining the blastoderm in Elasmobranchii and Teleostei. The
mesoblast so formed is to be compared with that which arises on the
ventral side of the embryo in the Frog, by a direct differentiation of
the yolk-cells.
What was stated for the Elasmobranchii with reference to the general
fate of the mesoblast holds approximately for all the other forms.
_The Epiblast._
The epiblast in a large number of Chordata arises as a single row of
more or less columnar cells. Since the epidermis, into which it
becomes converted, is formed of two more or less distinct strata in
all Chordata except Amphioxus and Ascidians, the primitive row of
epiblast cells, when single, necessarily becomes divided in the course
of development into two layers.
In some of the Vertebrata, viz. the Anurous Amphibia, Teleostei,
Acipenser, and Lepidosteus, the epiblast is from the first formed of
two distinct strata. The upper of these, formed of a single row of
cells, is known as the epidermic stratum, and the lower, formed of
several rows, as the nervous stratum. In these cases the two original
strata of the epiblast are equivalent to those which appear at a later
period in the other forms. Thus Vertebrates may be divided into groups
according to the primitive condition of their epiblast, viz. a larger
group with but a single stratum of cells at first; and a smaller group
with two strata.
While there is no great difficulty in determining the equivalent parts
of the epidermis in these two groups, it still remains an open
question in which of them the epiblast retains its primitive
condition.
Though it is not easy to bring conclusive proofs on the one side or
the other, the balance of argument appears to me to be decidedly in
favour of regarding the condition of the epiblast in the larger group
as primitive, and its condition in the smaller group as secondary, and
due to the throwing back of the differentiation of the epiblast to a
very early period of development.
In favour of this view may be urged (1) the fact that the simple
condition is retained in Amphioxus through life. (2) The correlation
in Amphibia, and the other forms belonging to this group, between a
closed auditory pit and the early division of the epiblast into two
strata; there being no doubt that the auditory pit was at first
permanently open, a condition of the epiblast which necessitates its
never having an external opening must clearly be secondary. (3) It
appears more likely that a particular genetic feature should be thrown
back in development, than that such an important feature, as a
distinction between two primary layers, should be absolutely lost
during an early period of development, and then reappear in later
stages.
The fact of the epiblast of the neural canal being divided, like the
remainder of the layer, into nervous and epidermic parts, cannot, I
think, be used as an argument in favour of the opposite view to that
here maintained. It seems probable that the central canal of the
nervous system arose phylogenetically as an involution from the
exterior, and that the epidermis lining it is merely part of the
original epidermis, which has retained its primitive structure as a
simple stratum, but is naturally distinguishable from the nervous
structures adjacent to it.
Where the epiblast is divided at an early period into two strata, the
nervous stratum is always the active one, and takes the main share in
forming all the organs derived from the layer.
Formation of the central nervous system. In all Chordata an axial
strip of the dorsal epiblast, extending from the lip of the blastopore
to the anterior extremity of the head, and known as the medullary
plate, becomes isolated from the remainder of the layer to give rise
to the central nervous axis.
According to the manner in which this takes place, three types may,
however, be distinguished. In Amphioxus the axial strip becomes first
detached from the adjoining epiblast, which then meets and forms a
continuous layer above it (fig. 190 A and B _np_). The sides of the
medullary plate, which is thus shut off from the surface, bend over
and meet so as to convert the plate into a canal (fig. 190 C _nc_). In
the second and ordinary type the sides of the medullary plate fold
over and meet so as to form a canal before the plate becomes isolated
from the external epiblast.
[FIG. 190. SECTIONS OF AN AMPHIOXUS EMBRYO AT THREE STAGES. (After
Kowalevsky.)
A. Section at gastrula stage.
B. Section of an embryo slightly younger than that represented in
fig. 169 D.
C. Section through the anterior part of an embryo at the stage
represented in fig. 169 E.
_np._ neural plate; _nc._ neural canal; _mes._ archenteron in A and
B, and mesenteron in C; _ch._ notochord; _so._ mesoblastic somite.]
The third type is characteristic of Lepidosteus, Teleostei, and
Petromyzon. Here the axial plate becomes narrowed in such a way that
it forms a solid keel-like projection towards the ventral surface
(fig. 191 _Me_). This keel subsequently becomes separated from the
remainder of the epidermis, and a central canal is afterwards
developed in it. Calberla and Scott hold that the epidermic layer of
the skin is involuted into this keel in Petromyzon, and Calberla
maintains the same view for Teleostei (fig. 32), but further
observations on this subject are required. In the Teleostei a very
shallow depression along the axis of the keel is the only indication
of the medullary groove of other forms.
In Amphioxus (fig. 190), the Tunicata, Petromyzon (?), Elasmobranchii
(fig. 182), the Urodela and Mammalia (fig. 187), the epiblast of the
medullary plate is only formed of a single row of cells at the time
when the formation of the central nervous system commences; but,
except in Amphioxus and the Tunicata, it becomes several cells deep
before the completion of the process. In other types the epiblast is
several cells deep even before the differentiation of a medullary
plate. In the Anura, the nervous layer of the epidermis alone is
thickened in the formation of the central nervous system (fig. 72);
and after the closure of the medullary canal, the epidermic layer
fuses for a period with the nervous layer, though on the subsequent
formation of the central epithelium of the nervous canal, there can be
little doubt that it becomes again distinct.
[FIG. 191. SECTION THROUGH AN EMBRYO OF LEPIDOSTEUS ON THE FIFTH DAY
AFTER IMPREGNATION.
_MC._ medullary cord; _Ep._ epiblast; _Me._ mesoblast; _hy._
hypoblast; _Ch._ notochord.]
It seems almost certain that the formation of the central nervous
system from a solid keel-like thickening of the epidermis is a derived
and secondary mode; and that the folding of the medullary plate into a
canal is primitive. Apart from its greater frequency the latter mode
of formation of the central nervous system is shewn to be the
primitive type by the fact that it offers a simple explanation of the
presence of the central canal of the nervous system; while the
existence of such a canal cannot easily be explained on the assumption
that the central nervous system was originally developed as a
keel-like thickening of the epiblast.
It is remarkable that the primitive medullary plate rarely exhibits
any indication of being formed of two symmetrical halves. Such
indications are, however, found in the Amphibia (fig. 192 and fig.
72); and, since in the adult state the nervous cord exhibits nearly as
distinct traces of being formed of two united strands as does the
ventral nerve-cord of many Chætopods, it is quite possible that the
structure of the medullary plate in Amphibia may be more primitive
than that in other types[99].
[99] A parallel to the unpaired medullary plate of most Chordata
is supplied by the embryologically unpaired ventral cord of most
Gephyrea and some crustacea. In these forms there can be little
doubt that the ventral cord has arisen from the fusion of two
originally independent strands, so that it is not an extremely
improbable hypothesis to suppose that the same may have been the
case in the Chordata.
Formation of the organs of special sense. The more important parts of
the organs of smell, sight, and hearing are derived from the epiblast;
and it has been asserted that the olfactory pit, optic vesicles and
auditory pit take their origin from a special sense plate, continuous
at first with this medullary plate. In my opinion this view cannot be
maintained.
[FIG. 192. TRANSVERSE SECTION THROUGH THE CEPHALIC REGION OF A YOUNG
NEWT EMBRYO. (After Scott and Osborn.)
_In.hy._ invaginated hypoblast, the dorsal part of which will form
the notochord; _ep._ epiblast of neural plate; _sp._
splanchnopleure; _al._ alimentary tract; _yk._ and _Y.hy._
yolk-cells.]
In the case of the group of forms in which the epiblast is early
divided into nervous and epidermic layers, the former layer alone
becomes involuted in the formation of the auditory pit and the lens,
the external openings of which are never developed, while it is also
mainly concerned in the formation of the olfactory pit.
_Summary of the more important Organs derived from the three
germinal layers._
The epiblast primarily gives origin to two very important parts of the
body, viz. the central nervous system and the epidermis.
It is from the involuted epiblast of the neural tube that the whole of
the grey and white matter of the brain and spinal cord appears to be
developed, the simple columnar cells of the epiblast being directly
transformed into the characteristic multipolar nerve cells. The whole
of the sympathetic nervous system and the peripheral nervous elements
of the body, including both the spinal and the cranial nerves and
ganglia, are epiblastic in origin.
The epithelium (ciliated in the young animal) lining the canalis
centralis of the spinal cord, together with that lining the ventricles
of the brain, is the undifferentiated remnant of the primitive
epiblast.
The epiblast also forms the epidermis; not however the dermis, which
is of mesoblastic origin. The line of junction between the epiblast
and the mesoblast coincides with that between the epidermis and the
dermis. From the epiblast are formed all such tegumentary organs or
parts of organs as are epidermic in nature.
In addition to the above, the epiblast plays an important part in the
formation of the organs of special sense.
According to their mode of formation, these organs may be arranged
into two divisions. In the first come the organs where the sensory
expansion is derived from the involuted epiblast of the medullary
canal. To this class belongs the retina, including the pigment
epithelium of the choroid, which is formed from the original optic
vesicle budded out from the fore-brain.
To the second class belong the epithelial expansions of the membranous
labyrinth of the ear, and the cavity of the nose, which are formed by
an involution of the epiblast covering the external surface of the
embryo. These accordingly have no primary connection with the brain.
'Taste bulbs' and other terminal nervous organs, such as those of the
lateral line in fishes, are also structures formed from the external
epiblast.
In addition to these we have the crystalline lens formed of involuted
epiblast as well as the cavity of the mouth and anus, and the glands
derived from them. The pituitary body is also epiblastic in origin.
From the hypoblast are derived the epithelium of the digestive canal,
the epithelium of the trachea, bronchial tubes and air cells, the
cylindrical epithelium of the ducts of the liver, pancreas, thyroid
body, and other glands of the alimentary canal, as well as the hepatic
cells constituting the parenchyma of the liver, developed from the
hypoblast cylinders given off around the primary hepatic diverticula.
Homologous probably with the hepatic cells, and equally of hypoblastic
origin, are the spheroidal 'secreting cells' of the pancreas and other
glands. The epithelium of the salivary glands, though these so closely
resemble the pancreas, is probably of epiblastic origin, inasmuch as
the cavity of the mouth is entirely lined by epiblast.
The hypoblast also lines the allantois. To these parts must be added
the notochord and subnotochordal rod. From the mesoblast are formed
all the remaining parts of the body. The muscles, the bones, the
connective tissue and the vessels, both arteries, veins, capillaries
and lymphatics with their appropriate epithelium, are entirely formed
from the mesoblast.
The generative and urinary organs are entirely derived from the
mesoblast. It is worthy of notice that the epithelium of the urinary
glands, though resembling the hypoblastic epithelium of the alimentary
canal, is undoubtedly mesoblastic.
From the mesoblast are lastly derived all the muscular, connective
tissue, and vascular elements, as well of the alimentary canal and its
appendages as of the skin and the tegumentary organs. Just as it is
only the epidermic moiety of the latter which is derived from the
epiblast, so it is only the epithelium of the former which comes from
the hypoblast.
_Growth in length of the Vertebrate Embryo._
With reference to the formation and growth in length of the body of
the Vertebrate embryo two different views have been put forward, which
can be best explained by taking the Elasmobranch embryo as our type.
One of these views, generally held by embryologists and adopted in the
previous pages, is that the Elasmobranch embryo arises from a
differentiation of the edge of the blastoderm; which extends inwards
from the edge for some little distance. This differentiation is
supposed to contain within itself the rudiments of the whole of the
embryo with the exception of the yolk-sack; and the hinder extremity
of it, at the edge of the blastoderm, is regarded as corresponding
with the hind end of the body of the adult. The growth in length takes
place by a process of intussusception, and, till there are formed the
full number of mesoblastic somites, it is effected, as in Chætopods,
by the continual addition of fresh somites between the last-formed
somite and the hind end of the body.
A second and somewhat paradoxical view has been recently brought into
prominence by His and Rauber. This view has moreover since been taken
up by many embryologists, and has led to strange comparisons between
the formation of the mesoblastic plates of the Chætopods and the
medullary folds of Vertebrata. According to this view the embryo grows
in length by the coalescence of the two halves of the thickened edges
of the blastoderm in the dorsal median line. The groove between the
coalescing edges is the medullary groove, which increases in length by
the continued coalescence of fresh portions of the edge of the
blastoderm.
The following is His' own statement of his view: "I have shewn that
the embryo of Osseous Fishes grows together in length from two
symmetrically-placed structures in the thickened edge of the
blastoderm. Only the foremost end of the head and the hindermost end
of the tail undergo no concrescence, since they are formed out of that
part of the edge of the blastoderm which, together with the two
lateral halves, completes the ring. The whole edge of the blastoderm
is used in the formation of the embryo."
The edges of the blastoderm which meet to form the body of the embryo
are regarded as the blastopore, so that, on this view, the blastopore
primitively extends for the whole length of the dorsal side of the
embryo, and the groove between the coalesced lips becomes the
medullary groove.
It is not possible for me to enter at any great length into the
arguments used to support this position.
They may be summarised as (1) The general appearance; _i.e._ that the
thickened edge of the blastoderm is continuous with the medullary
fold.
(2) Certain measurements (His) which mainly appear to me to prove that
the growth takes place by the addition of fresh somites between that
last formed and the end of the body.
(3) Some of the phenomena of double monsters (Rauber).
None of these arguments appear to be very forcible, but as the view of
His and Rauber, if true, would certainly be important, I shall attempt
shortly to state the arguments against it, employing as my type the
Elasmobranchii, by the development of which, according to His, the
view which he adopts is more conclusively proved than by that of any
other group.
(1) The general appearance of the thickened edge of the blastoderm
becoming continuous with the medullary folds has been used as an
argument for the medullary folds being merely the coalesced thickened
edges of the blastoderm. Since, however, the medullary folds are
merely parts of the medullary plate, and since the medullary plate is
continuous with the adjoining epiblast of the embryonic rim, the
latter structure must be continuous with the medullary folds however
they are formed, and the mere fact of their being so continuous cannot
be used as an argument either way. Moreover, were the concrescence
theory true, the coalescing edges of the blastoderm might be expected
to form an acute angle with each other, which they are far from doing.
(2) The medullary groove becomes closed behind earlier than in front,
and the closure commences while the embryo is still quite short, and
_before the hind end has begun to project over the yolk_. After the
medullary canal becomes closed, and is continued behind into the
alimentary canal by the neurenteric passage, it is clearly impossible
for any further increase in length to take place by concrescence. If
therefore His' and Rauber's view is accepted, it will have to be
maintained that only a small part of the body is formed by concrescence,
while the larger posterior part grows by intussusception. The
difficulty involved in this supposition is much increased by the fact
that long after the growth by concrescence must have ceased the yolk
blastopore still remains open, and the embryo is still attached to the
edge of the blastoderm; so that it cannot be maintained that the
growth by concrescence has come to an end because the thickened edges
of the blastoderm have completely coalesced.
The above are arguments derived simply from a consideration of the
growth of the embryo; and they prove (1) that the points adduced by
His and Rauber are not at all conclusive; (2) that the growth in
length of the greater part of the body takes place by the addition of
fresh somites behind, as in Chætopods, and it would therefore be
extremely surprising that a small middle part of the body should grow
in quite a different way.
Many minor arguments used by His might be replied to, but it is hardly
necessary to do so, and some of them depend upon erroneous views as to
the course of development, such as an argument about the notochord,
which depends for its validity upon the assumption that the notochord
ridge appears at the same time as the medullary plate, while, as a
matter of fact, the ridge does not appear till considerably later. In
addition to the arguments of the class hitherto used, there may be
brought against the His-Rauber view a series of arguments from
comparative embryology.
(1) Were the vertebrate blastopore to be co-extensive with the dorsal
surface, as His and Rauber maintain, clear evidence of this ought to
be apparent in Amphioxus. In Amphioxus, however, the blastopore is at
first placed exactly at the hind end of the body, though later it
passes up just on to the dorsal side (_vide_ p. 4). It nearly closes
before the appearance of the medullary groove or mesoblastic somites;
and the medullary folds have nothing to do with its lips, except in so
far as they are continuous with them behind, just as in
Elasmobranchii.
(2) The food-yolk in the Vertebrata is placed on the ventral side of
the body, and becomes enveloped by the blastoderm; so that in all
large-yolked Vertebrates the ventral walls of the body are obviously
completed by the closure of the lips of the blastopore, on the ventral
side.
If His and Rauber are right the dorsal walls are also completed by the
closure of the blastopore, so that the whole of the dorsal, as well as
of the ventral wall of the embryo, must be formed by the concrescence
of the lips of the blastopore; which is clearly a _reductio ad
absurdum_ of the whole theory. To my own arguments on the subject I
may add those of Kupffer, who has very justly criticised His'
statements, and has shewn that growth of the blastoderm in Clupea and
Gasterosteus is absolutely inconsistent with the concrescence theory.
The more the theory of His and Rauber is examined by the light of
comparative embryology, the more does it appear quite untenable; and
it may be laid down as a safe conclusion from a comparative study of
vertebrate embryology that the blastopore of Vertebrates is
primitively situated at the hind end of the body, but that, owing to
the development of a large food-yolk, it also extends, in most cases,
over a larger or smaller part of the ventral side.
_The origin of the Allantois and Amnion._
The development and structure of the allantois and amnion have already
been dealt with at sufficient length in the chapters on Aves and
Mammalia; but a few words as to the origin of these parts will not be
out of place here.
The Allantois. The relations of the allantois to the adjoining organs,
and the conversion of its stalk into the bladder, afford ample
evidence that it has taken its origin from a urinary bladder such as
is found in Amphibia. We have in tracing the origin of the allantois
to deal with a case of what Dohrn would call 'change of function.' The
allantois is in fact a urinary bladder which, _precociously_ developed
and enormously extended in the embryo, has acquired respiratory
(Sauropsida) and nutritive (Mammalia) functions. No form is known to
have been preserved with the allantois in a transitional state between
an ordinary bladder and a large vascular sack.
The advantage of secondary respiratory organs during foetal life, in
addition to the yolk-sack, is evinced by the fact that such organs are
very widely developed in the Ichthyopsida. Thus in Elasmobranchii we
have the external gills (cf. p. 62). Amongst Amphibia we have the tail
modified to be a respiratory organ in Pipa Americana; and in
Notodelphis, Alytes and Cæcilia compressicanda the external gills are
modified and enlarged for respiratory purposes within the egg (cf. pp.
140 and 143).
The Amnion. The origin of the amnion is more difficult to explain than
that of the allantois; and it does not seem possible to derive it from
any pre-existing organ.
It appears to me, however, very probable that it was evolved _pari
passu_ with the allantois, as a simple fold of the somatopleure round
the embryo, into which the allantois extended itself as it increased
in size and became a respiratory organ. It would be obviously
advantageous for such a fold, having once started, to become larger
and larger in order to give more and more room for the allantois to
spread into.
The continued increase of this fold would lead to its edges meeting on
the dorsal side of the embryo, and it is easy to conceive that they
might then coalesce.
To afford room for the allantois close to the surface of the egg,
where respiration could most advantageously be carried on, it would be
convenient that the two laminæ of the amnion--the true and false
amnion--should then separate and leave a free space above the embryo,
and thus it may have come about that a separation finally takes place
between the true and false amnion.
This explanation of the origin of the amnion, though of course
hypothetical, has the advantage of suiting itself in most points to
the actual ontogeny of the organ. The main difficulty is the early
development of the head-fold of the amnion, since, from the position
of the allantois, it might have been anticipated that the tail-fold
would be the first formed and most important fold of the amnion.
BIBLIOGRAPHY.
(239) F. M. Balfour. "A comparison of the early stages in the
development of Vertebrates." _Quart. J. of Micr. Science_, Vol. XV.
1875.
(240) F. M. Balfour. "A monograph on the development of Elasmobranch
Fishes." London, 1878.
(241) F. M. Balfour. "On the early development of the Lacertilia
together with some observations, etc." _Quart. J. of Micr. Science_,
Vol. XIX. 1879.
(242) A. Götte. _Die Entwicklungsgeschichte d. Unke._ Leipzig, 1875.
(243) W. His. "Ueb. d. Bildung d. Haifischembryonen." _Zeit. f. Anat.
u. Entwick._, Vol. II. 1877. Cf. also His' papers on Teleostei, Nos.
65 and 66.
(244) A. Kowalevsky. "Entwick. d. Amphioxus lanceolatus." _Mém. Acad.
des Sciences St Pétersbourg_, Ser. VII. Tom. XI. 1867.
(245) A. Kowalevsky. "Weitere Studien üb. d. Entwick. d. Amphioxus
lanceolatus." _Archiv f. mikr. Anat._, Vol. XIII. 1877.
(246) C. Kupffer. "Die Entstehung d. Allantois u. d. Gastrula d.
Wirbelthiere." _Zool. Anzeiger_, Vol. II. 1879, pp. 520, 593, 612.
(247) R. Remak. _Untersuchungen üb. d. Entwicklung d. Wirbelthiere_,
1850-1858.
(248) A. Rauber. _Primitivstreifen u. Neurula d. Wirbelthiere._
Leipzig, 1877.
CHAPTER XII.
OBSERVATIONS ON THE ANCESTRAL FORM OF THE CHORDATA.
The present section of this work would not be complete without some
attempt to reconstruct, from the materials recorded in the previous
chapters, and from those supplied by comparative anatomy, the
characters of the ancestors of the Chordata; and to trace as far as
possible from what invertebrate stock this ancestor was derived.
The second of these questions has been recently dealt with in a very
suggestive manner by both Dohrn (No. 250) and Semper (Nos. 255 and
256), but it is still so obscure that I shall refrain from any
detailed discussion of it.
While differing very widely in many points both Dohrn and Semper have
arrived at the view, already tentatively put forward by earlier
anatomists, that the nearest allies of the Chordata are to be sought
for amongst the Chætopoda, and that the dorsal surface of the Chordata
with the spinal cord corresponds morphologically with the ventral
surface of the Chætopods with the ventral ganglion chain. In
discussing this subject some time ago[100] I suggested that we must
look for the ancestors of the Chordata, not in allies of the present
Chætopoda, but in a stock of segmented forms descended from the same
unsegmented types as the Chætopoda, but in which two lateral
nerve-cords, like those of Nemertines, coalesced dorsally, instead of
ventrally to form a median nervous cord. This group of forms, if my
suggestion as to its existence is well founded, appears now to have
perished. The recent researches of Hubrecht on the anatomy of the
Nemertines[101] have, however, added somewhat to the probability of my
views, in that they shew that in some existing Nemertines the
nerve-cords approach each other very closely in the dorsal line.
[100] _Monograph on the development of Elasmobranch Fishes_, pp.
170-173.
[101] Hubrecht, "Zur Anat. u. Phys. d. Nervensystems der
Nemertinen." _Kön. Akad. Wiss. Amsterdam_; and "Researches on the
Nervous System of Nemertines." _Quart. Journ. of Micr. Science_,
1880.
With reference to the characters of the ancestor of the Chordata the
following pages contain a few tentative suggestions rather than an
attempt to deal with the whole subject; while the origin of certain of
the organs is dealt with in a more special manner in the chapters on
organogeny which form the second part of this work.
Before entering upon the more special subject of this chapter, it will
be convenient to clear the ground by insisting on a few morphological
conclusions to be drawn from the study of Amphioxus,--a form which,
although probably in some respects degenerate, is nevertheless capable
of furnishing on certain points very valuable evidence.
(1) In the first place it is clear from Amphioxus that the ancestors
of the Chordata were segmented, and that their mesoblast was divided
into myotomes which extended even into the region in front of the
mouth. The mesoblast of the greater part of what is called the head in
the Vertebrata proper was therefore segmented like that of the trunk.
(2) The only internal skeleton present was the unsegmented
notochord--a fact which demonstrates that the skeleton is of
comparatively little importance for the solution of a large number of
fundamental questions, as for example the point which has been mooted
recently as to whether gill-clefts existed at one time in front of the
present mouth; and for this reason:--that from the evidence of
Amphioxus and the lower Vertebrata[102] it is clear that such clefts,
if they ever existed, _had atrophied completely_ before the
formation of cartilaginous branchial bars; so that any skeletal
structures in front of the mouth, which have been interpreted by
morphologists as branchial bars, can never have acted in supporting
the walls of branchial clefts.
[102] The greater part of the branchial skeleton of Petromyzon
appears clearly to belong to an extra-branchial system much more
superficially situated than the true branchial bars of the higher
forms. At the same time there is no doubt that certain parts of
the skeleton of the adult Lamprey have, as pointed out by Huxley,
striking points of resemblance to parts of a true mandibular and
hyoid arches. Further embryological evidence is required on the
subject, but the statements on this head on p. 84 ought to be
qualified.
Should Huxley's views on this subject be finally proved correct,
it is probable that, taking into consideration the resemblance of
these skeletal parts in the Tadpole to those in the Lamprey, the
cartilaginous mandibular bar, before being in any way modified to
form true jaws, became secondarily adapted to support a suctorial
mouth, and that it subsequently became converted into the true
jaws. Thus the evolution of this bar in the Frog would be a true
repetition of the ancestral history, while its ontogeny in
Elasmobranchii and other types would be much abbreviated. For a
fuller statement on this point I must refer the reader to the
chapter on the skull.
It is difficult to believe that the posterior branchial bars
could have coexisted with such a highly developed branchial
skeleton as that in Petromyzon, so that the absence of the
posterior branchial bars in Petromyzon receives by far its most
plausible explanation on the supposition that Petromyzon is
descended from a vertebrate stock in which true branchial bars
had not been evolved.
(3) The region which, in the Vertebrata, forms the oesophagus and
stomach, was, in the ancestors of the Chordata, perforated by
gill-clefts. This fact, which has been clearly pointed out by
Gegenbaur, is demonstrated by the arrangement of the gill-clefts in
Amphioxus, and by the distribution of the vagus nerve in the
Vertebrata[103]. On the other hand the insertion of the liver, which
was probably a very primitive organ, appears to indicate with
approximate certainty the posterior limit of the branchial clefts.
[103] The extension forwards in the vertebrata of an
uninterrupted body-cavity into the region previously occupied by
visceral clefts presents no difficulty. In Amphioxus the true
body cavity extends forwards, more or less divided by the
branchial clefts, for the whole length of the branchial region,
and in embryos of the lower Vertebrata there is a section of the
body cavity--the so-called head-cavities--between each pair of
pouches. On the disappearance of the pouches all these parts
would naturally coalesce into a continuous whole.
With these few preliminary observations we may pass to the main
subject of this section. A fundamental question which presents itself
on the threshold of our enquiries is the differentiation of the head.
In the Chætopoda the head is formed of a præoral lobe and of the oral
segment; while in Arthropods a somewhat variable number of segments
are added behind to this primitive head, and form with it what may be
called a secondary compound head. It is fairly clear that the section
of the trunk, which, in Amphioxus, is perforated by the visceral
clefts, has become the head in the Vertebrates proper, so that the
latter forms are provided with a secondary head like that of
Arthropods. There remain however difficult questions (1) as to the
elements of which this head is composed, and (2) as to the extent of
its differentiation in the ancestors of the Chordata.
In Arthropods and Chætopods there is a very distinct element in the
head known as the procephalic lobe in the case of Arthropods, and the
præoral lobe in that of Chætopods; and this lobe is especially
characterized by the fact that the supraoesophageal ganglia and optic
organs are formed as differentiations of part of the epiblast covering
it. Is such an element to be recognized in the head of the Chordata?
From a superficial examination of Amphioxus the answer would
undoubtedly be no; but then it has to be borne in mind that Amphioxus,
in correlation with its habit of burying itself in sand, is especially
degenerate in the development of its sense-organs; so that it is not
difficult to believe that its præoral lobe may have become so reduced
as not to be recognizable. In the true Vertebrata there is a portion
of the head which has undoubtedly many features of the præoral lobe in
the types already alluded to, viz. the part containing the cerebral
hemispheres and the thalamencephalon. If there is any part of the
brain homologous with the supraoesophageal ganglia of the
Invertebrates, and it is difficult to believe there is not such a
part, it must be part of, or contain, the fore-brain. The fore-brain
resembles the supraoesophageal ganglia in being intimately connected
in its development with the optic organs, and in supplying with nerves
only organs of sense. Its connection with the olfactory organs is an
argument in the same direction. Even in Amphioxus there is a small
bulb at the end of the nervous tube supplying what is very probably
the homologue of the olfactory organ of the Vertebrata; and it is
quite possible that this bulb is the reduced rudiment of what forms
the fore-brain in the Vertebrata.
The evidence at our disposal appears to me to indicate that the third
nerve belongs to the cranio-spinal series of segmental nerves, while
the optic and olfactory nerves appear to me equally clearly not to
belong to this series[104]. The mid-brain, as giving origin to the
third nerve, would appear not to have been part of the ganglion of the
præoral lobe.
[104] Marshall, in his valuable paper on the development of the
olfactory organ, takes a very different view of this subject. For
a discussion of this view I must refer the reader to the chapter
on the nervous system.
These considerations indicate with fair probability that the part of
the head containing the fore-brain is the equivalent of the præoral
lobe of many Invertebrate forms; and the primitive position of the
Vertebrate mouth on the ventral side of the head affords a distinct
support for this view. It must however be admitted that this part of
the head is not sharply separated in development from that behind;
and, though the fore-brain is usually differentiated very early as a
distinct lobe of the primitive nervous tube, yet that such
differentiation is hardly more marked than in the other parts of the
brain. The termination of the notochord immediately behind the
fore-brain is, however, an argument in favour of the morphological
distinctness of the latter structure.
The evidence at our disposal appears to indicate that the posterior
part of the head was not differentiated from the trunk in lower
Chordata; but that, as the Chordata rose in the scale of development,
more and more centralizing work became thrown on the anterior part of
the nervous cord, and _pari passu_ this part became differentiated
into the mid- and hind-brain. An analogy for such a differentiation is
supplied in the compound suboesophageal ganglion of many Arthropods;
and, as will be shewn in the chapter on the nervous system, there is
strong embryological evidence that the mid- and hind-brains had
primitively the same structure as the spinal cord. The head appears
however to have suffered in the course of its differentiation a great
concentration in its posterior part, which becomes progressively more
marked, even within the limits of the surviving Vertebrata. This
concentration is especially shewn in the structure of the vagus nerve,
which, as first pointed out by Gegenbaur, bears evidence of having
been originally composed of a great series of nerves, each supplying a
visceral cleft. Rudiments of the posterior nerves still remain as the
branches to the oesophagus and stomach[105].
[105] The lateral branch of the vagus nerve probably became
differentiated in connection with the lateral line, which seems
to have been first formed in the head, and subsequently to have
extended into the trunk (_vide_ section on Lateral Line).
The atrophy of the posterior visceral clefts seems to have taken place
simultaneously with the concentration of the neural part of the head;
but the former process did not proceed so rapidly as the latter, so
that the visceral region of the head is longer in the lower Vertebrata
than the neural region, and is dorsally overlapped by the anterior
part of the spinal cord and the anterior muscle-plates (_vide_ fig.
47).
On the above view the posterior part of the head must have been
originally composed of a series of somites like those of the trunk,
but in existing Vertebrata all trace of these, except in so far as
they are indicated by the visceral clefts, has vanished in the adult.
The cranial nerves however, especially in the embryo, still indicate
the number of anterior somites; and an embryonic segmentation of the
mesoblast has also been found in many lower forms in the region of the
head, giving rise to a series of cavities known as head-cavities,
enclosed by mesoblastic walls which afterwards break up into muscles.
These cavities correspond with the nerves, and it appears that there
is a præmandibular cavity corresponding with the third nerve (fig.
193, _1pp_) and a mandibular cavity (_2pp_) and a cavity in each of
the succeeding visceral arches. The fifth nerve, the seventh nerve,
the glossopharyngeal nerve, and the successive elements of the vagus
nerve correspond with the posterior head-cavities.
[FIG. 193. TRANSVERSE SECTION THROUGH THE FRONT PART OF THE HEAD OF
A YOUNG PRISTIURUS EMBRYO.
The section, owing to the cranial flexure, cuts both the fore- and
the hind-brain. It shews the præmandibular and mandibular
head-cavities _1pp_ and _2pp_, etc.
_fb._ fore-brain; _l._ lens of eye; _m._ mouth; _pt._ upper end of
mouth, forming pituitary involution; _1ao._ mandibular aortic arch;
_1pp._ and _2pp._ first and second head-cavities; _1vc._ first
visceral cleft; _V._ fifth nerve; _aun._ ganglion of auditory nerve;
_VII._ seventh nerve; _aa._ dorsal aorta; _acv._ anterior cardinal
vein; _ch._ notochord.]
The medullary canal. The general history of the medullary plate seems
to point to the conclusion that the central canal of the nervous
system has been formed by a groove having appeared in the ancestor of
the Chordata along the median dorsal line, which caused the sides of
the nervous plate, which was placed immediately below the skin, or may
perhaps at that stage not have been distinctly differentiated from the
skin, to be bent upwards; and that this groove subsequently became
converted into a canal. This view is not only supported by the actual
development of the central canal of the nervous system (the types of
Teleostei, Lepidosteus and Petromyzon being undoubtedly secondary),
but also (1) by the presence of cilia in the epithelium lining the
canal, probably inherited from cilia coating the external skin, and
(2) by the posterior roots arising from the extreme dorsal line (fig.
194), a position which can most easily be explained on the supposition
that the two sides of the plate, from which the nerves originally
proceeded have been folded up so as to meet each other in the median
dorsal line[106].
[106] _Vide_ for further details the chapter on the nervous
system.
The medullary plate, before becoming folded to form the medullary
groove, is (except in Amphibia) without any indication of being
composed of two halves. In both the embryo and adult the walls of the
tube have however a structure which points to their having arisen from
the coalescence of two lateral, and most probably at one time
independent, cords; and as already indicated this is the view I am
myself inclined to adopt; _vide_ pp. 303 and 304.
[FIG. 194. TRANSVERSE SECTION THROUGH THE TRUNK OF AN EMBRYO
SLIGHTLY OLDER THAN FIG. 28 E.
_nc._ neural canal; _pr._ posterior root of spinal nerve; _x._
subnotochordal rod; _ao._ aorta; _sc._ somatic mesoblast; _sp._
splanchnic mesoblast; _mp._ muscle-plate; _mp´._ portion of
muscle-plate converted into muscle; _Vv._ portion of the vertebral
plate which will give rise to the vertebral bodies; _al._ alimentary
tract.]
The origin and nature of the mouth. The most obvious point connected
with the development of the mouth is the fact that in all vertebrate
embryos it is placed ventrally, at some little distance from the front
end of the body. This feature is retained in the adult stage in
Elasmobranchii, the Myxinoids, and some Ganoids, but is lost in other
vertebrate forms. A mouth, situated as is the embryonic vertebrate
mouth, is very ill adapted for biting; and though it acquires in this
position a distinctly biting character in the Elasmobranchii, yet it
is almost certain that it had not such a character in the ancestral
Chordata, and that its terminal position in higher types indicates a
step in advance of the Elasmobranchii.
On the structure of the primitive mouth there appears to me to be some
interesting embryological evidence, to which attention has already
been called in the preceding chapters. In a large number of the larvæ
or embryos of the lower Vertebrates the mouth has a more or less
distinctly suctorial character, and is connected with suctorial organs
which may be placed either in front of or behind it. The more
important instances of this kind are (1) the Tadpoles of the Anura,
with their posteriorly placed suctorial disc, (2) Lepidosteus larva
(fig. 195) with its anteriorly placed suctorial disc, (3) the adhesive
papillæ of the larvæ of the Tunicata. To these may be added the
suctorial mouth of the Myxinoid fishes[107].
[107] The existing Myxinoid Fishes are no doubt degenerate types,
as was first clearly pointed out by Dohrn; but at the same time
(although Dohrn does not share this view) it appears to me almost
certain that they are the remnants of a large and very primitive
group, which have very likely been preserved owing to their
parasitic or semiparasitic habits; much in the same way as many
of the Insectivora have been preserved owing to their
subterranean habits. I am acquainted with no evidence,
embryological or otherwise, that they are degraded
gnathostomatous forms, and the group probably disappeared as a
whole from its incapacity to compete successfully with Vertebrata
in which true jaws had become developed.
All these considerations point to the conclusion that in the ancestral
Chordata the mouth had a more or less definitely suctorial
character[108], and was placed on the ventral surface immediately
behind the præoral lobe; and that this mouth has become in the higher
types gradually modified for biting purposes, and has been carried to
the front end of the head.
[108] I do not conceive that the existence of suctorial
structures necessarily implies parasitic habits. They might be
used for various purposes, especially by predaceous forms not
provided with jaws.
The mouth in Elasmobranchii and other Vertebrates is originally a wide
somewhat rhomboidal cavity (fig. 28 G); on the development of the
mandibular and its maxillary (pterygo-quadrate) process the opening of
the mouth becomes narrowed to a slit. The wide condition of the mouth
may not improbably be interpreted as a remnant of the suctorial state.
The fact that no more definite remnants of the suctorial mouth are
found in so primitive a group as the Elasmobranchii is probably to be
explained by the fact that the members of this group undergo an
abbreviated development within the egg.
While the embryological data appear to me to point to the existence of
a primitive suctorial mouth, very different conclusions have been put
forward by other embryologists, more especially by Dohrn, which are
sufficiently striking and suggestive to merit a further discussion.
As mentioned above, both Dohrn and Semper hold that the Vertebrata are
descended from Chætopod-like forms, in which the ventral surface has
become the dorsal. In consequence of this view Dohrn has arrived at
the following conclusions: (1) that primitively the alimentary canal
perforated the nervous system in the region of the original
oesophageal nerve-ring; (2) that there was therefore an original
dorsal mouth (the present ventral mouth of the Chætopoda); and (3)
that the present mouth was secondary and derived from two visceral
clefts which have ventrally coalesced.
[FIG. 195. VENTRAL VIEW OF THE HEAD OF A LEPIDOSTEUS EMBRYO SHORTLY
BEFORE HATCHING, TO SHEW THE LARGE SUCTORIAL DISC.
_m._ mouth; _op._ eye; _sd._ suctorial disc.]
A full discussion of these views[109] is not within the scope of this
work; but, while recognizing that there is much to be said in favour
of the interchange of the dorsal and ventral surfaces, I am still
inclined to hold that the difficulties involved in this view are so
great that it must, provisionally at least, be rejected; and that
there are therefore no reasons against supposing the present
vertebrate mouth to be the primitive mouth. There is no embryological
evidence in favour of the view adopted by Dohrn that the present mouth
was formed by the coalescence of two clefts.
[109] For a partial discussion of this subject I would refer the
reader to my _Monograph on Elasmobranch Fishes_, pp. 165-172.
If it is once admitted that the present mouth is the primitive mouth,
and is more or less nearly in its original situation, very strong
evidence will be required to shew that any structures originally
situated in front of it are the remnants of visceral clefts; and if it
should be proved that such remnants of visceral clefts were present,
the views so far arrived at in this section would, I think, have to be
to a large extent reconsidered.
The nasal pits have been supposed by Dohrn to be remnants of visceral
clefts, and this view has been maintained in a very able manner by
Marshall. The arguments of Marshall do not, however, appear to me to
have any great weight unless it is previously granted that there is an
antecedent probability in favour of the presence of a pair of
gill-clefts in the position of the nasal pits; and even then the
development of the nasal pits as epiblastic involutions, instead of
hypoblastic outgrowths, is a serious difficulty which has not in my
opinion been successfully met. A further argument of Marshall from the
supposed segmental nature of the olfactory nerve has already been
spoken of.
While most of the structures supposed to be remains of gill-clefts in
front of the mouth do not appear to me to be of this nature, there is
one organ which stands in a more doubtful category. This organ is the
so-called choroid gland. The similarity of this organ to the
pseudobranch of the mandibular or hyoid arch was pointed out to me by
Dohrn, and the suggestion was made by him that it is the remnant of a
præmandibular gill which has been retained owing to its functional
connection with the eye[110]. Admitting this explanation to be true
(which however is by no means certain) are we necessarily compelled to
hold that the choroid gland is the remnant of a gill-cleft originally
situated in front of the mouth? I believe not. It is easy to conceive
that there may originally have been a præmandibular cleft _behind_ the
suctorial mouth, but that this cleft gradually atrophied (for the same
reasons that the mandibular cleft shews a tendency to atrophy in
existing fishes, &c.), the rudiment of the gill (choroid gland) alone
remaining to mark its situation. After the disappearance of this cleft
the suctorial mouth may have become relatively shifted backwards. In
the meantime the branchial bars became developed, and as the mouth was
changed into a biting one, the bar (the mandibular arch) supporting
the then first cleft became gradually modified and converted into a
supporting apparatus for the mouth, and finally formed the skeleton of
the jaws. In the hyostylic Vertebrata the hyoid arch also became
modified in connection with the formation of the jaws.
[110] The probability of the choroid gland having the meaning
attributed to it by Dohrn is strengthened by the existence of a
præmandibular segment as evidenced by the presence of a
præmandibular head-cavity, the walls of which as shewn by
Marshall and myself give rise to the majority of the eye-muscles
and of a nerve (the third nerve, cf. Marshall) corresponding to
it; so that these parts together with the choroid gland may be
rudiments belonging to the same segment. On the other hand the
absence of the choroid gland in Ganoidei and Elasmobranchii,
where a mandibular pseudobranch is present, coupled with the
absence of a mandibular pseudobranch in Teleostei where alone a
choroid gland is present, renders the above view about the
choroid gland somewhat doubtful. A thorough investigation of the
ontogeny of the choroid gland might throw further light on this
interesting question, but I think it not impossible that the
choroid gland may be nothing else but the modified _mandibular_
pseudobranch, a view which fits in very well with the relations
of the vessels of the Elasmobranch mandibular pseudobranch to the
choroid. For the relations and structure of the choroid gland
_vide_ F. Müller, _Vergl. Anat. Myxinoiden_, Part III. p. 82.
It is possible that the fourth nerve and the superior oblique
muscle of the eye which it supplies may be the last remaining
remnants of a second præmandibular segment originally situated
between the segment of the third nerve and that of the fifth
nerve (mandibular segment).
The conclusions arrived at may be summed up as follows:
The relations which exist in all jaw-bearing Vertebrates between the
mandibular arch and the oral aperture are secondary, and arose _pari
passu_ with the evolution of the jaws[111].
[111] I do not mean to exclude the possibility of the mandibular
arch having supported a suctorial mouth before it became
converted into a pair of jaws.
[FIG. 196. THE HEADS OF ELASMOBRANCH EMBRYOS AT TWO STAGES VIEWED AS
TRANSPARENT OBJECTS.
A. Pristiurus embryo of the same stage as fig. 28 F. B. Somewhat
older Scyllium embryo.
_III._ third nerve; _V._ fifth nerve; _VII._ seventh nerve; _au.n._
auditory nerve; _gl._ glossopharyngeal nerve; _Vg._ vagus nerve;
_fb._ fore-brain; _pn._ pineal gland; _mb._ mid-brain; _hb._
hind-brain; _iv.v._ fourth ventricle; _cb._ cerebellum; _ol._
olfactory pit; _op._ eye; _au.V._ auditory vesicle; _m._ mesoblast
at base of brain; _ch._ notochord; _ht._ heart; _Vc._ visceral
clefts; _eg._ external gills; _pp._ sections of body cavity in the
head.]
The cranial flexure and the form of the head in vertebrate embryos.
All embryologists who have studied the embryos of the various
vertebrate groups have been struck with the remarkable similarity
which exists between them, more especially as concerns the form of the
head. This similarity is closest between the members of the Amniota,
but there is also a very marked resemblance between the Amniota and
the Elasmobranchii. The peculiarity in question, which is
characteristically shewn in fig. 196, consists in the cerebral
hemispheres and thalamencephalon being ventrally flexed to such an
extent that the mid-brain forms the termination of the long axis of
the body. At a later period in development the cerebral hemispheres
come to be placed at the front end of the head; but the original nick
or bend of the floor of the brain is never got rid of.
It is obvious that in dealing with the light thrown by embryology on
the ancestral form of the Chordata the significance of this peculiar
character of the head of many vertebrate embryos must be discussed. Is
the constancy of this character to be explained by supposing that at
one period vertebrate ancestors had a head with the same features as
the embryonic head of existing Vertebrata?
This is the most obvious explanation, but it does not at the same time
appear to me satisfactory. In the first place the mouth is so situated
at the time of the maximum cranial flexure that it could hardly have
been functional; so that it is almost impossible to believe that an
animal with a head such as that of these embryos can have existed.
Then again, this type of embryonic head is especially characteristic
of the Amniota, all of which are developed in the egg. It is not
generally so marked in the Ichthyopsida. In Amphibia, Teleostei,
Ganoidæ and Petromyzontidæ, the head never completely acquires the
peculiar characteristic form of the head of the Amniota, and all these
forms are hatched at a relatively much earlier phase of development,
so that they are leading a free existence at a stage when the embryos
of the Amniota are not yet hatched. The only Ichthyopsidan type with a
head like that of the Amniota is the Elasmobranchii, and the
Elasmobranchii are the only Ichthyopsida which undergo the major part
of their development within the egg.
These considerations appear to shew that the peculiar characters of
the embryonic head above alluded to are in some way connected with an
embryonic as opposed to a larval development; and for reasons which
are explained in the section on larval forms, it is probable that a
larval development is a more faithful record of ancestral history than
an embryonic development. The flexure at the base of the brain appears
however to be a typical vertebrate character, but this flexure never
led to a conformation of the head in the adult state similar to that
of the embryos of the Amniota. The form of the head in these embryos
is probably to be explained by supposing that some advantage is gained
by a relatively early development of the brain, which appears to be
its proximate cause; and since these embryos had not to lead a free
existence (for which such a form of the head would have been unsuited)
there was nothing to interfere with the action of natural selection in
bringing about this form of head during foetal life.
Postanal gut and neurenteric canal. One of the most remarkable
structures in the trunk is the postanal gut (fig. 197). Its structure
is fully dealt with in the chapter on the alimentary tract, but
attention may here be called to the light which it appears to throw on
the characters of the ancestor of the Chordata.
In face of the facts which are known with reference to the postanal
section of the alimentary tract, it can hardly be doubted that this
portion of the alimentary tract must have been at one time functional.
This seems to me to be shewn (1) by the constancy and persistence of
this obviously now functionless rudiment, (2) by its greater
development in the lower than in the higher forms, (3) by its relation
to the formation of the notochord and subnotochordal rod.
[FIG. 197. LONGITUDINAL SECTION THROUGH AN ADVANCED EMBRYO OF
BOMBINATOR. (After Götte.)
_m._ mouth; _an._ anus; _l._ liver; _ne._ neurenteric canal; _mc._
medullary canal; _ch._ notochord; _pn._ pineal gland.]
If the above position be admitted, it is not permissible to shirk the
conclusions which seem necessarily to follow, however great the
difficulties may be which are involved in their acceptance. These
conclusions have in part already been dealt with by Dohrn in his
suggestive tract (No. 250). In the first place the alimentary canal
must primitively have been continued to the end of the tail; and if
so, it is hardly credible that the existing anus can have been the
original one. Although, therefore, it is far from easy, on the
physiological principles involved in the Darwinian theory, to
understand the formation of a new anus[112]; it is nevertheless
necessary to believe that the present vertebrate anus is a formation
acquired within the group of the Chordata, and not inherited from some
older group. This involves a series of further consequences. The
opening of the urinogenital ducts into the cloaca must also be
secondary, and it is probable that the segmental tubes were
primitively continued along the whole postanal region of the
vertebrate tail, opening into the body cavity which embryology proves
to have been originally present there. They are in fact continued in
many existing forms for some distance behind the present anus. If the
present anus is secondary, there must have been a primitive anus,
which was probably situated behind the postanal vesicle; and therefore
in the region of the neurenteric canal. The neurenteric canal is,
however, the remnant of the blastopore (_vide_ p. 277). It follows,
therefore, _that the vertebrate blastopore is probably almost, if not
exactly identical in position with the primitive anus_. This
consideration may assist in explaining the remarkable phenomenon of
the existence of the neurenteric canal. The attempt has already been
made to shew that the central canal of the nervous system is really a
groove converted into a tube and lined by the external epidermis. This
tube (as may be concluded from embryological considerations) was
probably at first open posteriorly, and no doubt terminated at the
primitive anus. On the closure of the primitive anal opening, the
terminal portions of the postanal gut and the neural tube, may
conceivably have been so placed that both of them opened into a common
cavity, which previously had communication with the exterior by the
anus. Such an arrangement would necessarily result in the formation of
a neurenteric canal. It seems not impossible that a dilated vesicle,
often present at the end of the postanal gut (_vide_ fig. 28*, p. 58),
may have been the common cavity into which both neural and alimentary
tubes opened[113]. Till further light is thrown by fresh discoveries
upon the primitive condition of the posterior continuation of the
vertebrate alimentary tract, it is perhaps fruitless to attempt to
work out more in detail the above speculation.
[112] Dohrn (No. 250, p. 25) gives an explanation of the origin
of the new anus which does not appear to me quite satisfactory.
[113] As pointed out in Vol. II. p. 255, there is a striking
similarity between the history of the neurenteric canal in
Vertebrates, and the history of the blastopore and ventral groove
as described by Kowalevsky in the larva of Chiton. Mr A. Sedgwick
has pointed out to me that the ciliated ventral groove in
Protoneomenia, which contains the anus, is probably the homologue
of the groove found in the larva of Chiton, and not, as usually
supposed, simply the foot. Were this groove to be converted into
a canal, on the sides of which were placed the nervous cords,
there would be formed a precisely similar neurenteric canal to
that in Vertebrata, though I do not mean to suggest that there is
any homology between the two (_vide_ Hubrecht, _Zool. Anzeiger_,
1880, p. 589).
Body cavity and mesoblastic somites. The Chordata, or at least the
most primitive existing members of the group, are characterized by the
fact that the body cavity arises as a pair of outgrowths of the
archenteric cavity. This feature[114] in the development is a nearly
certain indication that the Chordata are a very primitive stock. The
most remarkable point with reference to the development of the two
outgrowths is, however, the fact that the dorsal part of each
outgrowth becomes separated from the ventral. Its walls become
_segmented_ and form the mesoblastic somites, which eventually, on the
obliteration of their cavity, give rise to the muscle-plates and to
the tissue surrounding the notochord. It is not easy to understand the
full significance of the processes concerned in the formation of the
mesoblastic somites (_vide_ p. 296). The mesoblastic somites have no
doubt a striking resemblance to the mesoblastic somites of the
Chætopods, and most probably the segmentation of the mesoblast in the
two groups is a phenomenon of the same nature; but the difference in
origin between the two types of mesoblastic somites is so striking,
and the development of the muscular system from them is so dissimilar
in the two groups, as to render a direct descent of the Chordata from
the Chætopoda very improbable. The ventral parts of the original
outgrowth give rise to the permanent body cavity, which appears
originally to have been divided into two parts by a dorsal and a
ventral mesentery.
[114] _Vide_ the chapter on the Germinal Layers.
The notochord. The most characteristic organ of the Chordata is
without doubt the notochord. The ontogenetic development of this organ
probably indicates that it arose as a differentiation of the dorsal
wall of the archenteron; at the same time it is not perhaps safe to
lay too much stress upon its mode of development. Embryological and
anatomical evidence demonstrate, however, in the clearest manner that
the early Chordata were provided with this organ as their sole axial
skeleton; and no invertebrate group can fairly be regarded as
genetically related to the Chordata till it can be shewn to possess
some organ either derived from a notochord, or capable of having
become developed into a notochord. No such organ has as yet been
recognized in any invertebrate group[115].
[115] In the Chætopods various organs have been interpreted as
rudiments of a notochord, but none of these interpretations will
bear examination.
Gill-clefts. The gill-clefts, which are essentially pouches of the
throat opening externally, constitute extremely characteristic organs
of the Chordata, and have always been taken into consideration in any
comparison between the Chordata and the Invertebrata.
Amongst the Invertebrata organs of undoubtedly the same nature are, so
far as I know, only found in Balanoglossus, where they were discovered
by Kowalevsky. The resemblance in this case is very striking; but
although it is quite possible that the gill-clefts in Balanoglossus
are genetically connected with those of the Chordata, yet the
organization of Balanoglossus is as a whole so different from that of
the Chordata that no comparison can be instituted between the two
groups in the present state of our knowledge.
Other organs of the Invertebrata have some resemblance to the
gill-clefts. The lateral pits of the Nemertines, which appear to grow
out as a pair of oesophageal diverticula, which are eventually placed
in communication with the exterior by a pair of ciliated canals
(_vide_ Vol. II. pp. 200 and 202), are such organs.
Semper (No. 256) has made the interesting discovery that in the
budding of Nais and Chætogaster two lateral masses of cells, in each
of which a lumen may be formed, unite with the oral invagination and
primitive alimentary canal to form the permanent cephalic gut. The
lateral masses of cells are regarded by him as branchial passages
homologous in some way with those in the Chordata. The somewhat scanty
observations on this subject which he has recorded do not appear to me
to lend much support to this interpretation.
It is probable that the part of the alimentary tract in which
gill-clefts are present was originally a simple unperforated tube
provided with highly vascular walls; and that respiration was carried
on in it by the alternate introduction and expulsion of sea water. A
more or less similar mode of respiration has been recently shewn by
Eisig[116] to take place in the fore part of the alimentary tract of
many Chætopods. This part of the alimentary tract was probably
provided with paired cæcal pouches with their blind ends in contiguity
with the skin.
[116] "Ueb. d. Vorkommen eines schwimmblasenähnlichen Organs bei
Anneliden." _Mittheil. a. d. zool. Station zu Neapel_, Vol. II.
1881.
Perforations placing these pouches in communication with the exterior
must be supposed to have been formed; and the existence of openings
into the alimentary tract at the end of the tentacles of many Actiniæ
and of the hepatic diverticula of some nudibranchiate Molluscs (Eolis,
&c.[117]) shews that such perforations may easily be made. On the
formation of such perforations the water taken in at the mouth would
pass out by them; and the respiration would be localized in the walls
of the pouches leading to them, and thus the typical mode of
respiration of the Chordata would be established.
[117] The openings of the hepatic diverticula through the sacks
lined with thread cells are described by Hancock and Embleton,
_Ann. and Mag. of Nat. History_, Vol. XV. 1845, p. 82. Von
Jhering has also recently described these openings (_Zool.
Anzeiger_, No. 23) and apparently attributes their discovery to
himself.
Phylogeny of the Chordata. It may be convenient to shew in a definite
way the bearing of the above speculations on the phylogeny of the
Chordata. For this purpose, I have drawn up the subjoined table, which
exhibits what I believe to be the relationships of the existing groups
of the Chordata. Such a table cannot of course be constructed from
embryological data alone, and it does not fall within the scope of
this work to defend its parts in detail.
MAMMALIA SAUROPSIDA
| |
-----------------------------
|
PROTO-AMNIOTA AMPHIBIA
| |
----------------------------------
|
TELEOSTEI PROTO-PENTADACTYLOIDEI
| |
GANOIDEI | ---- DIPNOI
| |
--------------------|
PROTO-GANOIDEI
|
|-- HOLOCEPHALI
|------- ELASMOBRANCHII
|
PROTO-GNATHOSTOMATA
|
--------------------------|
| |
_Cyclostomata_ PROTO-VERTEBRATA
|
--------------------------|-------------------------
| |
_Cephalochorda_ PROTOCHORDATA _Urochorda_
In the above table the names printed in large capitals are
hypothetical groups. The other groups are all in existence at the
present day, but those printed in Italics are probably degenerate.
The ancestral forms of the Chordata, which may be called the
Protochordata, must be supposed to have had (1) a notochord as their
sole axial skeleton, (2) a ventral mouth, surrounded by suctorial
structures, and (3) very numerous gill-slits. Two degenerate offshoots
of this stock still persist in Amphioxus (Cephalochorda), and the
Ascidians (Urochorda).
The direct descendants of the ancestral Chordata, were probably a
group which may be called the Protovertebrata, of which there is no
persisting representative. In this group, imperfect neural arches were
probably present; and a ventral suctorial mouth without a mandible and
maxillæ was still persistent. The branchial clefts had, however,
become reduced in number, and were provided with gill-folds; and a
secondary head (_vide_ p. 313), with brain and organs of sense like
those of the higher Vertebrata, had become formed.
The Cyclostomata are probably a degenerate offshoot of this group.
With the development of the branchial bars, and the conversion of the
mandibular bar into the skeleton of the jaws, we come to the
Proto-gnathostomata. The nearest living representatives of this group
are the Elasmobranchii, which still retain in the adult state the
ventrally placed mouth. Owing to the development of food-yolk in the
Elasmobranch ovum the early stages of development are to some extent
abbreviated, and almost all trace of a stage with a suctorial mouth
has become lost.
We next come to an hypothetical group which we may call the
Proto-ganoidei. Bridge, in his memoir on Polyodon[118], which contains
some very interesting speculations on the affinities of the Ganoids,
has called this group the Pneumatocoela, from the fact that we find
for the first time a full development of the air-bladder, though it is
possible that a rudiment of this organ, in the form of a pouch opening
on the dorsal side of the stomachic extremity of the oesophagus, was
present in the earlier type.
[118] _Phil. Trans._ 1878. Part II.
Existing Ganoids are descendants of the Proto-ganoidei. Some of them
at all events retain in larval life the suctorial mouth of the
Protovertebrata; and the mode of formation of their germinal layers,
resembling as it does that in the Lamprey and the Amphibia, probably
indicates that they are not descended from forms with a large
food-yolk like that of Elasmobranchii, and that the latter group is
therefore a lateral offshoot from the main line of descent.
Of the two groups into which the Ganoidei may be divided it is clear
that certain members of the one (Telcostoidei), viz. Lepidosteus and
Amia, shew approximations to the Teleostei, which no doubt originated
from the Ganoids; while the other (Selachoidei or Sturiones) is more
nearly related to the Dipnoi. Polypterus has also marked affinities in
this direction, _e.g._ the external gills of the larva (_vide_ p.
118).
The Teleostei, which have in common a meroblastic segmentation, had
probably a Ganoid ancestor, the ova of which were provided with a
large amount of food-yolk. In most existing Teleostei, the ovum has
become again reduced in size, but the meroblastic segmentation has
been preserved. It is quite possible that Amia may also be a
descendant of the Ganoid ancestor of the Teleostei; but Lepidosteus,
as shewn by its complete segmentation, is clearly not so.
The Dipnoi as well as all the higher Vertebrata are descendants of the
Proto-ganoidei.
The character of the limbs of higher Vertebrata indicates that there
was an ancestral group, which may be called the Proto-pentadactyloidei,
in which the pentadactyle limb became established; and that to this
group the common ancestor of the Amphibia and Amniota belonged.
It is possible that the Plesiosauri and Ichthyosauri of Mesozoic times
may have been more nearly related to this group than either to the
Amniota or the Amphibia. The Proto-pentadactyloidei were probably much
more closely related to the Amphibia than to the Amniota. They
certainly must have been capable of living in water as well as on
land, and had of course persistent branchial clefts. It is also fairly
certain that they were not provided with large-yolked ova, otherwise
the mode of formation of the layers in Amphibia could not be easily
explained.
The Mammalia and Sauropsida are probably independent offshoots from a
common stem which may be called the Protoamniota.
BIBLIOGRAPHY.
(249) F. M. Balfour. _A Monograph on the development of Elasmobranch
Fishes_. London, 1878.
(250) A. Dohrn. _Der Ursprung d. Wirbelthiere und d. Princip. d.
Functionswechsel._ Leipzig, 1875.
(251) E. Haeckel. _Schöpfungsgeschichte._ Leipzig. _Vide_ also
Translation. _The History of Creation._ King and Co., London, 1876.
(252) E. Haeckel. _Anthropogenie._ Leipzig. _Vide_ also Translation.
_Anthropogeny._ Kegan Paul and Co., London, 1878.
(253) A. Kowalevsky. "Entwicklungsgeschichte d. Amphioxus
lanceolatus." _Mém. Acad. d. Scien. St Pétersbourg_, Ser. VII. Tom.
XI. 1867, and _Archiv f. mikr. Anat._, Vol. XIII. 1877.
(254) A. Kowalevsky. "Weitere Stud. üb. d. Entwick. d. einfachen
Ascidien." _Archiv f. mikr. Anat._, Vol. VII. 1871.
(255) C. Semper. "Die Stammesverwandschaft d. Wirbelthiere u.
Wirbellosen." _Arbeit. a. d. zool.-zoot. Instit. Würzburg_, Vol. II.
1875.
(256) C. Semper. "Die Verwandschaftbeziehungen d. gegliederten
Thiere." _Arbeit. a. d. zool.-zoot. Instit. Würzburg_, Vol. III.
1876-1877.
CHAPTER XIII.
GENERAL CONCLUSIONS.
I. THE MODE OF ORIGIN AND HOMOLOGIES OF THE GERMINAL LAYERS.
It has already been shewn in the earlier chapters of the work that
during the first phases of development the history of all the Metazoa
is the same. They all originate from the coalescence of two cells, the
ovum and spermatozoon. The coalesced product of these cells--the
fertilized ovum--then undergoes a process known as the segmentation,
in the course of which it becomes divided in typical cases into a
number of uniform cells. An attempt was made from the point of view of
evolution to explain these processes. The ovum and spermatozoon were
regarded as representing phylogenetically two physiologically
differentiated forms of a Protozoon; their coalescence was equivalent
to conjugation: the subsequent segmentation of the fertilized ovum was
the multiplication by division of the organism resulting from the
conjugation; the resulting organisms, remaining, however, united to
form a fresh organism in a higher state of aggregation.
In the systematic section of this work the embryological history of
the Metazoa has been treated. The present chapter contains a review of
the cardinal features of the various histories, together with an
attempt to determine how far there are any points common to the whole
of these histories; and the phylogenetic interpretation to be given to
such points.
Some years ago it appeared probable that a definite answer would be
given to the questions which must necessarily be raised in the present
chapter; but the results of the extended investigations made during
the last few years have shewn that these expectations were premature,
and in spite of the numerous recent valuable contributions to this
branch of Embryology, amongst which special attention may be called to
those of Kowalevsky (No. 277), Lankester (Nos. 278 and 279), and
Haeckel (No. 266), there are few embryologists who would venture to
assert that any answers which can be given are more than tentative
gropings towards the truth.
In the following pages I aim more at summarising the facts, and
critically examining the different theories which can be held, than at
dogmatically supporting any definite views of my own.
In all the Metazoa, the development of which has been investigated,
the first process of differentiation, which follows upon the
segmentation, consists in the cells of the organism becoming divided
into two groups or layers, known respectively as epiblast and
hypoblast.
These two layers were first discovered in the young embryos of
vertebrated animals by Pander and Von Baer, and have been since known
as the germinal layers, though their cellular nature was not at first
recognised. They were shewn, together with a third layer, or
mesoblast, which subsequently appears between them, to bear throughout
the Vertebrata constant relations to the organs which became developed
from them. A very great step was subsequently made by Remak (No. 287),
who successfully worked out the problem of vertebrate embryology on
the cellular theory.
Rathke in his memoir on the development of Astacus (No. 286) attempted
at a very early period to extend the doctrine of the derivation of the
organs from the germinal layers to the Invertebrata. In 1859 Huxley
made an important step towards the explanation of the nature of these
layers by comparing them with the ectoderm and endoderm of the
Hydrozoa; while the brilliant researches of Kowalevsky on the
development of a great variety of invertebrate forms formed the
starting point of the current views on this subject.
The differentiation of the epiblast and hypoblast may commence during
the later phases of the segmentation, but is generally not completed
till after its termination. Not only do the cells of the blastoderm
become differentiated into two layers, but these two layers, in the
case of a very large number of ova with but little food-yolk,
constitute a double-walled sack--the gastrula (fig. 198)--the
characters of which are too well known to require further description.
Following the lines of phylogenetic speculation above indicated, it
may be concluded that the two-layered condition of the organism
represents in a general way the passage from the protozoon to the
metazoon condition. It is probable that we may safely go further, and
assert that the gastrula reproduces, with more or less fidelity, a
stage in the evolution of the Metazoa, permanent in the simpler
Hydrozoa, during which the organism was provided with (1) a fully
developed digestive cavity (fig. 198 _b_) lined by the hypoblast with
digestive and assimilative functions, (2) an oral opening (_a_), and
(3) a superficial epiblast (_d_). These generalisations, which are now
widely accepted, are no doubt very valuable, but they leave unanswered
the following important questions:
(1) By what steps did the compound Protozoon become differentiated
into a Metazoon?
(2) Are there any grounds for thinking that there is more than one
line along which the Metazoa have become independently evolved
from the Protozoa?
(3) To what extent is there a complete homology between the two
primary germinal layers throughout the Metazoa?
[FIG. 198. DIAGRAM OF A GASTRULA. (From Gegenbaur.)
_a._ mouth; _b._ archenteron; _c._ hypoblast; _d._ epiblast.]
Ontogenetically there is a great variety of processes by which the
passage from the segmented ovum to the two-layered or diploblastic
condition is arrived at.
These processes may be grouped under the following heads:
1. Invagination. Under this term a considerable number of closely
connected processes are included. When the segmentation results in the
formation of a blastosphere, one half of the blastosphere may be
pushed in towards the opposite half, and a gastrula be thus produced
(fig. 199, A and B). This process is known as embolic invagination.
Another process, known as epibolic invagination, consists in epiblast
cells growing round and enclosing the hypoblast (fig. 200). This
process replaces the former process when the hypoblast cells are so
bulky from being distended by food-yolk that their invagination is
mechanically impossible.
[FIG. 199. TWO STAGES IN THE DEVELOPMENT OF HOLOTHURIA TUBULOSA,
VIEWED IN OPTICAL SECTION. (After Selenka.)
A. Stage at the close of segmentation. B. Gastrula stage.
_mr._ micropyle; _fl._ chorion; _s.c._ segmentation cavity; _bl._
blastoderm; _ep._ epiblast; _hy._ hypoblast; _ms._ amoeboid cells
derived from hypoblast; _a.e._ archenteron.]
There are various peculiar modifications of invagination which cannot
be dealt with in detail.
Invagination in one form or other occurs in some or all the members of
the following groups:
[FIG. 200. TRANSVERSE SECTION THROUGH THE OVUM OF EUAXES DURING AN
EARLY STAGE OF DEVELOPMENT, TO SHEW THE NATURE OF EPIBOLIC
INVAGINATION. (After Kowalevsky.)
_ep._ epiblast; _ms._ mesoblastic band; _hy._ hypoblast.]
The Dicyemidæ, Calcispongiæ (after the amphiblastula stage) and
Silicispongiæ, Coelenterata, Turbellaria, Nemertea, Rotifera,
Mollusca, Polyzoa, Brachiopoda, Chætopoda, Discophora, Gephyrea,
Chætognatha, Nematelminthes, Crustacea, Echinodermata, and Chordata.
The gastrula of the Crustacea is peculiar, as is also that of many of
the Chordata (Reptilia, Aves, Mammalia), but there is every reason to
suppose that the gastrulæ of these groups are simply modifications of
the normal type.
2. Delamination. Three types of delamination may be distinguished:
_a._ Delamination where the cells of a solid morula become divided
into a superficial epiblast, and a central solid mass in which the
digestive cavity is subsequently hollowed out (fig. 201).
[FIG. 201. TWO STAGES IN THE DEVELOPMENT OF STEPHANOMIA PICTUM, TO
ILLUSTRATE THE FORMATION OF THE LAYERS BY DELAMINATION. (After
Metschnikoff.)
A. Stage after the delamination; _ep._ epiblastic invagination to
form pneumatocyst.
B. Later stage after the formation of the gastric cavity in the
solid hypoblast. _po._ polypite; _t._ tentacle; _pp._ pneumatocyst;
_ep._ epiblast of pneumatocyst; _hy._ hypoblast surrounding
pneumatocyst.]
_b._ Delamination where the segmented ovum has the form of a
blastosphere, the cells of which give rise by budding to scattered
cells in the interior of the vesicle, which, though they may at
first form a solid mass, finally arrange themselves in the form of a
definite layer around a central digestive cavity (fig. 202).
_c._ Delamination where the segmented ovum has the form of a
blastosphere in the cells of which the protoplasm is differentiated
into an inner and an outer part. By a subsequent process the inner
parts of the cells become separated from the outer, and the walls of
the blastosphere are so divided into two distinct layers (fig. 205).
Although the third of these processes is usually regarded as the type
of delamination, it does not, so far as I know, occur in nature, but
is most nearly approached in Geryonia (fig. 203).
The first type of delamination is found in the Ceratospongiæ, some
Silicispongiæ (?), and in many Hydrozoa and Actinozoa, and in Nemertea
and Nematelminthes (_Gordioidea?_). The second type occurs in many
Porifera [_Calcispongiæ_ (_Ascetta_), _Myxospongiæ_], and in some
Coelenterata, and Brachiopoda (_Thecidium_).
[FIG. 202. THREE LARVAL STAGES OF EUCOPE POLYSTYLA. (After
Kowalevsky.)
A. Blastosphere stage with hypoblast spheres becoming budded off
into central cavity. B. Planula stage with solid hypoblast. C.
Planula stage with a gastric cavity. _ep._ epiblast; _hy._
hypoblast; _al._ gastric cavity.]
Delamination and invagination are undoubtedly the two most frequent
modes in which the layers are differentiated, but there are in
addition several others. In the first place the whole of the Tracheata
(with the apparent exception of the Scorpion) develop, so far as is
known, on a plan peculiar to them, which approaches delamination. This
consists in the appearance of a superficial layer of cells enclosing a
central yolk mass, which corresponds to the hypoblast (figs. 204 and
214). This mode of development might be classed under delamination,
were it not for the fact that the early development of many Crustacea
is almost the same, but is subsequently followed by an invagination
(fig. 208), which apparently corresponds to the normal invagination of
other types. There are strong grounds for thinking that the tracheate
type of formation of the epiblast and hypoblast is a _secondary
modification of an invaginate type_ (_vide_ Vol. II. p. 457).
[FIG. 203. DIAGRAMMATIC FIGURES SHEWING THE DELAMINATION OF THE
EMBRYO OF GERYONIA. (After Fol.)
A. Stage at the commencement of the delamination; the dotted lines
_x_ shew the course of the next planes of division. B. Stage at the
close of the delamination. _cs._ segmentation cavity; _a._
endoplasm; _b._ ectoplasm; _ep._ epiblast; _hy._ hypoblast.]
[FIG. 204. SEGMENTATION AND FORMATION OF THE BLASTODERM IN CHELIFER.
(After Metschnikoff.)
In A the ovum is divided into a number of separate segments. In B a
number of small cells have appeared (_bl_) which form a blastoderm
enveloping the large yolk-spheres. In C the blastoderm has become
divided into two layers.]
The type of some Turbellaria (_Stylochopsis ponticus_) and that of
Nephelis amongst the Discophora is not capable of being reduced to the
invaginate type.
The development of almost all the parasitic groups, _i.e._ the
Trematoda, the Cestoda, the Acanthocephala, and the Linguatulida, and
also of the Tardigrada, Pycnogonida, and other minor groups, is too
imperfectly known to be classed with either the delaminate or
invaginate types.
It will, I think, be conceded on all sides that, if any of the
ontogenetic processes by which a gastrula form is reached are
repetitions of the process by which a simple two-layered gastrula was
actually evolved from a compound Protozoon, these processes are most
probably of the nature either of invagination or of delamination.
The much disputed questions which have been raised about the gastrula
and planula theories, originally put forward by Haeckel and Lankester,
resolve themselves then into the simple question, whether any, and if
so which, of the ontogenetic processes by which the gastrula is formed
are repetitions of the phylogenetic origin of the gastrula.
It is very difficult to bring forward arguments of a conclusive kind
in favour of either of these processes. The fact that delaminate and
invaginate gastrulæ are in several instances found coexisting in the
same group renders it certain that there are not two independent phyla
of the Metazoa, derived respectively from an invaginate and a
delaminate gastrula[119].
[119] It is not difficult to picture a possible derivation of
delamination from invagination; while a comparison of the
formation of the inner layers (mesoblast and hypoblast) in
Ascetta (amongst the Sponges), and in the Echinodermata, shews a
very simple way in which it is possible to conceive of a passage
of delamination into invagination. In Ascetta the cells, which
give rise to the mesoblast and hypoblast, are budded off from the
inner wall of the blastosphere, especially at one point; while in
Echinodermata (fig. 199) there is a small invaginated sack which
gives rise to the hypoblast, while from the walls of this sack
amoeboid cells are budded off which give rise to a large part of
the mesoblast. If we suppose the hypoblast cells budded off at
one point in Ascetta gradually to form an invaginated sack, while
the mesoblast cells continued to be budded off as before, we
should pass from the delaminate type of Ascetta to the invaginate
type of an Echinoderm.
The four most important cases in which the two processes coexist are
the Porifera, the Coelenterata, the Nemertea, and the Brachiopoda. In
the cases of the Porifera and Coelenterata, there do not appear to me
to be any means of deciding which of these processes is derived from
the other; but in the Nemertea and the Brachiopoda the case is
different. In all the types of Nemertea in which the development is
relatively not abbreviated there is an invaginate gastrula, while in
the types with a greatly abbreviated development there is a delaminate
gastrula. It would seem to follow from this that a delaminate gastrula
has here been a secondary result of an abbreviation in the
development. In the Brachiopoda, again, the majority of types develop
by a process of invagination, while Thecidium appears to develop by
delamination; here also the delaminate type would appear to be
secondarily derived from the invaginate.
If these considerations are justified, delamination must be in some
instances secondarily derived from invagination; and this fact is so
far an argument in favour of the more primitive nature of
invagination; though it by no means follows that in the invaginate
process the steps by which the Metazoa were derived from the Protozoa
are preserved.
It does not, therefore, seem possible to decide conclusively in favour
of either of these processes by a comparison of the cases where they
occur in the same groups.
The relative frequency of the two processes supplies us with another
possible means for deciding between them; and there is no doubt that
here again the scale inclines towards invagination. It must, however,
be borne in mind that the frequency of the process of invagination
admits of another possible explanation. There is a continual tendency
for the processes of development to be abbreviated and simplified, and
it is quite possible that the frequent occurrence of invagination is
due to the fact of its being, in most cases, the simplest means by
which the two-layered condition can be reached. But this argument can
have but little weight until it can be shewn in each case that
invagination is a simpler process than delamination; and it is
rendered improbable by the cases already mentioned in which
delamination has been secondarily derived from invagination.
If it were the case that the blastopore had _in all types_ the same
relation to the adult mouth, there would be strong grounds for
regarding the invaginate gastrula as an ancestral form; but the fact
that this is by no means so is an argument of great weight in favour
of some other explanation of the frequency of invagination.
The force of this consideration can best be displayed by a short
summary of the fate of the blastopore in different forms.
The fate of the blastopore is so variable that it is difficult even to
classify the cases which have been described.
(1) It becomes the permanent mouth in the following forms[120]:
_Coelenterata._--Pelagia, Cereanthus.
_Turbellaria._--Leptoplana (?), Thysanozoon.
_Nemertea._--Pilidium, larvæ of the type of Desor.
_Mollusca._--In numerous examples of most Molluscan groups, except
the Cephalopoda.
_Chætopoda._--Most Oligochæta, and probably many Polychæta.
_Gephyrea._--Phascolosoma, Phoronis.
_Nematelminthes._--Cucullanus.
(2) It closes in the position where the mouth is subsequently
formed.
_Coelenterata._--Ctenophora (?).
_Mollusca._--In numerous examples of most Molluscan groups, except
the Cephalopoda.
_Crustacea._--Cirripedia (?), some Cladocera (Moina) (?).
(3) It becomes the permanent anus.
_Mollusca._--Paludina.
_Chætopoda._--Serpula and some other types.
_Echinodermata._--Almost universally, except amongst the Crinoidea.
(4) It closes in the position where the anus is subsequently formed.
_Echinodermata._--Crinoidea.
(5) It closes in a position which does not correspond or is not
known to correspond[121] either with the future mouth or
anus.--_Porifera_--Sycandra. _Coelenterata_--Chrysaora*,
Aurelia*. _Nemertea*_--Some larvæ which develop without a
metamorphosis. _Rotifera*. Mollusca_--Cephalopoda. _Polyzoa*._
_Brachiopoda_--Argiope, Terebratula, Terebratulina.
_Chætopoda_--Euaxes. _Discophora_--Clepsine.
_Gephyrea_--Bonellia*. _Chætognatha. Crustacea_--Decapoda.
_Chordata._
[120] The above list is somewhat tentative; and future
investigations will probably shew that many of the statements at
present current about the position of the blastopore are
inaccurate.
[121] The forms in which the position of the blastopore in
relation to the mouth or anus is not known are marked with an
asterisk.
The forms which have been classed together under the last heading vary
considerably in the character of the blastopore. In some cases the
fact of its not coinciding either with the mouth or anus appears to be
due simply to the presence of a large amount of food-yolk. The cases
of the Cephalopoda, of Euaxes, and perhaps of Clepsine and Bonellia,
are to be explained in this way: in the case of all these forms,
except Bonellia, the blastopore has the form of an elongated slit
along the ventral surface. This type of blastopore is characteristic
of the Mollusca generally, of the Polyzoa, of the Nematelminthes, and
very possibly of the Chætopoda and Discophora. In the Chætognatha
(fig. 209 B) the blastopore is situated, so far as can be determined,
behind the future anus. In many Decapoda the blastopore is placed
behind, but not far from, the anus. In the Chordata it is also placed
posteriorly to the anus, and, remarkably enough, remains, in a large
number of forms, for some time in connection with the neural tube by a
neurenteric canal.
The great variations in the character of the gastrula, indicated in
the above summary, go far to shew that if the gastrulæ, as we find
them in most types, have any ancestral characters, these characters
can only be of the most general kind. This may best be shewn by the
consideration of a few striking instances. The blastopore in Mollusca
has an elongated slit-like form, extending along the ventral surface
from the mouth to the anus. In Echinodermata it is a narrow pore,
remaining as the anus. In most Chætopoda it is a pore remaining as the
mouth, but in some as the anus. In Chordata it is a posteriorly-placed
pore, opening into both the archenteron and the neural canal.
It is clearly out of the question to explain all these differences as
having connection with the characters of ancestral forms. Many of them
can only be accounted for as secondary adaptations for the convenience
of development.
The epibolic gastrula of Mammalia (_vide_ pp. 215 and 291) is a still
more striking case of a secondary embryonic process, and is not
directly derived from the gastrula of the lower Chordata. It probably
originated in connection with the loss of food-yolk which took place
on the establishment of a placental nutrition for the foetus. The
epibolic gastrula of the Scorpion, of Isopods, and of other
Arthropoda, seems also to be a derived gastrula. These instances of
secondary gastrulæ are very probably by no means isolated, and should
serve as a warning against laying too much stress upon the frequency
of the occurrence of invagination. The great influence of the
food-yolk upon the early development might be illustrated by numerous
examples, especially amongst the Chordata (_vide_ Chapter XI.).
If the descendants of a form with a large amount of food-yolk in its
ova were to produce ova with but little food-yolk, the type of
formation of the germinal layers which would thereby result would be
by no means the same as that of the ancestors of the forms with much
food-yolk, but would probably be something very different, as in the
case of Mammalia. Yet amongst the countless generations of ancestors
of most existing forms, such oscillations in the amount of the
food-yolk must have occurred in a large number of instances.
The whole of the above considerations point towards the view that the
formation of the hypoblast by invagination, as it occurs in most forms
at the present day, can have in many instances no special phylogenetic
significance, and that the argument from frequency, in favour of
invagination as opposed to delamination, is not of prime importance.
A third possible method of deciding between delamination and
invagination is to be found in the consideration as to which of these
processes occurs in the most primitive forms. If there were any
agreement amongst primitive forms as to the type of their development
this argument might have some weight. On the whole, delamination is,
no doubt, characteristic of many primitive types, but the not
infrequent occurrence of invagination in both the Coelenterata and the
Porifera--the two groups which would on all hands be admitted to be
amongst the most primitive--deprives this argument of much of the
value it might otherwise have.
To sum up--considering the almost indisputable fact that both the
processes above dealt with have in many instances had a purely
secondary origin, no valid arguments can be produced to shew that
either of them reproduces the mode of passage between the Protozoa and
the ancestral two-layered Metazoa. These conclusions do not, however,
throw any doubt upon the fact that the gastrula, however evolved, was
a primitive form of the Metazoa; since this conclusion is founded upon
the actual existence of adult gastrula forms independently of their
occurrence in development.
[FIG. 205. DIAGRAM SHEWING THE FORMATION OF A GASTRULA BY
DELAMINATION. (From Lankester.)
Fig. 1, ovum; fig. 2, stage in segmentation; fig. 3, commencement of
delamination after the appearance of a central cavity; fig. 4,
delamination completed, mouth forming at _M._ In figs. 1, 2, and 3,
_Ec._ is ectoplasm, and _En._ is endoplasm. In fig. 4, _Ec._ is
epiblast, and _En._ hypoblast. _E._ and _F._ food particles.]
Though embryology does not at present furnish us with a definite
answer to the question how the Metazoa became developed from the
Protozoa, it is nevertheless worth while reviewing some of the
processes by which this can be conceived to have occurred.
On purely _à priori_ grounds there is in my opinion more to be said
for invagination than for any other view.
On this view we may suppose that the colony of Protozoa in the course
of conversion into Metazoa had the form of a blastosphere; and that at
one pole of this a depression appeared. The cells lining this
depression we may suppose to have been amoeboid, and to have carried
on the work of digestion; while the remaining cells were probably
ciliated. The digestion may be supposed to have been at first carried
on in the interior of the cells, as in the Protozoa; but, as the
depression became deeper (in order to increase the area of nutritive
cells and to retain the food) a digestive secretion probably became
poured out from the cells lining it, and the mode of digestion
generally characteristic of the Metazoa was thereby inaugurated. It
may be noted that an intracellular protozoon type of digestion
persists in the Porifera, and appears also to occur in many
Coelenterata, Turbellaria, &c., though in most of these cases both
kinds of digestion probably go on simultaneously[122].
[122] J. Parker, "On the Histology of _Hydra fusca_," _Quart.
Journ. Micr. Science_, vol. XX. 1880; and El. Metschnikoff, "Ueb.
die intracelluläre Verdauung bei Coelenteraten," _Zoologischer
Anzeiger_, No. 56, vol. III. 1880 and Lankester, "On the
intracellular digestion and endoderm of Limnocodium," _Quart.
Journ. Micr. Science_, vol. XXI. 1881.
Another hypothetical mode of passage, which fits in with delamination,
has been put forward by Lankester, and is illustrated by fig. 205. He
supposes that at the blastosphere stage the fluid in the centre of the
colony acquired special digestive properties; the inner ends of the
cells having at this stage somewhat different properties from the
outer, and the food being still incepted by the surface of the cells
(fig. 205, 3). In a later stage of the process the inner portions of
the cells became separated off as the hypoblast; while the food,
though still ingested in the form of solid particles by the
superficial cells, was carried through the protoplasm into the central
digestive cavity. Later (fig. 205, 4), the point where the food
entered became localised, and eventually a mouth became formed at this
point.
The main objection which can be raised against Lankester's view is
that it presupposes a type of delamination which does not occur in
nature except in Geryonia.
Metschnikoff has propounded a third view with reference to
delamination. He starts as before with a ciliated blastosphere. He
next supposes the cells from the walls of this to become budded off
into the central cavity, as in Eucope (fig. 202), and to lose their
cilia. These cells give rise to an internal parenchyma, which carries
on an intracellular digestion. At a later stage a central digestive
cavity is supposed to be formed. This view of the passage from the
protozoon to the metazoon state, though to my mind improbable in
itself, fits in very well with the ontogeny of the lower Hydrozoa.
Another view has been put forward by myself in the chapter on the
Porifera[123], to the effect that the amphiblastula larva of
Calcispongiæ may be a transitional form between the Protozoa and the
Metazoa, composed of a hemisphere of nutritive amoeboid cells, and a
hemisphere of ciliated cells. The absence of such a larval form in the
Coelenterata and higher Metazoa is opposed, however, to this larva
being regarded as a transitional form, except for the Porifera.
[123] Vol. II. p. 149.
It is obvious that so long as there is complete uncertainty as to the
value to be attached to the early developmental processes, it is not
possible to decide from these processes whether there is only a single
metazoon phylum or whether there may not be two or more such phyla. At
the same time there appear to be strong arguments for regarding the
Porifera as a phylum of the Metazoa derived independently from the
Protozoa. This seems to me to be shewn (1) by the striking larval
peculiarities of the Porifera; (2) by the early development of the
mesoblast in the Porifera, which stands in strong contrast to the
absence of this layer in the embryos of most Coelenterata; and above
all, (3) by the remarkable characters of the system of digestive
channels. A further argument in the same direction is supplied by the
fact that the germinal layers of the Sponges very probably do not
correspond physiologically to the germinal layers of other types. The
embryological evidence is insufficient to decide whether the
amphiblastula larva is, as suggested above, to be regarded as the
larval ancestor of the Porifera.
Homologies of the germinal layers. The question as to how far there is
a complete homology between the two primary germinal layers throughout
the Metazoa was the third of the questions proposed to be discussed
here.
Since there are some Metazoa with only two germinal layers, and other
Metazoa with three, and since, as is shewn in the following section,
the third layer or mesoblast can only be regarded as a derivative of
one or both the primary layers, it is clear that a complete homology
between the two primary germinal layers does not exist.
That there is a general homology appears on the other hand hardly open
to doubt.
The primary layers are usually continuous with each other, near one or
both (when both are present) the openings of the alimentary tract.
As a rule an oral and anal section of the alimentary tract--the
stomodæum and proctodæum--are derived from the epiblast; but the
limits of both these sections are so variable, sometimes even in
closely allied forms, that it is difficult to avoid the conclusion
that there is a border-land between the epiblast and hypoblast, which
appears by its development to belong in some forms to the epiblast and
in other forms to the hypoblast. If this is not the case it is
necessary to admit that there are instances in which a very large
portion of the alimentary canal is phylogenetically an epiblastic
structure. In some of the Isopods, for example, the stomodæum and
proctodæum give rise to almost the whole of the alimentary canal with
its appendages, except the liver.
The origin of the Mesoblast. A diploblastic condition of the organism
preceded, as we have seen, the triploblastic. The epiblast during the
diploblastic condition was, as appears from such forms as Hydra,
especially the sensory and protective layer, while the hypoblast was
the secretory and assimilating layer; both layers giving rise to
muscular elements. It must not, however, be supposed that in the early
diploblastic ancestors there was a complete differentiation of
function, but there is reason to think that both the primary layers
retained an indefinite capacity for developing into any form of
tissue[124]. The fact of the triploblastic condition being later than
the diploblastic proves in a conclusive way that the mesoblast is a
derivative of one or both the primary layers. In the Coelenterata we
can study the actual origin from the two primary layers of various
forms of tissue which in the higher types are derived from the
mesoblast[125]. This fact, as well as general _à priori_
considerations, conclusively prove that the mesoblast did not at first
originate as a mass of independent cells between the two primary
layers, but that in the first instance it gradually arose as
differentiations of the two layers, and that its condition in the
embryo as an independent layer of undifferentiated cells is a
secondary condition, brought about by the general tendency towards a
simplification of development, and a retardation of histological
differentiation[126].
[124] The Hertwigs (No. 270) have for instance shewn that nervous
structures are developed in the hypoblast in the Actinozoa and
other Coelenterata.
[125] There is considerable confusion in the use of the names for
the embryonic layers. In some cases various tissues formed by
differentiations of the primary layers have been called
mesoblast. Schultze, and more recently the Hertwigs, have pointed
out the inconvenience of this nomenclature. In the case of the
Coelenterata it is difficult to decide in certain instances
(_e.g._ Sympodium) whether the cells which give rise to a
particular tissue of the adult are to be regarded as forming a
mesoblast, _i.e._ a middle undifferentiated layer of cells, or
whether they arise as already histologically differentiated
elements from one of the primary layers. The attempt to
distinguish by a special nomenclature the epiblast and hypoblast
after and before the separation of the mesoblast, which has been
made by Allen Thomson (No. 1), appears incapable of being
consistently applied, though it is convenient to distinguish a
primary and a secondary hypoblast. A proposal of the Hertwigs to
adopt special names for the outer and inner limiting membranes of
the adult, and for the interposed mass of organs, appears to me
unnecessary.
[126] The causes which give rise to a retardation of histological
differentiation will be dealt with in the second part of this
chapter which deals with larval characters and larval forms.
The Hertwigs have recently attempted (No. 271) to distinguish two
types of differentiation of the mesoblast, viz. (1) a direct
differentiation from the primitive epithelial cells; (2) a
differentiation from primitively indifferent cells budded off into the
gelatinous matter between the two primary layers.
It is quite possible that this distinction may be well founded, but no
conclusive evidence of the occurrence of the second process has yet
been adduced. The Ctenophora are the type upon which special stress is
laid, but the early passage of amoeboid cells into the gelatinous
tissue, which subsequently become muscular, is very probably an
embryonic abbreviation; and it is quite possible that these cells may
phylogenetically have originated from epithelial cells provided with
contractile processes passing through the gelatinous tissue.
The conversion of non-embryonic connective-tissue cells into muscle
cells in the higher types has been described, but very much more
evidence is required before it can be accepted as a common occurrence.
In addition to the probably degraded Dicyemidæ and Orthonectidæ, the
Coelenterata are the only group in which a true mesoblast is not
always present. In other words, the Coelenterata are the only group in
which there is not found in the embryo an undifferentiated group of
cells from which the majority of the organs situated between the
epidermis and the alimentary epithelium are developed.
The organs invariably derived, in the triploblastic forms, from the
mesoblast, are the vascular and lymphatic systems, the muscular
system, and the greater part of the connective tissue and the
excretory and generative (?) systems. On the other hand, the nervous
systems (with a few possible exceptions) and organs of sense, the
epithelium of most glands, and a few exceptional connective-tissue
organs, as for example the notochord, are developed from the two
primary layers.
The fact of the first-named set of organs being invariably derived
from the mesoblast points to the establishment of the two following
propositions:--(1) That with the differentiation of the mesoblast as a
distinct layer by the process already explained, the two primary
layers lost for the most part the capacity they primitively possessed
of giving rise to muscular and connective-tissue differentiations[127],
to the epithelium of the excretory organs, and to generative cells.
(2) That the mesoblast throughout the triploblastic Metazoa, in so far
as these forms have sprung from a common triploblastic ancestor, is an
homologous structure.
[127] The connective-tissue test of the Tunicata, though derived
from the epiblast, is not really an example of such a
differentiation.
The second proposition follows from the first. The mesoblast can only
have ceased to be homologous throughout the triploblastica by
additions from the two primary layers, and the existence of such
additions is negatived by the first proposition.
These two propositions, which hang together, are possibly only
approximately true, since it is quite possible that future
investigations may shew that differentiations of the two primary
layers are not so rare as has been hitherto imagined.
Ranvier[128] finds that the muscles of the sweat-glands are developed
from the inner part of the layer of epiblast cells, invaginated to
form these glands.
[128] M. L. Ranvier. "Sur la structure des glandes sudoripares."
_Comptes Rendus_, Dec. 29, 1879.
Götte[129] describes the epiblast cells of the larva of Comatula as
being at a certain stage contractile and compares them with the
epithelio-muscular cells of Hydra. These cells would appear
subsequently to be converted into a simple cuticular structure.
[129] A. Götte, "Vergleich. Entwick. d. Comatula mediterranea."
_Archiv f. mikr. Anat._ vol. XII. p. 597.
It is moreover quite possible that fresh differentiations from the two
primary layers may have arisen after the triploblastic condition had
been established, and by the process of simplification of development
and precocious segregation, as Lankester calls it, have become
indistinguishable from the normal mesoblast. In spite of these
exceptions it is probable that the major part of the muscular system
of all existing triploblastic forms has been differentiated from the
muscular system of the ancestor or ancestors (if there is more than
one phylum) of the triploblastica. In the case of other tissues there
are a few instances which might be regarded as examples of an organ
primitively developed in one of the two primary layers having become
secondarily carried into the mesoblast. The notochord has sometimes
been cited as such an organ, but, as indicated in a previous chapter,
it is probable that its hypoblastic origin can always be demonstrated.
[FIG. 206. EPIBOLIC GASTRULA OF BONELLIA. (After Spengel.)
A. Stage when the four hypoblast cells are nearly enclosed.
B. Stage after the formation of the mesoblast has commenced by an
infolding of the lips of the blastopore.
_ep._ epiblast; _me._ mesoblast; _bl._ blastopore.]
The nervous system, although imbedded in mesoblastic derivates in the
adults of all the higher triploblastica, retains with marvellous
constancy its epiblastic origin (though it is usually separated from
the epiblast prior to its histogenic differentiation); yet in the
Cephalopoda, and some other Mollusca, the evidence is in favour of its
developing in the mesoblast. Should future investigations confirm
these conclusions, a good example will be afforded of an organ
changing the layer from which it usually develops[130]. The
explanation of such a change would be precisely the same as that
already given for the mesoblast as a whole.
[130] The Hertwigs hold that there is a distinct part of the
nervous system which was at first differentiated in the mesoblast
in many types, amongst others the Mollusca. The evidence in
favour of this view is extremely scanty and the view itself
appears to me highly improbable.
The actual mode of origin of various tissues, which in the true
triploblastic forms arise in mesoblast, can be traced in the
Coelenterata[131]. In this group the epiblast and hypoblast both give
rise to muscular and connective-tissue elements; and although the main
part of the nervous system is formed in the epiblast, it seems certain
that in some types nerves may be derived from the hypoblast[132].
These facts are extremely interesting, but it is by no means certain
that any conclusions can be directly drawn from them as to the actual
origin of the mesoblast in the triploblastic forms, till we know from
what diploblastic forms the triploblastica originated. All that they
shew is that any of the constituents of the mesoblast may have
originated from either of the primitive layers.
[131] The reader is referred for this subject to the valuable
memoirs which have been recently published by the Hertwigs,
especially to No. 270. He will find a general account of the
subject written before the appearance of the Hertwigs' memoir in
pp. 180-182 of Volume II. of this treatise.
[132] It would be interesting to know the history of the various
nervous structures found in the walls of the alimentary tract in
the higher forms. I have shewn (_Development of Elasmobranch
Fishes_, p. 172) that the central part of the sympathetic system
is derived from the epiblast. It would however be well to work
over the development of Auerbach's plexus.
[FIG. 207. TWO TRANSVERSE SECTIONS THROUGH EMBRYOS OF HYDROPHILUS
PICEUS. (After Kowalevsky.)
A. Section through an embryo at the point where the two germinal
folds most approximate.
B. Section through an embryo, in the anterior region where the folds
of the amnion have not united.
_gg._ germinal groove; _me._ mesoblast; _am._ amnion; _yk._ yolk.]
For further light as to the origin of the mesoblast, it is necessary
to turn to its actual development.
The following summary illustrates the more important modes in which
the mesoblast originates.
[FIG. 208. FIGURES ILLUSTRATING THE DEVELOPMENT OF ASTACUS. (From
Parker; after Reichenbach.)
A. Section through part of the ovum during segmentation. _n._
nuclei; _w.y._ white yolk; _y.p._ yolk pyramids; _c._ central
yolk mass.
B. and C. Longitudinal sections of the gastrula stage. _a._
_en._ archenteron; _b._ blastopore; _ms._ mesoblast; _ec._ epiblast;
hypoblast, distinguished from epiblast by shading.
D. Highly magnified view of anterior lip of blastopore, to shew the
origin of the primary mesoblast from the wall of the archenteron.
_p.ms._ primary mesoblast; _ec._ epiblast; _en._ hypoblast.
E. Two hypoblast cells to shew the amoeba-like absorption of yolk
spheres. _y._ yolk; _n._ nucleus; _p._ pseudopodial process.
F. Hypoblast cells giving rise endogenously to the secondary
mesoblast (_s.ms._); _n._ nucleus.]
1. It grows inwards from the lips of the blastopore as a pair of
bands. In these cases it may originate (_a_) from cells which are
clearly hypoblastic, (_b_) from cells which are clearly epiblastic,
(_c_) from cells which cannot be regarded as belonging to either
layer.
Mollusca.--Gasteropoda, Cephalopoda, and Lamellibranchiata. In
Gasteropoda and Lamellibranchiata the mesoblast sometimes originates
from a pair of cells at the lips of the blastopore, though very
probably some of the elements subsequently come from the epiblast; and
in Cephalopoda it begins as a ring of cells round the edge of the
blastoderm.
Polyzoa Entoprocta.--It originates from a pair of cells at the lips of
the blastopore.
Chætopoda.--Euaxes. It arises as a ridge of cells at the lips of the
blastopore (fig. 200).
Gephyrea.--Bonellia. It arises (fig. 206) as an infolding of the
epiblastic lips of the blastopore.
Nematelminthes.--Cucullanus. It grows backwards from the hypoblast
cells at the persistent oral opening of the blastopore.
Tracheata.--Insecta. It grows inwards from the lips of the germinal
groove (fig. 207), which probably represent the remains of a
blastopore. Part of the mesoblast is probably also derived from the
yolk-cells. A similar though more modified development of the
mesoblast occurs in the Araneina (fig. 214).
Crustacea.--Decapoda. It partly grows in from the hypoblastic lips of
the blastopore, and is partly derived from the yolk-cells (fig. 208).
[FIG. 209. THREE STAGES IN THE DEVELOPMENT OF SAGITTA. (A. and C.
after Bütschli, and B. after Kowalevsky.)
The three embryos are represented in the same positions.
A. Represents the gastrula stage.
B. Represents a succeeding stage, in which the primitive archenteron
is commencing to be divided into three.
C. Represents a later stage, in which the mouth involution (_m_) has
become continuous with the alimentary tract, and the blastopore has
become closed.
_m._ mouth; _al._ alimentary canal; _ae._ archenteron; _bl.p._
blastopore; _pv._ perivisceral cavity; _sp._ splanchnic mesoblast;
_so._ somatic mesoblast; _ge._ generative organs.]
2. The mesoblast is developed from the walls of hollow outgrowths of
the archenteron, the cavities of which become the body cavity.
Brachiopoda.--The walls of a pair of outgrowths form the whole of the
mesoblast.
Chætognatha.--The mesoblast arises in the same manner as in the
Brachiopoda (fig. 209).
Echinodermata.--The lining of the peritoneal cavity is developed from
the walls of outgrowths of the archenteron, but the greater part of
the mesoblast is derived from the amoeboid cells budded off from the
walls of the archenteron (fig. 210).
[FIG. 210. LONGITUDINAL SECTION THROUGH AN EMBRYO OF CUCUMARIA
DOLIOLUM AT THE END OF THE FOURTH DAY.
_Vpv._ vaso-peritoneal vesicle; _ME._ mesenteron; _Blp._, _Ptd._
blastopore, proctodæum.]
Enteropneusta (Balanoglossus).--The body cavity is derived from two
pairs of alimentary diverticula, the walls of which give rise to the
greater part of the mesoblast.
Chordata.--Paired archenteric outgrowths give rise to the whole
mesoblast in Amphioxus (fig. 211), and the mode of formation of the
mesoblast in other Chordata is probably secondarily derived from this.
3. The cells which will form the mesoblast become marked out very
early, and cannot be regarded as definitely springing from either of
the primary layers.
Turbellaria.--Leptoplana (fig. 212), Planaria polychroa (?).
Chætopoda.--Lumbricus, &c.
Discophora.
It is very possible that the cases quoted under this head ought more
properly to belong to group 1.
4. The mesoblast cells are split off from the epiblast.
Nemertea.--Larva of Desor. The mesoblast is stated to be split off
from the four invaginated discs.
5. The mesoblast is split off from the hypoblast.
Nemertea.--Some of the types without a metamorphosis.
Mollusca.--Scaphopoda. It is derived from the lateral and ventral
cells of the hypoblast.
Gephyrea.--Phascolosoma.
Vertebrata.--In most of the Ichthyopsida the mesoblast is derived from
the hypoblast (fig. 213). In some types (_i.e._ most of the Amniota)
the mesoblast might be described as originating at the lips of the
blastopore (primitive streak).
6. The mesoblast is derived from both germinal layers.
Tracheata.--Araneina (fig. 214). It is derived partly from cells split
off from the epiblast and partly from the yolk-cells; but it is
probable that the statement that the mesoblast is derived from both
the germinal layers is only formally accurate; and that the derivation
of part of the mesoblast from the yolk-cells is not to be interpreted
as a derivation from the hypoblast.
Amniota.--The derivation of the mesoblast of the Amniota from both the
primary germinal layers is without doubt a secondary process.
The conclusions to be drawn from the above summary are by no means
such as might have been anticipated. The analogy of the Coelenterata
would lead us to expect that the mesoblast would be derived partly
from the epiblast and partly from the hypoblast. Such, however, is not
for the most part the case, though more complete investigations may
shew that there are a greater number of instances in which the
mesoblast has a mixed origin than might be supposed from the above
summary.
[FIG. 211. SECTIONS OF AN AMPHIOXUS EMBRYO AT THREE STAGES. (After
Kowalevsky.)
A. Section at gastrula stage.
B. Section of a somewhat older embryo.
C. Section through the anterior part of still older embryo.
_np._ neural plate; _nc._ neural canal; _mes._ archenteron in A, and
mesenteron in B and C; _ch._ notochord; _so._ mesoblastic somite.]
I have attempted to reduce the types of development of the mesoblast
to six; but owing to the nature of the case it is not always easy to
distinguish the first of these from the last four. Of the six types
the second will on most hands be admitted to be the most remarkable.
The formation of hollow outgrowths of the archenteron, the cavities of
which give rise to the body cavity, can only be explained on the
supposition that the body cavity of the types in which such outgrowths
occur is derived from diverticula cut off from the alimentary tract.
The lining epithelium of the diverticula--the peritoneal
epithelium--is clearly part of the primitive hypoblast, and this part
of the mesoblast is clearly hypoblastic in origin.
[FIG. 212. SECTIONS THROUGH THE OVUM OF LEPTOPLANA TREMELLARIS IN
THREE STAGES OF DEVELOPMENT. (After Hallez.)
_ep._ epiblast; _m._ mesoblast; _hy._ yolk-cells (hypoblast); _bl._
blastopore.]
In the case of the Chætognatha (Sagitta), Brachiopoda, and Amphioxus,
the whole of the mesoblast originates from the walls of the
diverticula; while in the Echinodermata the walls of the diverticula
only give rise to the vaso-peritoneal epithelium, the remainder of the
mesoblast being derived from amoeboid cells which spring from the
walls of the archenteron before the origin of the vaso-peritoneal
outgrowths (figs. 199 and 210).
Reserving for the moment the question as to what conclusions can be
deduced from the above facts as to the origin of the mesoblast, it is
important to determine how far the facts of embryology warrant us in
supposing that in the whole of the triploblastic forms the body cavity
originated from the alimentary diverticula. There can be but little
doubt that the mode of origin of the mesoblast in many Vertebrata, as
two solid plates split off from the hypoblast, in which a cavity is
secondarily developed, is an abbreviation of the process observable in
Amphioxus; but this process approaches in some forms of Vertebrata to
the ingrowth of the mesoblast from the lips of the blastopore.
It is, therefore, highly probable that the paired ingrowths of the
mesoblast from the lips of the blastopore may have been in the first
instance derived from a pair of archenteric diverticula. This process
of formation of the mesoblast is, as may be seen by reference to the
summary, the most frequent, including as it does the Chætopoda, the
Mollusca, the Arthropoda, &c.[133]
[133] The wide occurrence of this process was first pointed out
by Rabl. He holds, however, a peculiar modification of the
gastræa theory, for which I must refer the reader to his paper
(No. 284); according to this theory the mesoblast has sprung from
a zone of cells of the blastosphere, at the junction between the
cells which will be invaginated and the epiblast cells. In the
bilateral blastosphere, from which he holds that all the higher
forms (Bilateralia) have originated, these cells had a bilateral
arrangement, and thus the bilateral origin of the mesoblast is
explained. The origin of the mesoblast from the lips of the
blastopore is explained by the position of its mother-cells in
the blastosphere. It need scarcely be said that the views already
put forward as to the probable mode of origin of the mesoblast,
founded on the analogy of the Coelenterata, are quite
incompatible with Rabl's theories.
[FIG. 213. TWO SECTIONS OF A YOUNG ELASMOBRANCH EMBRYO, TO SHEW THE
MESOBLAST SPLIT OFF AS TWO LATERAL MASSES FROM THE HYPOBLAST.
_mg._ medullary groove; _ep._ epiblast; _m._ mesoblast; _hy._
hypoblast; _n.al._ cells formed around the nuclei of the yolk which
have entered the hypoblast.]
While there is no difficulty in the view that the body cavity may have
originated from a pair of enteric diverticula in the case of the forms
where a body cavity is present, there is a considerable difficulty in
holding this view, for forms in which there is no body cavity distinct
from the alimentary diverticula.
Of these types the Platyelminthes are the most striking. It is, no
doubt, possible that a body cavity may have existed in the
Platyelminthes, and become lost; and the case of the Discophora, which
in their muscular and connective tissue systems as well as in the
absence of a body cavity resemble the Platyelminthes, may be cited in
favour of this view, in that, being closely related to the Chætopoda,
they are almost certainly descended from ancestors with a true body
cavity. The usual view of the primitive character of the
Platyelminthes, which has much to support it, is, however, opposed to
the idea that the body cavity has disappeared.
If Kowalevsky[134] is right in stating that he has found a form
intermediate between the Coelenterata and the Platyelminthes, there
will be strong grounds for holding that the Platyelminthes are, like
the Coelenterata, forms the ancestors of which were not provided with
a body cavity.
[134] _Zoologischer Anzeiger_, No. 52, p. 140. This form has been
named by Kowalevsky _Coeloplana Metschnikowii_. Kowalevsky's
description appears, however, to be quite compatible with the
view that this form is a creeping Ctenophor, in no way related to
the Turbellarians.
Perhaps the triploblastica are composed of two groups, viz. (1) a more
ancestral group (the Platyelminthes), in which there is no body cavity
as distinct from the alimentary, and (2) a group descended from these,
in which two of the alimentary diverticula have become separated from
the alimentary tract to form a body cavity (remaining triploblastica).
However this may be, the above considerations are sufficient to shew
how much there is that is still obscure with reference even to the
body cavity.
[FIG. 214. SECTION THROUGH AN EMBRYO OF AGELENA LABYRINTHICA.
The section is represented with the ventral plate upwards. In the
ventral plate is seen a keel-like thickening, which gives rise to
the main mass of the mesoblast.
_yk._ yolk divided into large polygonal cells, in several of which
are nuclei.]
If embryology gives no certain sound as to the questions just raised
with reference to the body cavity, still less is it to be hoped that
the remaining questions with reference to the origin of the mesoblast
can be satisfactorily answered. It is clear, in the first place, from
an inspection of the summary given above, that the process of
development of the mesoblast is, in all the higher forms, very much
abbreviated and modified. Not only is its differentiation relatively
deferred, but it does not in most cases originate, as it must have
done to start with, as a more or less continuous sheet, split off from
parts of one or both the primary layers. It originates in most cases
from the hypoblast, and although the considerations already urged
preclude us from laying very great stress on this mode of origin, yet
the derivation of the mesoblast from the walls of archenteric
outgrowths suggests the view that the whole, or at any rate the
greater part, of the mesoblast primitively arose by a process of
histogenic differentiation from the walls of the archenteron or rather
from diverticula of these walls. This view, which was originally put
forward by myself (No. 260), appears at first sight very improbable,
but if the statement of the Hertwigs (No. 270), that there is a large
development of a hypoblastic muscular system in the Actinozoa, is well
founded, it cannot be rejected as impossible. Lankester (No. 279), on
the other hand, has urged that the mode of origin of the mesoblast in
the Echinodermata is more primitive; and that the amoeboid cells which
here give rise to the muscular and connective tissues represent cells
which originally arose from the whole inner surface of the epiblast.
It is, however, to be noted that even in the Echinodermata the
amoeboid cells actually arise from the _hypoblast_, and their mode of
origin may, therefore, be used to support the view that the main part
of the muscular system of higher types is derived from the primitive
hypoblast.
The great changes which have taken place in the development of the
mesoblast would be more intelligible on this view than on the view
that the major part of the mesoblast primitively originated from the
epiblast. The presence of food-yolk is much more frequent in the
hypoblast than in the epiblast; and it is well known that a large
number of the changes in early development are caused by food-yolk.
If, therefore, the mesoblast has been derived from the hypoblast, many
more changes might be expected to have been introduced into its early
development than if it had been derived from the epiblast. At the same
time the hypoblastic origin of the mesoblast would assist in
explaining how it has come about that the development of the nervous
system is almost always much less modified than that of the mesoblast,
and that the nervous system is not, as might, on the grounds of
analogy, have been anticipated, as a rule secondarily developed in the
mesoblast.
The Hertwigs have recently suggested in their very interesting memoir
(No. 271) that the Triploblastica are to be divided into two phyla,
(1) the Enterocoela, and (2) the Pseudocoela; the former group
containing the Chætopoda, Gephyrea, Brachiopoda, Nematoda, Arthropoda,
Echinodermata, Enteropneusta and Chordata; and the latter the
Mollusca, Polyzoa, the Rotifera, and Platyelminthes.
The Enterocoela are forms in which the primitive alimentary
diverticula have given origin to the body cavity, while the major part
of the muscular system has originated from the epithelial walls of
these diverticula, part however being in many cases also derived from
the amoeboid cells, called by them mesenchyme, by the second process
of mesoblastic differentiation mentioned on p. 347.
In the Pseudocoela the muscular system has become differentiated from
mesenchyme cells; while the body cavity, where it exists, is merely a
split in the mesenchyme.
It is impossible for me to attempt in this place to state fully, or do
justice to, the original and suggestive views contained in this paper.
The general conclusion I cannot however accept. The views of the
Hertwigs depend to a large extent upon the supposition that it is
possible to distinguish histologically muscle cells derived from
epithelial cells, from those derived from mesenchyme cells. That in
many cases, and strikingly so in the Chordata, the muscle cells retain
clear indications of their primitive origin from epithelial cells, I
freely admit; but I do not believe either that its histological
character can ever be conclusive as to the non-epithelial origin of a
muscle cell, or that its derivation in the embryo from an indifferent
amoeboid cell is any proof that it did not, to start with, originate
from an epithelial cell.
I hold, as is clear from the preceding statements, that such immense
secondary modifications have taken place in the development of the
mesoblast, that no such definite conclusions can be deduced from its
mode of development as the Hertwigs suppose.
In support of the view that the early character of embryonic cells is
no safe index as to their phylogenetic origin, I would point to the
few following facts.
(1) In the Porifera and many of the Coelenterata (Eucope polystyla,
Geryonia, &c.) the hypoblast (endoderm) originates from cells, which
according to the Hertwigs' views ought to be classed as mesenchyme.
(2) In numerous instances muscles which have, phylogenetically, an
undoubted epithelial origin, are ontogenetically derived from cells
which ought to be classed as mesenchyme. The muscles of the head in
all the higher Vertebrata, in which the head cavities have
disappeared, are examples of this kind; the muscles of many of the
Tracheata, notably the Araneina, must also be placed in the same
category.
(3) The Mollusca are considered by the Hertwigs to be typical
Pseudocoela. A critical examination of the early development of the
mesoblast in these forms demonstrates however that with reference to
the mesoblast they must be classed in the same group as the Chætopoda.
The mesoblast (Vol. II. p. 227) clearly originates as two bands of
cells which grow inwards from the blastopore, and in some forms
(Paludina, Vol. II. fig. 107) become divided into a splanchnic and
somatic layer, with a body cavity between them. All these processes
are such as are, in other instances, admitted to indicate
Enterocoelous affinities.
The subsequent conversion of the mesoblast elements into amoeboid
cells, out of which branched muscles are formed, is in my opinion
simply due to the envelopment of the soft Molluscan body within a hard
shell.
In addition to these instances I may point out that the distinction
between the Pseudocoela and Enterocoela utterly breaks down in the
case of the Discophora, and the Hertwigs have made no serious attempt
to discuss the characters of this group in the light of their theory,
and that the derivation of the Echinoderm muscles from mesenchyme
cells is a difficulty which is very slightly treated.
II. LARVAL FORMS: THEIR NATURE, ORIGIN AND AFFINITIES.
Preliminary considerations. In a general way two types of development
may be distinguished, viz. a foetal type and a larval type. In the
foetal type animals undergo the whole or nearly the whole of their
development within the egg or within the body of the parent, and are
hatched in a condition closely resembling the adult; and in the larval
type they are born at an earlier stage of development, in a condition
differing to a greater or less extent from the adult, and reach the
adult state either by a series of small steps, or by a more or less
considerable metamorphosis.
The satisfactory application of embryological data to morphology
depends upon a knowledge of the extent to which the record of
ancestral history has been preserved in development. Unless secondary
changes intervened this record would be complete; it becomes therefore
of the first importance to the embryologist to study the nature and
extent of the secondary changes likely to occur in the foetal or the
larval state.
The principles which govern the perpetuation of variations which occur
in either the larval or the foetal state are the same as those for the
adult condition. Variations favourable to the survival of the species
are equally likely to be perpetuated, at whatever period of life they
occur, prior to the loss of the reproductive powers. The possible
nature and extent of the secondary changes which may have occurred in
the developmental history of forms, which have either a long larval
existence, or which are born in a nearly complete condition, is
primarily determined by the nature of the favourable variations which
can occur in each case.
Where the development is a foetal one, the favourable variations which
can most easily occur are--(1) abbreviations, (2) an increase in the
amount of food-yolk stored up for the use of the developing embryo.
Abbreviations take place because direct development is always simpler,
and therefore more advantageous; and, owing to the fact of the foetus
not being required to lead an independent existence till birth, and of
its being in the meantime nourished by food-yolk, or directly by the
parent, there are no physiological causes to prevent the characters of
any stage of the development, _which are of functional importance
during a free but not during a foetal existence_, from disappearing
from the developmental history. All organs of locomotion and nutrition
not required by the adult will, for this reason, obviously have a
tendency to disappear or to be reduced in foetal developments; and a
little consideration will shew that the ancestral stages in the
development of the nervous and muscular systems, organs of sense, and
digestive system will be liable to drop out or be modified, _when a
simplification can thereby be effected_. The circulatory and excretory
systems will not be modified to the same extent, because both of them
are usually functional during foetal life.
The mechanical effects of food-yolk are very considerable, and
numerous instances of its influence will be found in the earlier
chapters of this work[135]. It mainly affects the early stages of
development, _i.e._ the form of the gastrula, &c.
[135] For numerous instances of this kind, _vide_ Chapter XI. of
Vol. III.
The favourable variations which may occur in the free larva are much
less limited than those which can occur in the foetus. Secondary
characters are therefore very numerous in larvæ, and there may even be
larvæ with secondary characters only, as, for instance, the larvæ of
Insects.
In spite of the liability of larvæ to acquire secondary characters,
there is a powerful counterbalancing influence tending towards the
preservation of ancestral characters, in that larvæ are necessarily
compelled at all stages of their growth to retain _in a functional
state_ such systems of organs, at any rate, as are essential for a
free and independent existence. It thus comes about that, in spite of
the many causes tending to produce secondary changes in larvæ, there
is always a better chance of larvæ repeating, in an unabbreviated
form, their ancestral history, than is the case with embryos, which
undergo their development within the egg.
It may be further noted as a fact which favours the relative retention
by larvæ of ancestral characters, that a secondary larval stage is
less likely to be repeated in development than an ancestral stage,
because there is always a strong tendency for the former, which is a
secondarily intercalated link in the chain of development, to drop out
by the occurrence of a _reversion_ to the original type of
development.
The relative chances of the ancestral history being preserved in the
foetus or the larva may be summed up in the following way:--There is a
greater chance of the ancestral history being _lost_ in forms which
develop in the egg; and of its being _masked_ in those which are
hatched as larvæ.
The evidence from existing forms undoubtedly confirms the _a priori_
considerations just urged[136]. This is well shewn by a study of the
development of Echinodermata, Nemertea, Mollusca, Crustacea, and
Tunicata. The free larvæ of the four first groups are more similar
amongst themselves than the embryos which develop directly, and since
this similarity cannot be supposed to be due to the larvæ having been
modified by living under precisely similar conditions, it must be due
to their retaining common ancestral characters. In the case of the
_Tunicata_ the free larvæ retain much more completely than the embryos
certain characters such as the notochord, the cerebrospinal canal,
etc., which are known to be ancestral.
[136] It has long been known that land and freshwater forms
develop without a metamorphosis much more frequently than marine
forms. This is probably to be explained by the fact that there is
not the same possibility of a land or freshwater species
extending itself over a wide area by the agency of free larvæ,
and there is, therefore, much less advantage in the existence of
such larvæ; while the fact of such larvæ being more liable to be
preyed upon than eggs, which are either concealed, or carried
about by the parent, might render a larval stage absolutely
disadvantageous.
Types of Larvæ.--Although there is no reason to suppose that all
larval forms are ancestral, yet it seems reasonable to anticipate that
a certain number of the known types of larvæ would retain the
characters of the ancestors of the more important phyla of the animal
kingdom.
Before examining in detail the claims of various larvæ to such a
character, it is necessary to consider somewhat more at length the
kind of variations which are most likely to occur in larval forms.
It is probable _a priori_ that there are two kinds of larvæ, which may
be distinguished as primary and secondary larvæ. Primary larvæ are
more or less modified ancestral forms, which have continued
uninterruptedly to develop as free larvæ from the time when they
constituted the adult form of the species. Secondary larvæ are those
which have become introduced into the ontogeny of species, the young
of which were originally hatched with all the characters of the adult;
such secondary larvæ may have originated from a diminution of
food-yolk in the egg and a consequently earlier commencement of a free
existence, or from a simple adaptive modification in the just hatched
young. Secondary larval forms may resemble the primary larval forms in
cases where the ancestral characters were retained by the embryo in
its development within the egg; but in other instances their
characters are probably entirely adaptive.
_Causes tending to produce secondary changes in larvæ._--The modes of
action of natural selection on larvæ may probably be divided more or
less artificially into two classes.
1. The changes in development directly produced by the existence of
a larval stage.
2. The adaptive changes in a larva acquired in the ordinary course
of the struggle for existence.
The changes which come under the first head consist essentially in a
displacement in the order of development of certain organs. There is
always a tendency in development to throw back the differentiation of
the embryonic cells into definite tissues to as late a date as
possible. This takes place in order to enable the changes of form,
which every organ undergoes, in repeating even in an abbreviated way
its phylogenetic history, to be effected with the least expenditure of
energy. Owing to this tendency it comes about that when an organism is
hatched as a larva many of the organs are still in an undifferentiated
state, although the ancestral form which this larva represents had all
its organs fully differentiated. In order, however, that the larva may
be enabled to exist as an independent organism, certain sets of
organs, _e.g._ the muscular, nervous, and digestive systems, have to
be histologically differentiated. If the period of foetal life is
shortened, an earlier differentiation of certain organs is a necessary
consequence; and in almost all cases the existence of a larval stage
causes a displacement in order of development of organs, the complete
differentiation of many organs being retarded relatively to the
muscular, nervous, and digestive systems.
The possible changes under the second head appear to be unlimited.
There is, so far as I see, no possible reason why an indefinite number
of organs should not be developed in larvæ to protect them from their
enemies, and to enable them to compete with larvæ of other species,
and so on. The only limit to such development appears to be the
shortness of larval life, which is not likely to be prolonged, since,
_ceteris paribus_, the more quickly maturity is reached the better it
is for the species.
A very superficial examination of marine larvæ shews that there are
certain peculiarities common to most of them, and it is important to
determine how far such peculiarities are to be regarded as adaptive.
Almost all marine larvæ are provided with well-developed organs of
locomotion, and transparent bodies. These two features are precisely
those which it is most essential for such larvæ to have. Organs of
locomotion are important, in order that larvæ may be scattered as
widely as possible, and so disseminate the species; and transparency
is very important in rendering larvæ invisible, and so less liable to
be preyed upon by their numerous enemies[137].
[137] The phosphorescence of many larvæ is very peculiar. I
should have anticipated that phosphorescence would have rendered
them much more liable to be captured by the forms which feed upon
them; and it is difficult to see of what advantage it can be to
them.
These considerations, coupled with the fact that almost all
free-swimming animals, which have not other special means of
protection, are transparent, seem to shew that the transparency of
larvæ at all events is adaptive; and it is probable that organs of
locomotion are in many cases specially developed, and not ancestral.
Various spinous processes on the larvæ of Crustacea and Teleostei are
also examples of secondarily acquired protective organs.
These general considerations are sufficient to form a basis for the
discussion of the characters of the known types of larvæ.
The following table contains a list of the more important of such
larval forms:
DICYEMIDÆ.--The Infusoriform larva (vol. II. fig. 62).
PORIFERA.--(_a_) The Amphiblastula larva (fig. 215), with one-half
of the body ciliated, and the other half without cilia; (_b_) an
oval uniformly ciliated larva, which may be either solid or have
the form of a vesicle.
COELENERATA.--The planula (fig. 216).
TURBELLARIA.--(_a_) The eight-lobed larva of Müller (fig. 222);
(_b_) the larva of Götte and Metschnikoff, with some Pilidium
characters.
NEMERTEA.--The Pilidium (fig. 221).
TREMATODA.--The Cercaria.
ROTIFERA.--The Trochosphere-like larvæ of Brachionus (fig. 217) and
Lacinularia.
MOLLUSCA.--The Trochosphere larva (fig. 218), and the subsequent
Veliger larva (fig. 219).
BRACHIOPODA.--The three-lobed larva, with a postoral ring of cilia
(fig. 220).
POLYZOA.--A larval form with a single ciliated ring surrounding the
mouth, and an aboral ciliated ring or disc (fig. 228).
CHÆTOPODA.--Various larval forms with many characters like those of
the molluscan Trochosphere, frequently with distinct transverse
bands of cilia. They are classified as Atrochæ, Mesotrochæ,
Telotrochæ (fig. 225 A and fig. 226), Polytrochæ, and Monotrochæ
(fig. 225 B).
GEPHYREA NUDA.--Larval forms like those of preceding groups. A
specially characteristic larva is that of Echiurus (fig. 227).
GEPHYREA TUBICOLA.--Actinotrocha (fig. 230), with a postoral
ciliated ring of arms.
MYRIAPODA.--A functionally hexapodous larval form is common to all
the Chilognatha (vol. II. fig. 174).
INSECTA.--Various secondary larval forms.
CRUSTACEA.--The Nauplius (vol. II. fig. 208) and the Zoæa (vol. II.
fig. 210).
ECHINODERMATA.--The Auricularia (fig. 223 A), the Bipinnaria (fig.
223 B), and the Pluteus (fig. 224), and the transversely-ringed
larvæ of Crinoidea (vol. II. fig. 268). The three first of which
can be reduced to a common type (fig. 231 C).
ENTEROPNEUSTA.--Tornaria (fig. 229).
UROCHORDA (TUNICATA).--The tadpole-like larva (vol. III. fig. 8).
GANOIDEI.--A larva with a disc with adhesive papillæ in front of the
mouth (vol. III. fig. 67).
ANURUS AMPHIBIA.--The tadpole (vol. III. fig. 80).
[FIG. 215. TWO FREE STAGES IN THE DEVELOPMENT OF SYCANDRA RAPHANUS.
(After Schultze.)
A. Amphiblastula stage.
B. Stage after the ciliated cells have commenced to be invaginated.
_c.s._ segmentation cavity; _ec._ granular epiblast cells; _en._
ciliated hypoblast cells.]
[FIG. 216. THREE LARVAL STAGES OF EUCOPE PLOYSTYLA. (After Kowalevsky.)
A. Blastosphere stage with hypoblast spheres becoming budded into
the central cavity.
B. Planula stage with solid hypoblast.
C. Planula stage with a gastric cavity.
_ep._ epiblast; _hy._ hypoblast; _al._ gastric cavity.]
Of the larval forms included in the above list a certain number are
probably without affinities outside the group to which they belong.
This is the case with the larvæ of the Myriapoda, the Crustacean
larvæ, and with the larval forms of the Chordata. I shall leave these
forms out of consideration.
There are, again, some larval forms which may possibly turn out
hereafter to be of importance, but from which, in the present state of
our knowledge, we cannot draw any conclusions. The infusoriform larva
of the Dicyemidæ, and the Cercaria of the Trematodes, are such forms.
Excluding these and certain other forms, we have finally left for
consideration the larvæ of the Coelenterata, the Turbellaria, the
Rotifera, the Nemertea, the Mollusca, the Polyzoa, the Brachiopoda,
the Chætopoda, the Gephyrea, the Echinodermata, and the Enteropneusta.
The larvæ of these forms can be divided into two groups. The one group
contains the larva of the Coelenterata or Planula, the other group the
larvæ of all the other forms.
The Planula (fig. 216) is characterised by its extreme simplicity. It
is a two-layered organism, with a form varying from cylindrical to
oval, and usually a radial symmetry. So long as it remains free it is
not usually provided with a mouth, and it is as yet uncertain whether
or no the absence of a mouth is to be regarded as an ancestral
character. The Planula is very probably the ancestral form of the
Coelenterata.
[FIG. 217. EMBRYO OF BRACHIONUS URCEOLARIS, SHORTLY BEFORE IT IS
HATCHED. (After Salensky.)
_m._ mouth; _ms._ masticatory apparatus; _me._ mesenteron; _an._
anus; _ld._ lateral gland; _ov._ ovary; _t._ tail (foot); _tr._
trochal disc; _sg._ supraoesophageal ganglion.]
The larvæ of almost all the other groups, although they may be
subdivided into a series of very distinct types, yet agree in the
possession of certain common characters[138]. There is a more or less
dome-shaped dorsal surface, and a flattened or concave ventral
surface, containing the opening of the mouth, and usually extending
posteriorly to the opening of the anus, when such is present.
[138] The larva of the Brachiopoda does not possess most of the
characters mentioned below. It is probably, all the same, a
highly differentiated larval form belonging to this group.
The dorsal dome is continued in front of the mouth to form a _large
præoral lobe_.
There is usually present at first an uniform covering of cilia; but in
the later larval stages there are almost always formed definite bands
or rings of long cilia, by which locomotion is effected. These bands
are often produced into arm-like processes.
The alimentary canal has, typically, the form of a bent tube with a
ventral concavity, constituted (when an anus is present) of three
sections, viz. an oesophagus, a stomach, and a rectum. The oesophagus
and sometimes the rectum are epiblastic in origin, while the stomach
always and the rectum usually are derived from the hypoblast[139].
[139] There is some uncertainty as to the development of the
oesophagus in the Echinodermata, but recent researches appear to
indicate that it is developed from the hypoblast.
[FIG. 218. DIAGRAM OF AN EMBRYO OF PLEUROBRANCHIDIUM. (From
Lankester.)
_f._ foot; _ot._ otocyst; _m._ mouth; _v._ velum; _ng._ nerve
ganglion; _ry._ residual yolk spheres; _shs._ shell-gland; _i._
intestine.]
To the above characters may be added a glass-like transparency; and
the presence of a widish space possibly filled with gelatinous tissue,
and often traversed by contractile cells, between the alimentary tract
and the body wall.
Considering the very profound differences which exist between many of
these larvæ, it may seem that the characters just enumerated are
hardly sufficient to justify my grouping them together. It is,
however, to be borne in mind that my grounds for doing so depend quite
as much upon the fact that they constitute a series without any great
breaks in it, as upon the existence of characters common to the whole
of them. It is also worth noting that most of the characters which
have been enumerated as common to the whole of these larvæ are not
such secondary characters as (in accordance with the considerations
used above) might be expected to arise from the fact of their being
subjected to nearly similar conditions of life. Their transparency is,
no doubt, such a secondary character, and it is not impossible that
the existence of ciliated bands may be so also; but it is quite
possible that if, as I suppose, these larvæ reproduce the characters
of some ancestral form, this form may have existed at a time when all
marine animals were free-swimming, and that it may, therefore, have
been provided with at least one ciliated band.
[FIG. 219. LARVÆ OF CEPHALOPHOROUS MOLLUSCA IN THE VELIGER STAGE.
(From Gegenbaur.)
A. and B. Earlier and later stage of Gasteropod. C. Pteropod
(Cymbulia). _v._ velum; _c._ shell; _p._ foot; _op._ operculum; _t._
tentacle.]
[FIG. 220. LARVA OF ARGIOPE. (From Gegenbaur; after Kowalevsky.)
_m._ mantle; _b._ setæ; _d._ archenteron.]
The detailed consideration of the characters of these larvæ, given
below, supports this view.
This great class of larvæ may, as already stated, be divided into a
series of minor subdivisions. These subdivisions are the following:
1. The Pilidium Group.--This group is characterised by the mouth being
situated nearly in the centre of the ventral surface, and by the
absence of an anus. It includes the Pilidium of the Nemertines (fig.
221), and the various larvæ of marine Dendrocoela (fig. 222). At the
apex of the præoral lobe a thickening of epiblast may be present, from
which (fig. 232) a contractile cord sometimes passes to the
oesophagus.
[FIG. 221. TWO STAGES IN THE DEVELOPMENT OF PILIDIUM. (After
Metschnikoff.)
_ae._ archenteron; _oe._ oesophagus; _st._ stomach; _am._ amnion;
_pr.d._ prostomial disc; _po.d._ metastomial disc; _c.s._ cephalic
sack (lateral pit).]
2. The Echinoderm Group.--This group (figs. 223, 224 and 231 C) is
characterised by the presence of a longitudinal _postoral_ band of
cilia, by the absence of special sense organs in the præoral region,
and by the development of the body cavity as an outgrowth of the
alimentary tract. The three typical divisions of the alimentary tract
are present, and there is a more or less developed præoral lobe. This
group only includes the larvæ of the Echinodermata.
3. The Trochosphere Group.--This group (figs. 225, 226) is
characterised by the presence of a præoral ring of long cilia, the
region in front of which forms a great part of the præoral lobe. The
mouth opens immediately behind the præoral ring of cilia, and there is
very often a second ring of short cilia parallel to the main ring,
immediately behind the mouth. The function of the ring of short cilia
is nutritive, in that its cilia are employed in bringing food to the
mouth; while the function of the main ring is locomotive. A perianal
patch or ring of cilia is often present (fig. 225 A), and in many
forms intermediate rings are developed between the præoral and
perianal rings.
[FIG. 222. A. LARVA OF EURYLEPTA AURICULATA IMMEDIATELY AFTER
HATCHING. VIEWED FROM THE SIDE. (After Hallez.) _m._ mouth.
B. MÜLLER'S TURBELLARIAN LARVA (PROBABLY THYSANOZOON). VIEWED FROM
THE VENTRAL SURFACE. (After Müller.) The ciliated band is
represented by the black line. _m._ mouth; _u.l._ upper lip.]
The præoral lobe is usually the seat of a special thickening of
epiblast, which gives rise to the supraoesophageal ganglion of the
adult. On this lobe optic organs are very often developed in
connection with the supraoesophageal ganglion, and a contractile band
frequently passes from this region to the oesophagus.
The alimentary tract is formed of the three typical divisions.
The body cavity is not developed directly as an outgrowth of the
alimentary tract, though the process by which it originates is very
probably secondarily modified from a pair of alimentary outgrowths.
Paired excretory organs, opening to the exterior and into the body
cavity, are often present (fig. 226 _nph_).
This type of larva is found in the Rotifera (fig. 217) (in which it is
preserved in the adult state), the Chætopoda (figs. 225 and 226), the
Mollusca (fig. 218), the Gephyrea nuda (fig. 227), and the Polyzoa
(fig. 228)[140].
[140] For a discussion as to the structure of the Polyzoon larva,
_vide_ Vol. II. p. 305.
[FIG. 223. A. THE LARVA OF A HOLOTHUROID.
B. THE LARVA OF AN ASTEROID.
_m._ mouth; _st._ stomach; _a._ anus; _l.c._ primitive longitudinal
ciliated band; _pr.c._ præoral ciliated band.]
4. Tornaria.--This larva (fig. 229) is intermediate in most of its
characters between the larvæ of the Echinodermata (more especially the
Bipinnaria) and the Trochosphere. It resembles Echinoderm larvæ in the
possession of a longitudinal ciliated band (divided into a præoral and
a postoral ring), and in the derivation of the body cavity and
water-vascular vesicle from alimentary diverticula; and it resembles
the Trochosphere in the presence of sense organs on the præoral lobe,
in the existence of a perianal ring of cilia, and in the possession of
a contractile band passing from the præoral lobe to the oesophagus.
[FIG. 224. A LARVA OF STRONGYLOCENTRUS. (From Agassiz.)
_m._ mouth; _a._ anus; _o._ oesophagus; _d._ stomach; _c._
intestine; _['v]._ and _v._ ciliated ridges; _w._ water-vascular
tube; _r._ calcareous rods.]
5. Actinotrocha.--The remarkable larva of Phoronis (fig. 230), known
as Actinotrocha, is characterised by the presence of (1) a postoral
and somewhat longitudinal ciliated ring produced into tentacles, and
(2) a perianal ring. It is provided with a præoral lobe, and a
terminal or somewhat dorsal anus.
6. The larva of the Brachiopoda articulata (fig. 220).
The relationships of the six types of larval forms thus briefly
characterised have been the subject of a considerable amount of
controversy, and the following suggestions on their affinities must be
viewed as somewhat speculative. The Pilidium type of larva is in some
important respects less highly differentiated than the larvæ of the
five other groups. It is, in the first place, without an anus; and
there are no grounds for supposing that the anus has become lost by
retrogressive changes. If for the moment it is granted that the
Pilidium larva represents more nearly than the larvæ of the other
groups the ancestral type of larva, what characters are we led to
assign to the ancestral form which this larva repeats?
[FIG. 225. TWO CHÆTOPOD LARVÆ. (From Gegenbaur.)
_o._ mouth; _i._ intestine; _a._ anus; _v._ præoral ciliated band;
_w._ perianal ciliated band.]
In the first place, this ancestral form, of which fig. 231 A is an
ideal representation, would appear to have had a dome-shaped body,
with a flattened oral surface and a rounded aboral surface. Its
symmetry was radial, and in the centre of the flattened oral surface
was placed the mouth, and round its edge was a ring of cilia. The
passage of a Pilidium-like larva into the vermiform bilateral
Platyelminth form, and therefore it may be presumed of the ancestral
form which this larva repeats, is effected by the larva becoming more
elongated, and by the region between the mouth and one end of the body
becoming the præoral region, and by an outgrowth between the mouth and
the opposite end developing into the trunk, an anus becoming placed at
its extremity in the higher forms.
If what has been so far postulated is correct, it is clear that this
primitive larval form bears a very close resemblance to a simplified
free-swimming Coelenterate (Medusa), and that the conversion of such a
radiate form into the bilateral took place, not by the elongation of
the aboral surface, and the formation of an anus there, but by the
unequal elongation of the oral face, an anterior part, together with
the dome above it, forming a præoral lobe, and a posterior outgrowth
the trunk (figs. 226 and 233); while the aboral surface became the
dorsal surface.
[FIG. 226. POLYGORDIUS LARVA. (After Hatschek.)
_m._ mouth; _sg._ supraoesophageal ganglion; _nph._ nephridion;
_me.p._ mesoblastic band; _an._ anus; _ol._ stomach.]
This view fits in very well with the anatomical resemblances between
the Coelenterata and the Turbellaria[141], and shews, if true, that
the ventral and median position of the mouth in many Turbellaria is
the primitive one.
[141] _Vide_ Vol. II. pp. 179 and 191. In this connection
attention may be called to _Coeloplana Metschnikowii_, a form
described by Kowalevsky, _Zoologischer Anzeiger_, No. 52, p. 140,
as being intermediate between the Ctenophora and the Turbellaria.
As already mentioned, there does not appear to me to be
sufficient evidence to prove that this form is not merely a
creeping Ctenophor.
[FIG. 227. LARVA OF ECHIURUS. (After Salensky.)
_m._ mouth; _an._ anus; _sg._ supraoesophageal ganglion (?).]
[FIG. 228. DIAGRAM OF A LARVA OF THE POLYZOA.
_m._ mouth; _an._ anus; _st._ stomach; _s._ ciliated disc.]
The above suggestion as to the mode of passage from the radial into
the bilateral form differs largely from that usually held.
Lankester[142], for instance, gives the following account of this
passage:
[142] _Quart. Journ. of Micr. Science_, Vol. XVII. pp. 422-3.
"It has been recognised by various writers, but notably by Gegenbaur
and Haeckel, that a condition of radiate symmetry must have preceded
the condition of bilateral symmetry in animal evolution. The
Diblastula may be conceived to have been at first absolutely spherical
with spherical symmetry. The establishment of a mouth led necessarily
to the establishment of a structural axis passing through the mouth,
around which axis the body was arranged with radial symmetry. This
condition is more or less perfectly maintained by many Coelenterates,
and is reassumed by degradation of higher forms (Echinoderms, some
Cirrhipedes, some Tunicates). The next step is the differentiation of
an upper and a lower surface in relation to the horizontal position,
with mouth placed anteriorly, assumed by the organism in locomotion.
With the differentiation of a superior and inferior surface, a right
and a left side, complementary one to the other, are necessarily also
differentiated. Thus the organism becomes bilaterally symmetrical. The
Coelentera are not wanting in indications of this bilateral symmetry,
but for all other higher groups of animals it is a fundamental
character. Probably the development of a region in front of, and
dorsal to the mouth, forming the _Prostomium_, was accomplished _pari
passu_ with the development of bilateral symmetry. In the radially
symmetrical Coelentera we find very commonly a series of lobes of the
body-wall or tentacles produced _equally_--with radial symmetry, that
is to say--all round the mouth, the mouth terminating the main axis of
the body--that is to say, the organism being 'telostomiate.' The later
fundamental form, common to all animals above the Coelentera, is
attained by shifting what was the main axis of the body--so that it
may be described now as the 'enteric' axis; whilst the new main axis,
that parallel with the plane of progression, passes through the dorsal
region of the body running obliquely in relation to the enteric axis.
Only one lobe or outgrowth of those radially disposed in the
telostomiate organisms now persists. This lobe lies dorsally to the
mouth, and through it runs the new main axis. This lobe is the
_Prostomium_, and all the organisms which thus develop a new main
axis, oblique to the old main axis, may be called prostomiate."
It will be seen from this quotation that the aboral part of the body
is supposed to elongate to form the trunk, while the præoral region is
derived from one of the tentacles.
Before proceeding to further considerations as to the origin of the
Bilateralia, suggested by the Pilidium type of larva, it is necessary
to enter into a more detailed comparison between our larval forms.
A very superficial consideration of the characters of these forms
brings to light two important features in which they differ, viz.:
(1) In the presence or absence of sense organs on the præoral lobe.
[FIG. 229. TWO STAGES IN THE DEVELOPMENT OF TORNARIA. (After
Metschnikoff.)
The black lines represent the ciliated bands.
_m._ mouth; _an._ anus; _br._ branchial cleft; _ht._ heart; _c._
body cavity between splanchnic and somatic mesoblast layers; _w._
so-called water-vascular vesicle; _v._ circular blood-vessel.]
(2) In the presence or absence of outgrowths from the alimentary tract
to form the body cavity.
The larvæ of the Echinodermata and Actinotrocha (?) are without sense
organs on the præoral lobe, while the other types of larvæ are
provided with them. Alimentary diverticula are characteristic of the
larvæ of the Echinodermata and of Tornaria.
If the conclusion already arrived at to the effect that the prototype
of the six larval groups was descended from a radiate ancestor is
correct, it appears to follow that the nervous system, in so far as it
was differentiated, had primitively a radiate form; and it is also
probably true that there were alimentary diverticula in the form of
radial pouches, _two_ of which may have given origin to the paired
diverticula which become the body cavity in such types as the
Echinodermata, Sagitta, etc. If these two points are granted, the
further conclusions seem to follow--(1) that the ganglion and sense
organs of the præoral lobe were secondary structures, which arose
(perhaps as differentiations of an original circular nerve ring) after
the assumption of a bilateral form; and (2) that the absence of these
organs in the larvæ of the Echinodermata and Actinotrocha (?) implies
that these larvæ retain, so far, more primitive characters than the
Pilidium. The same may be said of the alimentary diverticula. There
are thus indications that in two important points the Echinoderm larvæ
are more primitive than the Pilidium.
[FIG. 230. ACTINOTROCHA. (After Metschnikoff.)
_m._ mouth; _an._ anus.]
The above conclusions with reference to the Pilidium and Echinoderm
larvæ involve some not inconsiderable difficulties, and suggest
certain points for further discussion.
In the first place it is to be noted that the above speculations
render it probable that the type of nervous system from which that
found in the adults of the Echinodermata, Platyelminthes, Chætopoda,
Mollusca, etc., is derived, was a circumoral ring, like that of
Medusæ, with which radially arranged sense organs may have been
connected; and that in the Echinodermata _this form of nervous system
has been retained_, while in the other types it has been modified. Its
anterior part may have given rise to supraoesophageal ganglia and
organs of vision; these being developed on the assumption of a
bilaterally symmetrical form, and the consequent necessity arising for
the sense organs to be situated at the anterior end of the body. If
this view is correct, the question presents itself as to how far the
posterior part of the nervous system of the Bilateralia can be
regarded as derived from the primitive radiate ring.
[FIG. 231. THREE DIAGRAMS REPRESENTING THE IDEAL EVOLUTION OF
VARIOUS LARVAL FORMS.
A. Ideal ancestral larval form.
B. Larval form from which the Trochosphere larva may have been
derived.
C. Larval form from which the typical Echinoderm larva may have been
derived.
_m._ mouth; _an._ anus; _st._ stomach; _s.g._ supraoesophageal
ganglion. The black lines represent the ciliated bands.]
A circumoral nerve-ring, if longitudinally extended, might give rise
to a pair of nerve-cords united _in front and behind_--exactly such a
nervous system, in fact, as is present in many Nemertines[143] (the
Enopla and Pelagonemertes), in Peripatus[144], and in primitive
molluscan types (Chiton, Fissurella, etc.). From the lateral parts of
this ring it would be easy to derive the ventral cord of the Chætopoda
and Arthropoda. It is especially deserving of notice in connection
with the nervous system of the above-mentioned Nemertines and
Peripatus, that the commissure connecting the two nerve-cords behind
is placed on the _dorsal_ side of the intestine. As is at once
obvious, by referring to the diagram (fig. 231 B), this is the
position this commissure ought, undoubtedly, to occupy if derived from
part of a nerve-ring which originally followed more or less closely
the ciliated edge of the body of the supposed radiate ancestor.
[143] _Vide_ Hubrecht, "Zur Anat. und Phys. d. Nerven-System. d.
Nemertinen," _Kön. Akad. Wiss._, Amsterdam; and "Researches on
the Nervous System of Nemertines," _Quart. Journ. of Micr.
Science_, 1880.
[144] _Vide_ F. M. Balfour, "On some points in the Anat. of
Peripatus capensis," _Quart. Journ. of Micr. Science_, Vol. XIX.
1879.
The fact of this arrangement of the nervous system being found in so
primitive a type as the Nemertines tends to establish the views for
which I am arguing; the absence or imperfect development of the two
longitudinal cords in Turbellarians may very probably be due to the
posterior part of the nerve-ring having atrophied in this group.
It is by no means certain that this arrangement of the nervous system
in some Mollusca and in Peripatus is primitive, though it may be so.
In the larvæ of the Turbellaria the development of sense organs in the
præoral region is very clear (fig. 222 B); but this is by no means so
obvious in the case of the true Pilidium. There is in Pilidium (fig.
232 A) a thickening of epiblast at the summit of the dorsal dome,
which might seem, from the analogy of Mitraria, etc. (fig. 233), to
correspond to the thickening of the præoral lobe, which gives rise to
the supraoesophageal ganglion; but, as a matter of fact, this part of
the larva does not apparently enter into the formation of the young
Nemertine (fig. 232). The peculiar metamorphosis, which takes place in
the development of the Nemertine out of the Pilidium[145], may,
perhaps, eventually supply an explanation of this fact; but at present
it remains as a still unsolved difficulty.
[145] _Vide_ Vol. II. p. 204.
The position of the flagellum in Pilidium, and of the supraoesophageal
ganglion in Mitraria, suggests a different view of the origin of the
supraoesophageal ganglion from that adopted above. The position of the
ganglion in Mitraria corresponds closely with that of the auditory
organ in Ctenophora; and it is not impossible that the two structures
may have had a common origin. If this view is correct, we must suppose
that the apex of the aboral lobe has become the centre of the præoral
field of the Pilidium and Trochosphere larval forms[146]--a view which
fits in very well with their structure (figs. 226 and 233). The whole
of the questions concerning the nervous system are still very obscure,
and until further facts are brought to light no definite conclusions
can be arrived at.
[146] The independent development of the supraoesophageal
ganglion and ventral nerve-cord in Chætopoda (_vide_ Kleinenberg,
_Development of Lumbricus trapezoides_) agrees very
satisfactorily with this view.
The absence of sense organs on the præoral lobe of larval
Echinodermata, coupled with the structure of the nervous system of the
adult, points to the conclusion that the adult Echinodermata _have
retained_, and not, as is now usually held, secondarily acquired,
their radial symmetry; and if this is admitted it follows that the
obvious bilateral symmetry of Echinoderm larvæ is a secondary
character.
[FIG. 232. A. PILIDIUM WITH AN ADVANCED NEMERTINE WORM. B. RIPE
EMBRYO OF NEMERTES IN THE POSITION IT OCCUPIES IN PILIDIUM. (Both
after Bütschli.)
_oe._ oesophagus; _st._ stomach; _i._ intestine; _pr._ proboscis;
_lp._ lateral pit (cephalic sack); _an._ amnion; _n._ nervous
system.]
The bilateral symmetry of many Coelenterate larvæ (the larva of
Æginopsis, of many Acraspeda, of Actinia, &c.), coupled with the fact
that a bilateral symmetry is obviously advantageous to a free-swimming
form, is sufficient to shew that this supposition is by no means
extravagant; while the presence of only two alimentary diverticula in
Echinoderm larvæ is quite in accord with the presence of a single pair
of perigastric chambers in the early larva of Actinia, though it must
be admitted that the derivation of the water-vascular system from the
left diverticulum is not easy to understand on this view.
A difficulty in the above speculation is presented by the fact of the
anus of the Echinodermata being the permanent blastopore, and arising
prior to the mouth. If this fact has any special significance, it
becomes difficult to regard the larva of Echinoderms and that of the
other types as in any way related; but if the views already urged, in
a previous section on the germinal layers, as to the unimportance of
the blastopore, are admitted, the fact of the anus coinciding with the
blastopore ceases to be a difficulty. As may be seen, by referring to
fig. 231 C, the anus is placed on the dorsal side of the ciliated
band. This position for the anus adapts itself to the view that the
Echinoderm larva had originally a radial symmetry, _with the anus
placed at the aboral apex_, and that, with the elongation of the larva
on the attainment of a bilateral symmetry, the aboral apex became
shifted to the present position of the anus.
It may be noticed that the obscure points connected with the absence
of a body cavity in most adult Platyelminthes, which have already been
dealt with in the section of this chapter devoted to the germinal
layers, present themselves again here; and that it is necessary to
assume either that alimentary diverticula, like those in the
Echinodermata, were primitively present in the Platyelminthes, but
have now disappeared from the ontogeny of this group, or that the
alimentary diverticula have not become separated from the alimentary
tract.
So far the conclusion has been reached that the archetype of the six
types of larvæ had a radiate form, and that amongst existing larvæ it
is most nearly approached in general shape and in the form of the
alimentary canal by the Pilidium group, and in certain other
particulars by the Echinoderm larvæ.
The edge of the oral disc of the larval archetype was probably armed
with a ciliated ring, from which the ciliated ring of the Pilidium
type and of the Echinodermata was most likely derived. The ciliated
ring of the Pilidium varies greatly in its characters, and has not
always the form of a complete ring. In Pilidium proper (fig. 232 A) it
is a simple ring surrounding the edge of the oral disc. In Müller's
larva of Thysanozoon (fig. 222 B) it is inclined at an axis to the
oral disc, and might be called præoral, but such a term cannot be
properly used in the absence of an anus.
[FIG. 233. TWO STAGES IN THE DEVELOPMENT OF MITRARIA. (After
Metschnikoff.)
_m._ mouth; _an._ anus; _sg._ supraoesophageal ganglion; _br._ and
_b._ provisional bristles; _pr.b._ præoral ciliated band.]
[FIG. 234. CYPHONAUTES (LARVA OF MEMBRANIPORA). (After Hatschek.)
_m._ mouth; _a´._ anus; _f.g._ foot gland; _x._ problematical body
(probably a bud). The aboral apex is turned downwards.]
The Echinoderm ring is oblique to the axis of the body, and, owing to
the fact of its passing ventrally in front of the anus, must be called
postoral.
The next point to be considered is that of the affinities of the other
larval types to these two types.
The most important of all the larval types is the Trochosphere, and
this type is undoubtedly more closely related to the Pilidium than to
the Echinoderm larva. Mitraria amongst the Chætopods (fig. 233) has,
indeed, nearly the form of a Pilidium, and mainly differs from a
Pilidium in the possession of an anus and of provisional bristles; the
same may be said of Cyphonautes (fig. 234) amongst the Polyzoa.
The existence of these two forms appears to shew that the præoral
ciliated ring of the Trochosphere may very probably be derived
directly from the circumoral ciliated ring of the Pilidium; the other
ciliated rings or patches of the Trochosphere having a secondary
origin.
The larva of the Brachiopoda (fig. 220), in spite of its peculiar
characters, is, in all probability, more closely related to the
Chætopod Trochosphere than to any other larval type. The most
conspicuous point of agreement between them is, however, the
possession in common of provisional setæ.
Echinoderm larvæ differ from the Trochosphere, not only in the points
already alluded to, but in the character of the ciliated band. The
Echinoderm band is longitudinal and postoral. As just stated, there is
reason to think that the præoral band of the Trochosphere and the
postoral band of the Echinoderm larva are both derived from a ciliated
ring surrounding the oral disc of the prototype of these larvæ (_vide_
fig. 231). In the case of the Echinodermata the anus must have been
formed on the _dorsal side_ of this ring, and in the case of the
Trochosphere on the _ventral side_; and so the difference in position
between the two rings was brought about. Another view with reference
to these rings has been put forward by Gegenbaur and Lankester, to the
effect that the præoral ring of the Trochosphere is derived from the
breaking up of the single band of most Echinoderm larvæ into the two
bands found in Bipinnaria (_vide_ fig. 223) and the atrophy of the
posterior band. There is no doubt a good deal to be said for this
origin of the præoral ring, and it is strengthened by the case of
Tornaria; but the view adopted above appears to me more probable.
Actinotrocha (fig. 230) undoubtedly resembles more closely Echinoderm
larvæ than the Trochosphere. Its ciliated ring has Echinoderm
characters, and the growth along the line of the ciliated ring of a
series of arms is very similar to what takes place in many
Echinoderms. It also agrees with the Echinoderm larvæ in the absence
of sense organs on the præoral lobe.
Tornaria (fig. 229) cannot be definitely united either with the
Trochosphere or with the Echinoderm larval type. It has important
characters in common with both of these groups, and the mixture of
these characters renders it a very striking and well-defined larval
form.
Phylogenetic conclusions. The phylogenetic conclusions which follow
from the above views remain to be dealt with. The fact that all the
larvæ of the groups above the Coelenterata can be reduced to a common
type seems to indicate that all the higher groups are descended from a
single stem.
Considering that the larvæ of comparatively few groups have persisted,
no conclusions as to affinities can be drawn from the absence of a
larva in any group; and the presence in two groups of a common larval
form may be taken as proving a common descent, but does not
necessarily shew any close affinity.
There is every reason to believe that the types with a Trochosphere
larva, viz. the Rotifera, the Mollusca, the Chætopoda, the Gephyrea,
and the Polyzoa, are descended from a common ancestral form; and it is
also fairly certain there was a remote ancestor common to these forms
and to the Platyelminthes. A general affinity of the Brachiopoda with
the Chætopoda is more than probable. All these types, together with
various other types which are nearly related to them, but have not
preserved an early larval form, are descended from a bilateral
ancestor. The Echinodermata, on the other hand, are probably directly
descended from a radial ancestor, and have more or less completely
retained their radial symmetry. How far Actinotrocha[147] is related
to the Echinoderm larvæ cannot be settled. Its characters may possibly
be secondary, like those of the mesotrochal larvæ of Chætopods, or
they may be due to its having branched off very early from the stock
common to the whole of the forms above the Coelenterata. The position
of Tornaria is still more obscure. It is difficult, in the face of the
peculiar water-vascular vesicle with a dorsal pore, to avoid the
conclusion that it has some affinities with the Echinoderm larvæ. Such
affinities would seem, on the lines of speculation adopted in this
section, to prove that its affinities to the Trochosphere, striking as
they appear to be, are secondary and adaptive. From this conclusion,
if justified, it would follow that the Echinodermata and Enteropneusta
have a remote ancestor in common, but not that the two groups are in
any other way related.
[147] It is quite possible that Phoronis is in no way related to
the other Gephyrea.
General conclusions and summary. Starting from the demonstrated fact
that the larval forms of a number of widely separated types above the
Coelenterata have certain characters in common, it has been
_provisionally_ assumed that the characters have been inherited from a
common ancestor; and an attempt has been made to determine (1) the
characters of the prototype of all these larvæ, and (2) the mutual
relations of the larval forms in question. This attempt started with
certain more or less plausible suggestions, the truth of which can
only be tested by the coherence of the results which follow from them,
and their capacity to explain all the facts.
The results arrived at may be summarised as follows:
1. The larval forms above the Coelenterata may be divided into six
groups enumerated on pages 370 to 373.
2. The prototype of all these groups was an organism something like a
Medusa, with a radial symmetry. The mouth was placed in the centre of
a flattened ventral surface. The aboral surface was dome-shaped. Round
the edge of the oral surface was a ciliated ring, and probably a
nervous ring provided with sense organs. The alimentary canal was
prolonged into two or more diverticula, and there was no anus.
3. The bilaterally symmetrical types were derived from this larval
form by the larva becoming oval, and the region in front of the mouth
forming a præoral lobe, and that behind the mouth growing out to form
the trunk. The aboral dome became the dorsal surface.
On the establishment of a bilateral symmetry the anterior part of the
nervous ring gave rise (?) to the supraoesophageal ganglia, and the
optic organs connected with them; while the posterior part of the
nerve-ring formed (?) the ventral nerve-cords. The body cavity was
developed from two of the primitive alimentary diverticula.
The usual view that radiate forms have become bilateral by the
elongation of the aboral dome into the trunk is probably erroneous.
4. Pilidium is the larval form which most nearly reproduces the
characters of the larval prototype in the course of its conversion
into a bilateral form.
5. The Trochosphere is a completely differentiated bilateral form, in
which an anus has become developed. The præoral ciliated ring of the
Trochosphere is probably directly derived from the ciliated ring of
Pilidium, which is itself the original ring of the prototype of all
these larval forms.
6. Echinoderm larvæ, in the absence of a nerve-ganglion or special
organs of sense on the præoral lobe, and in the presence of alimentary
diverticula, which give rise to the body cavity, retain some
characters of the prototype larva which have been lost in Pilidium.
The ciliated ring of Echinoderm larvæ is probably derived directly
from that of the prototype by the formation of an anus on the dorsal
side of the ring. The anus was very probably originally situated at
the aboral apex.
Adult Echinoderms have probably retained the radial symmetry of the
forms from which they are descended, their nervous ring being directly
derived from the circular nervous ring of their ancestors. They have
not, as is usually supposed, secondarily acquired their radial
symmetry. The bilateral symmetry of the larva is, on this view,
secondary, like that of so many Coelenterate larvæ.
7. The points of similarity between Tornaria and (1) the Trochosphere
and (2) the Echinoderm larvæ are probably adaptive in the one case or
the other; and, while there is no difficulty in believing that those
to the Trochosphere are adaptive, the presence of a water-vascular
vesicle with a dorsal pore renders probable a real affinity with
Echinoderm larvæ.
8. It is not possible in the present state of our knowledge to decide
how far the resemblances between Actinotrocha and Echinoderm larvæ are
adaptive or primary.
BIBLIOGRAPHY.
(257) Allen Thomson. _British Association Address_, 1877.
(258) A. Agassiz. "Embryology of the Ctenophoræ." _Mem. Amer. Acad. of
Arts and Sciences_, Vol. X. 1874.
(259) K. E. von Baer. _Ueb. Entwicklungsgeschichte d. Thiere._
Königsberg, 1828-1837.
(260) F. M. Balfour. "A Comparison of the Early Stages in the
Development of Vertebrates." _Quart. Journ. of Micr. Sci._, Vol. XV.
1875.
(261) C. Claus. _Die Typenlehre u. E. Haeckel's sg. Gastræa-theorie._
Wien, 1874.
(262) C. Claus. _Grundzüge d. Zoologie._ Marburg und Leipzig, 1879.
(263) A. Dohrn. _Der Ursprung d. Wirbelthiere u. d. Princip des
Functionswechsels._ Leipzig, 1875.
(264) C. Gegenbaur. _Grundriss d. vergleichenden Anatomie._ Leipzig,
1878. _Vide_ also Translation. _Elements of Comparative Anatomy._
Macmillan & Co., 1878.
(265) A. Götte. _Entwicklungsgeschichte d. Unke._ Leipzig, 1874.
(266) E. Haeckel. _Studien z. Gastræa-theorie_, Jena, 1897; and also
_Jenaische Zeitschrift_, Vols. VIII. and IX. 1874-5.
(267) E. Haeckel. _Schöpfungsgeschichte._ Leipzig. _Vide_ also
Translation, _The History of Creation_. King & Co., London, 1878.
(268) E. Haeckel. _Anthropogenie._ Leipzig. _Vide_ also Translation,
_Anthropogeny_. Kegan Paul & Co., London, 1878.
(269) B. Hatschek. "Studien üb. Entwicklungsgeschichte d. Anneliden."
_Arbeit. a. d. zool. Instit. d. Univer. Wien._ 1878.
(270) O. and R. Hertwig. "Die Actinien." _Jenaische Zeitschrift_,
Vols. XIII. and XIV. 1879.
(271) O. and R. Hertwig. _Die Coelomtheorie._ Jena, 1881[148].
(272) O. Hertwig. _Die Chætognathen._ Jena, 1880.
(273) R. Hertwig. _Ueb. d. Bau d. Ctenophoren._ Jena, 1880.
(274) T. H. Huxley. _The Anatomy of Invertebrated Animals._ Churchill,
1877.
(274*) T. H. Huxley. "On the Classification of the Animal Kingdom."
_Quart. J. of Micr. Science_, Vol. XV. 1875.
(275) N. Kleinenberg. _Hydra, eine
anatomisch-entwicklungsgeschichtliche Untersuchung._ Leipzig, 1872.
(276) A. Kölliker. _Entwicklungsgeschichte d. Menschen u. d. höh.
Thiere._ Leipzig, 1879.
(277) A. Kowalevsky. "Embryologische Studien an Würmern u.
Arthropoden." _Mém. Acad. Pétersbourg_, Series VII. Vol. XVI. 1871.
(278) E. R. Lankester. "On the Germinal Layers of the Embryo as the
Basis of the Genealogical Classification of Animals." _Ann. and Mag.
of Nat. Hist._ 1873.
(279) E. R. Lankester. "Notes on Embryology and Classification."
_Quart. Journ. of Micr. Sci._, Vol. XVII. 1877.
(280) E. Metschnikoff. "Zur Entwicklungsgeschichte d. Kalkschwämme."
_Zeit. f. wiss. Zool._, Vol. XXIV. 1874.
(281) E. Metschnikoff. "Spongiologische Studien." _Zeit. f. wiss.
Zool._, Vol. XXXII. 1879.
(282) A. S. P. Packard. _Life Histories of Animals, including Man, or
Outlines of Comparative Embryology._ Holt and Co., New York, 1876.
(283) C. Rabl. "Ueb. d. Entwick. d. Malermuschel." _Jenaische
Zeitsch._, Vol. X. 1876.
(284) C. Rabl. "Ueb. d. Entwicklung. d. Tellerschnecke (Planorbis)."
_Morph. Jahrbuch_, Vol. V. 1879.
(285) H. Rathke. _Abhandlungen z. Bildung und Entwicklungsgesch. d.
Menschen u. d. Thiere._ Leipzig, 1833.
(286) H. Rathke. _Ueber die Bildung u. Entwicklungs. d. Flusskrebses._
Leipzig, 1829.
(287) R. Remak. _Untersuch. üb. d. Entwick. d. Wirbelthiere._ Berlin,
1855.
(288) Salensky. "Bemerkungen üb. Haeckels Gastræa-theorie." _Archiv.
f. Naturgeschichte_, 1874.
(289) E. Schäfer. "Some Teachings of Development." _Quart. Journ. of
Micr. Science_, Vol. XX. 1880.
(290) C. Semper. "Die Verwandtschaftbeziehungen d. gegliederten
Thiere." _Arbeiten a. d. zool.-zoot. Instit. Würzburg_, Vol. III.
1876-7.
[148] This important memoir only came into my hands after this
chapter was already in type.
PART II.
_ORGANOGENY._
PART II.
ORGANOGENY.
INTRODUCTION.
Our knowledge of the development of the organs in most of the
Invertebrate groups is so meagre that it would not be profitable to
attempt to treat systematically the organogeny of the whole animal
kingdom.
For this reason the plan adopted in this section of the work has been
to treat somewhat fully the organogeny of the Chordata, which is
comparatively well known; and merely to indicate a few salient facts
with reference to the organogeny of other groups. In the case of the
nervous system, and of some other organs which especially lend
themselves to this treatment, such as the organs of special sense and
the excretory system, a wider view of the subject has been taken; and
certain general principles underlying the development of other organs
have also been noticed.
The classification of the organs is a matter of some difficulty.
Considering the character of this treatise it seemed desirable to
arrange the organs according to the layers from which they are
developed. The compound nature of many organs, _e.g._ the eye and ear,
renders it, however, impossible to carry out consistently such a mode
of treatment. I have accordingly adopted a rough classification of the
organs according to the layers, dropping the principle where
convenient, as, for instance, in the case of the stomodæum and
proctodæum.
The organs which may be regarded as mainly derived from the epiblast
are (1) the skin; (2) the nervous system; (3) the organs of special
sense.
Those from the mesoblast are (1) the general connective tissue and
skeleton; (2) the vascular system and body cavity; (3) the muscular
system; (4) the urinogenital system.
Those from the hypoblast are the alimentary tract and its derivates;
with which the stomodæum and proctodæum and their respective derivates
are also dealt with.
BIBLIOGRAPHY.
_General works dealing with the development of the organs of the
Chordata._
(291) K. E. von Baer. _Ueber Entwicklungsgeschichte d. Thiere._
Königsberg, 1828-1837.
(292) F. M. Balfour. _A Monograph on the development of Elasmobranch
Fishes._ London, 1878.
(293) Th. C. W. Bischoff. _Entwicklungsgesch. d. Säugethiere U. d.
Menschen._ Leipzig, 1842.
(294) C. Gegenbaur. _Grundriss d. vergleichenden Anatomie._ Leipzig,
1878. _Vide_ also English translation, _Elements of Comp. Anatomy_.
London, 1878.
(295) M. Foster and F. M. Balfour. _The Elements of Embryology._ Part
I. London, 1874.
(296) Alex. Götte. _Entwicklungsgeschichte d. Unke._ Leipzig, 1875.
(297) W. His. _Untersuch. üb. d. erste Anlage d. Wirbelthierleibes._
Leipzig, 1868.
(298) A. Kölliker. _Entwicklungsgeschichte d. Menschen u. der höheren
Thiere._ Leipzig, 1879.
(299) H. Rathke. _Abhandlungen ü. Bildung und Entwicklungsgeschichte
d. Menschen u. d. Thiere._ Leipzig, 1838.
(300) H. Rathke. _Entwicklungs. d. Natter._ Königsberg, 1839.
(301) H. Rathke. _Entwicklungs. d. Wirbelthiere._ Leipzig, 1861.
(302) R. Remak. _Untersuchungen üb. d. Entwicklung d. Wirbelthiere._
Berlin, 1850-1855.
(303) S. L. Schenk. _Lehrbuch d. vergleich. Embryologie d.
Wirbelthiere._ Wien, 1874.