CONCLUDING REMARKS ON HETEROSTYLED PLANTS.
The essential character of heterostyled plants.
Summary of the differences in fertility between legitimately and illegitimately
fertilised plants.
Diameter of the pollen-grains, size of anthers and structure of stigma in the
different forms.
Affinities of the genera which include heterostyled species.
Nature of the advantages derived from heterostylism.
The means by which plants became heterostyled.
Transmission of form.
Equal-styled varieties of heterostyled plants.
Final remarks.
In the foregoing chapters all the heterostyled plants known to me have been more
or less fully described. Several other cases have been indicated, especially by
Professor Asa Gray and Kuhn, in which the individuals of the same species differ
in the length of their stamens and pistils (6/1. Asa Gray ‘American Journal of
Science’ 1865 page 101 and elsewhere as already referred to. Kuhn ‘Botanische
Zeitung’ 1867 page 67.); but as I have been often deceived by this character
taken alone, it seems to me the more prudent course not to rank any species as
heterostyled, unless we have evidence of more important differences between the
forms, as in the diameter of the pollen-grains, or in the structure of the
stigma. The individuals of many ordinary hermaphrodite plants habitually
fertilise one another, owing to their male and female organs being mature at
different periods, or to the structure of the parts, or to self-sterility, etc.;
and so it is with many hermaphrodite animals, for instance, land-snails or
earth-worms; but in all these cases any one individual can fully fertilise or be
fertilised by any other individual of the same species. This is not so with
heterostyled plants: a long-styled, mid-styled or short-styled plant cannot
fully fertilise or be fertilised by any other individual, but only by one
belonging to another form. Thus the essential character of plants belonging to
the heterostyled class is that the individuals are divided into two or three
bodies, like the males and females of dioecious plants or of the higher animals,
which exist in approximately equal numbers and are adapted for reciprocal
fertilisation. The existence, therefore, of two or three bodies of individuals,
differing from one another in the above more important characteristics, offers
by itself good evidence that the species is heterostyled. But absolutely
conclusive evidence can be derived only from experiments, and by finding that
pollen must be applied from the one form to the other in order to ensure
complete fertility.
In order to show how much more fertile each form is when legitimately fertilised
with pollen from the other form (or in the case of trimorphic species, with the
proper pollen from one of the two other forms) than when illegitimately
fertilised with its own-form pollen, I will append Table 6.33 giving a summary
of the results in all the cases hitherto ascertained. The fertility of the
unions may be judged by two standards, namely, by the proportion of flowers
which, when fertilised in the two methods, yield capsules, and by the average
number of seeds per capsule. When there is a dash in the left hand column
opposite to the name of the species, the proportion of the flowers which yielded
capsules was not recorded.
TABLE 6.33. Fertility of the legitimate unions taken together, compared with
that of the illegitimate unions together. The fertility of the legitimate
unions, as judged by both standards, is taken as 100.
Column 1: Name of species.
Column 2: Illegitimate unions : proportional number of flowers which produced
capsules.
Column 3: Illegitimate unions : average number of seeds per capsule.
Primula veris : 69 : 65.
Primula elatior : 27 : 75.
Primula vulgaris : 60 : 54.
Primula Sinensis : 84 : 63.
Primula Sinensis (second trial) : 0 : 53.
Primula Sinensis (Hildebrand) : 100 : 42.
Primula auricula (Scott) : 80 : 15.
Primula Sikkimensis (Scott) : 95 : 31.
Primula cortusoides (Scott) : 74 : 66.
Primula involucrata (Scott) : 72 : 48.
Primula farinosa (Scott) : 71 : 44.
Average of the nine species of Primula : 88.4 : 69.
Hottonia palustris (H. Muller) : - : 61.
Linum grandiflorum (the difference probably is much greater) : - : 69.
Linum perenne : - : 20.
Linum perenne (Hildebrand) : 0 : 0.
Pulmonaria officinalis (German stock, Hildebrand) : 0 : 0.
Pulmonaria angustifolia : 35 : 32.
Mitchella repens : 20 : 47.
Borreria, Brazilian sp. : - : 0.
Polygonum fagopyrum : - : 46.
Lythrum salicaria : 33 : 46.
Oxalis Valdiviana (Hildebrand) : 2 : 34.
Oxalis Regnelli : 0 : 0.
Oxalis speciosa : 15 : 49.
The two or three forms of the same heterostyled species do not differ from one
another in general habit or foliage, as sometimes, though rarely, happens with
the two sexes of dioecious plants. Nor does the calyx differ, but the corolla
sometimes differs slightly in shape, owing to the different position of the
anthers. In Borreria the hairs within the tube of the corolla are differently
situated in the long-styled and short-styled forms. In Pulmonaria there is a
slight difference in the size of the corolla, and in Pontederia in its colour.
In the reproductive organs the differences are much greater and more important.
In the one form the stamens may be all of the same length, and in the other
graduated in length, or alternately longer and shorter. The filaments may differ
in colour and thickness, and are sometimes nearly thrice as long in the one form
as in the other. They adhere also for very different proportional lengths to the
corolla. The anthers sometimes differ much in size in the two forms. Owing to
the rotation of the filaments, the anthers, when mature, dehisce towards the
circumference of the flower in one form of Faramea, and towards the centre in
the other form. The pollen-grains sometimes differ conspicuously in colour, and
often to an extraordinary degree in diameter. They differ also somewhat in
shape, and apparently in their contents, as they are unequally opaque. In the
short-styled form of Faramea the pollen-grains are covered with sharp points, so
as to cohere readily together or to an insect; whilst the smaller grains of the
long-styled form are quite smooth.
With respect to the pistil, the style may be almost thrice as long in the one
form as in the other. In Oxalis it sometimes differs in hairiness in the three
forms. In Linum the pistils either diverge and pass out between the filaments,
or stand nearly upright and parallel to them. The stigmas in the two forms often
differ much in size and shape, and more especially in the length and thickness
of their papillae; so that the surface may be rough or quite smooth. Owing to
the rotation of the styles, the papillose surface of the stigma is turned
outwards in one form of Linum perenne, and inwards in the other form. In flowers
of the same age of Primula veris the ovules are larger in the long-styled than
in the short-styled form. The seeds produced by the two or three forms often
differ in number, and sometimes in size and weight; thus, five seeds from the
long-styled form of Lythrum salicaria equal in weight six from the mid-styled
and seven from the short-styled form. Lastly, short-styled plants of Pulmonaria
officinalis bear a larger number of flowers, and these set a larger proportional
number of fruit, which however yield a lower average number of seed, than the
long-styled plants. With heterostyled plants we thus see in how many and in what
important characters the forms of the same undoubted species often differ from
one another--characters which with ordinary plants would be amply sufficient to
distinguish species of the same genus.
As the pollen-grains of ordinary species belonging to the same genus generally
resemble one another closely in all respects, it is worth while to show, in
Table 6.34, the difference in diameter between the grains from the two or three
forms of the same heterostyled species in the forty-three cases in which this
was ascertained. But it should be observed that some of the following
measurements are only approximately accurate, as only a few grains were
measured. In several cases, also, the grains had been dried and were then soaked
in water. Whenever they were of an elongated shape their longer diameters were
measured. The grains from the short-styled plants are invariably larger than
those from the long-styled, whenever there is any difference between them. The
diameter of the former is represented in the table by the number 100.
TABLE 6.34. Relative diameter of the pollen-grains from the forms of the same
heterostyled species; those from the short-styled form being represented by 100.
DIMORPHIC SPECIES.
Column 1: Name of species.
Column 2: From the long-styled form : relative diameter.
Primula veris : 67.
Primula vulgaris : 71.
Primula Sinensis (Hildebrand) : 57.
Primula auricula : 71.
Hottonia palustris (H. Muller) : 61.
Hottonia palustris (self) : 64.
Linum grandiflorum : 100.
Linum perenne (diameter variable) : 100 (?).
Linum flavum : 100.
Pulmonaria officinalis : 78.
Pulmonaria angustifolia : 91.
Polygonum fagopyrum : 82.
Leucosmia Burnettiana : 99.
Aegiphila elata : 62.
Menyanthes trifoliata : 84.
Limnanthemum Indicum : 100.
Villarsia (sp.?) : 75.
Forsythia suspensa : 94.
Cordia (sp.?) : 100.
Gilia pulchella : 100.
Gilia micrantha : 81.
Sethia acuminata : 83.
Erythroxylum (sp.?) : 93.
Cratoxylon formosum : 86.
Mitchella repens, pollen-grains of the long-styled a little smaller.
Borreria (sp.?) : 92.
Faramea (sp.?) : 67.
Suteria (sp.?) (Fritz Muller) : 75.
Houstonia coerulea : 72.
Oldenlandia (sp.?) : 78.
Hedyotis (sp.?) : 88.
Coccocypselum (sp.?) (Fritz Muller) : 100.
Lipostoma (sp.?) : 80.
Cinchona micrantha : 91.
TRIMORPHIC SPECIES.
Column 1: Name of species.
Column 2: Ratio expressing the extreme differences in diameter of the pollen-
grains from the two sets of anthers in the three forms.
Lythrum salicaria : 60.
Nesaea verticillata : 65.
Oxalis Valdiviana (Hildebrand) : 71.
Oxalis Regnelli : 78.
Oxalis speciosa : 69.
Oxalis sensitiva : 84.
Pontederia (sp.?) : 55.
Column 1: Name of species.
Column 2: Ratio between the diameters of the pollen-grains of the two sets of
anthers in the same form.
Oxalis rosea, long-styled form (Hildebrand) : 83.
Oxalis compressa, short-styled form : 83.
Pontederia (sp.?) short-styled form : 87.
Pontederia other sp. mid-styled form : 86.
We here see that, with seven or eight exceptions out of the forty-three cases,
the pollen-grains from one form are larger than those from the other form of the
same species. The extreme difference is as 100 to 55; and we should bear in mind
that in the case of spheres differing to this degree in diameter, their contents
differ in the ratio of six to one. With all the species in which the grains
differ in diameter, there is no exception to the rule that those from the
anthers of the short-styled form, the tubes of which have to penetrate the
longer pistil of the long-styled form, are larger than the grains from the other
form. This curious relation led Delpino (as it formerly did me) to believe that
the larger size of the grains in the short-styled flowers is connected with the
greater supply of matter needed for the development of their longer tubes. (6/2.
‘Sull’ Opera, la Distribuzione dei Sessi nelle Piante’ etc 1867 page 17.) But
the case of Linum, in which the grains of the two forms are of equal size,
whilst the pistil of the one is about twice as long as that of the other, made
me from the first feel very doubtful with respect to this view. My doubts have
since been strengthened by the cases of Limnanthemum and Coccocypselum, in which
the grains are of equal size in the two forms; whilst in the former genus the
pistil is nearly thrice and in the latter twice as long as in the other form. In
those species in which the grains are of unequal size in the two forms, there is
no close relationship between the degree of their inequality and that of their
pistils. Thus in Pulmonaria officinalis and in Erythroxylum the pistil in the
long-styled form is about twice the length of that in the other form, whilst in
the former species the pollen-grains are as 100 to 78, and in the latter as 100
to 93 in diameter. In the two forms of Suteria the pistil differs but little in
length, whilst the pollen-grains are as 100 to 75 in diameter. These cases seem
to prove that the difference in size between the grains in the two forms is not
determined by the length of the pistil, down which the tubes have to grow. That
with plants in general there is no close relationship between the size of the
pollen-grains and the length of the pistil is manifest: for instance, I found
that the distended grains of Datura arborea were .00243 of an inch in diameter,
and the pistil no less than 9.25 inches in length; now the pistil in the small
flowers of Polygonum fagopyrum is very short, yet the larger pollen-grains from
the short-styled plants had exactly the same diameter as those from the Datura,
with its enormously elongated pistil.
Notwithstanding these several considerations, it is difficult quite to give up
the belief that the pollen-grains from the longer stamens of heterostyled plants
have become larger in order to allow of the development of longer tubes; and the
foregoing opposing facts may possibly be reconciled in the following manner. The
tubes are at first developed from matter contained within the grains, for they
are sometimes exserted to a considerable length, before the grains have touched
the stigma; but botanists believe that they afterwards draw nourishment from the
conducting tissue of the pistil. It is hardly possible to doubt that this must
occur in such cases as that of the Datura, in which the tubes have to grow down
the whole length of the pistil, and therefore to a length equalling 3,806 times
the diameter of the grains (namely, .00243 of an inch) from which they are
protruded. I may here remark that I have seen the pollen-grains of a willow,
immersed in a very weak solution of honey, protrude their tubes, in the course
of twelve hours, to a length thirteen times as great as the diameter of the
grains. Now if we suppose that the tubes in some heterostyled species are
developed wholly or almost wholly from matter contained within the grains, while
in other species from matter yielded by the pistil, we can see that in the
former case it would be necessary that the grains of the two forms should differ
in size relatively to the length of the pistil which the tubes have to
penetrate, but that in the latter case it would not be necessary that the grains
should thus differ. Whether this explanation can be considered satisfactory must
remain at present doubtful.
There is another remarkable difference between the forms of several heterostyled
species, namely in the anthers of the short-styled flowers, which contain the
larger pollen-grains, being longer than those of the long-styled flowers. This
is the case with Hottonia palustris in the ratio of 100 to 83. With Limnanthemum
Indicum the ratio is as 100 to 70. With the allied Menyanthes the anthers of the
short-styled form are a little and with Villarsia conspicuously larger than
those of the long-styled. With Pulmonaria angustifolia they vary much in size,
but from an average of seven measurements of each kind the ratio is as 100 to
91. In six genera of the Rubiaceae there is a similar difference, either
slightly or well marked. Lastly, in the trimorphic Pontederia the ratio is 100
to 88; the anthers from the longest stamens in the short-styled form being
compared with those from the shortest stamens in the long-styled form. On the
other hand, there is a similar and well-marked difference in the length of the
stamens in the two forms of Forsythia suspensa and of Linum flavum; but in these
two cases the anthers of the short-styled flowers are shorter than those of the
long-styled. The relative size of the anthers was not particularly attended to
in the two forms of the other heterostyled plants, but I believe that they are
generally equal, as is certainly the case with those of the common primrose and
cowslip.
The pistil differs in length in the two forms of every heterostyled plant, and
although a similar difference is very general with the stamens, yet in the two
forms of Linum grandiflorum and of Cordia they are equal. There can hardly be a
doubt that the relative length of these organs is an adaptation for the safe
transportal by insects of the pollen from the one form to the other. The
exceptional cases in which these organs do not stand exactly on a level in the
two forms may probably be explained by the manner in which the flowers are
visited. With most of the species, if there is any difference in the size of the
stigma of the two forms, that of the long-styled, whatever its shape may be, is
larger than that of the short-styled. But here again there are some exceptions
to the rule, for in the short-styled form of Leucosmia Burnettiana the stigmas
are longer and much narrower than those of the long-styled; the ratio between
the lengths of the stigmas in the two forms being 100 to 60. In the three
Rubiaceous genera, Faramea, Houstonia and Oldenlandia, the stigmas of the short-
styled form are likewise somewhat longer and narrower; and in the three forms of
Oxalis sensitiva the difference is strongly marked, for if the length of the two
stigmas of the long-styled pistil be taken as 100, it will be represented in the
mid- and short-styled forms by the numbers 141 and 164. As in all these cases
the stigmas of the short-styled pistil are seated low down within a more or less
tubular corolla, it is probable that they are better fitted by being long and
narrow for brushing the pollen off the inserted proboscis of an insect.
With many heterostyled plants the stigma differs in roughness in the two forms,
and when this is the case there is no known exception to the rule that the
papillae on the stigma of the long-styled form are longer and often thicker than
those on that of the short-styled. For instance, the papillae on the long-styled
stigma of Hottonia palustris are more than twice the length of those in the
other form. This holds good even in the case of Houstonia coerulea, in which the
stigmas are much shorter and stouter in the long-styled than in the short-styled
form, for the papillae on the former compared with those on the latter are as
100 to 58 in length. The length of the pistil in the long-styled form of Linum
grandiflorum varies much, and the stigmatic papillae vary in a corresponding
manner. From this fact I inferred at first that in all cases the difference in
length between the stigmatic papillae in the two forms was one merely of
correlated growth; but this can hardly be the true or general explanation, as
the shorter stigmas of the long-styled form of Houstonia have the longer
papillae. It is a more probable view that the papillae, which render the stigma
of the long-styled form of various species rough, serve to entangle effectually
the large-sized pollen-grains brought by insects from the short-styled form,
thus ensuring its legitimate fertilisation. This view is supported by the fact
that the pollen-grains from the two forms of eight species in Table 6.34 hardly
differ in diameter, and the papillae on their stigmas do not differ in length.
The species which are at present positively or almost positively known to be
heterostyled belong, as shown in Table 6.35, to 38 genera, widely distributed
throughout the world. These genera are included in fourteen Families, most of
which are very distinct from one another, for they belong to nine of the several
great Series, into which phanerogamic plants have been divided by Bentham and
Hooker.
TABLE 6.35. List of genera including heterostyled species.
DICOTYLEDONS.
HYPERICINEAE:
Cratoxylon.
ERYTHROXYLEAE:
Erythroxylum.
Sethia.
GERANIACEAE:
Linum.
Oxalis.
LYTHRACEAE:
Lythrum.
Neseae.
RUBIACEAE:
Cinchona.
Bouvardia.
Manettia.
Hedyotis.
Oldenlandia.
Houstonia.
Coccocypselum.
Lipostoma.
Knoxia.
Faramea.
Psychotria.
Rudgea.
Suteria.
Mitchella.
Diodia.
Borreria.
Spermacoce.
PRIMULACEAE:
Primula.
Hottonia.
Androsace.
OLEACEAE:
Forsythia.
GENTIANACEAE:
Menyanthes.
Limnanthemum.
Villarsia.
POLEMONIACEAE:
Gilia.
CORDIEAE:
Cordia.
BORAGINEAE:
Pulmonaria.
VERBENACEAE:
Aegiphila.
POLYGONEAE:
Polygonum.
THYMELEAE:
Thymelea.
MONOCOTYLEDONS.
PONTEDERIACEAE:
Pontederia.
In some of these families the heterostyled condition must have been acquired at
a very remote period. Thus the three closely allied genera, Menyanthes,
Limnanthemum, and Villarsia, inhabit respectively Europe, India, and South
America. Heterostyled species of Hedyotis are found in the temperate regions of
North and the tropical regions of South America. Trimorphic species of Oxalis
live on both sides of the Cordillera in South America and at the Cape of Good
Hope. In these and some other cases it is not probable that each species
acquired its heterostyled structure independently of its close allies. If they
did not do so, the three closely connected genera of the Menyantheae and the
several trimorphic species of Oxalis must have inherited their structure from a
common progenitor. But an immense lapse of time will have been necessary in all
such cases for the modified descendants of a common progenitor to have spread
from a single centre to such widely remote and separated areas. The family of
the Rubiaceae contains not far short of as many heterostyled genera as all the
other thirteen families together; and hereafter no doubt other Rubiaceous genera
will be found to be heterostyled, although a large majority are homostyled.
Several closely allied genera in this family probably owe their heterostyled
structure to descent in common; but as the genera thus characterised are
distributed in no less than eight of the tribes into which this family has been
divided by Bentham and Hooker, it is almost certain that several of them must
have become heterostyled independently of one another. What there is in the
constitution or structure of the members of this family which favours their
becoming heterostyled, I cannot conjecture. Some families of considerable size,
such as the Boragineae and Verbenaceae, include, as far as is at present known,
only a single heterostyled genus. Polygonum also is the sole heterostyled genus
in its family; and though it is a very large genus, no other species except P.
fagopyrum is thus characterised. We may suspect that it has become heterostyled
within a comparatively recent period, as it seems to be less strongly so in
function than the species in any other genus, for both forms are capable of
yielding a considerable number of spontaneously self-fertilised seeds. Polygonum
in possessing only a single heterostyled species is an extreme case; but every
other genus of considerable size which includes some such species likewise
contains homostyled species. Lythrum includes trimorphic, dimorphic, and
homostyled species.
Trees, bushes, and herbaceous plants, both large and small, bearing single
flowers or flowers in dense spikes or heads, have been rendered heterostyled. So
have plants which inhabit alpine and lowland sites, dry land, marshes and water.
(6/3. Out of the 38 genera known to include heterostyled species, about eight,
or 21 per cent, are more or less aquatic in their habits. I was at first struck
with this fact, for I was not then aware how large a proportion of ordinary
plants inhabit such stations. Heterostyled plants may be said in one sense to
have their sexes separated, as the forms must mutually fertilise one another.
Therefore it seemed worth while to ascertain what proportion of the genera in
the Linnean classes, Monoecia, Dioecia and Polygamia, contained species which
live “in water, marshes, bogs or watery places.” In Sir W.J. Hooker’s ‘British
Flora’ 4th edition 1838, these three Linnean classes include 40 genera, 17 of
which (i.e. 43 per cent) contain species inhabiting the just-specified stations.
So that 43 per cent of those British plants which have their sexes separated are
more or less aquatic in their habits, whereas only 21 per cent of heterostyled
plants have such habits. I may add that the hermaphrodite classes, from
Monandria to Gynandria inclusive, contain 447 genera, of which 113 are aquatic
in the above sense, or only 25 per cent. It thus appears, as far as can be
judged from such imperfect data, that there is some connection between the
separation of the sexes in plants and the watery nature of the sites which they
inhabit; but that this does not hold good with heterostyled species.)
When I first began to experimentise on heterostyled plants it was under the
impression that they were tending to become dioecious; but I was soon forced to
relinquish this notion, as the long-styled plants of Primula which, from
possessing a longer pistil, larger stigma, shorter stamens with smaller pollen-
grains, seemed to be the more feminine of the two forms, yielded fewer seeds
than the short-styled plants which appeared to be in the above respects the more
masculine of the two. Moreover, trimorphic plants evidently come under the same
category with dimorphic, and the former cannot be looked at as tending to become
dioecious. With Lythrum salicaria, however, we have the curious and unique case
of the mid-styled form being more feminine or less masculine in nature than the
other two forms. This is shown by the large number of seeds which it yields in
whatever manner it may be fertilised, and by its pollen (the grains of which are
of smaller size than those from the corresponding stamens in the other two
forms) when applied to the stigma of any form producing fewer seeds than the
normal number. If we suppose the process of deterioration of the male organs in
the mid-styled form to continue, the final result would be the production of a
female plant; and Lythrum salicaria would then consist of two heterostyled
hermaphrodites and a female. No such case is known to exist, but it is a
possible one, as hermaphrodite and female forms of the same species are by no
means rare. Although there is no reason to believe that heterostyled plants are
regularly becoming dioecious, yet they offer singular facilities, as will
hereafter be shown, for such conversion; and this appears occasionally to have
been effected.
We may feel sure that plants have been rendered heterostyled to ensure cross-
fertilisation, for we now know that a cross between the distinct individuals of
the same species is highly important for the vigour and fertility of the
offspring. The same end is gained by dichogamy or the maturation of the
reproductive elements of the same flower at different periods,--by
dioeciousness--self-sterility--the prepotency of pollen from another individual
over a plant’s own pollen,--and lastly, by the structure of the flower in
relation to the visits of insects. The wonderful diversity of the means for
gaining the same end in this case, and in many others, depends on the nature of
all the previous changes through which the species has passed, and on the more
or less complete inheritance of the successive adaptations of each part to the
surrounding conditions. Plants which are already well adapted by the structure
of their flowers for cross-fertilisation by the aid of insects often possess an
irregular corolla, which has been modelled in relation to their visits; and it
would have been of little or no use to such plants to have become heterostyled.
We can thus understand why it is that not a single species is heterostyled in
such great families as the Leguminosae, Labiatae, Scrophulariaceae, Orchideae,
etc., all of which have irregular flowers. Every known heterostyled plant,
however, depends on insects for its fertilisation, and not on the wind; so that
it is a rather surprising fact that only one genus, Pontederia, has a plainly
irregular corolla.
Why some species are adapted for cross-fertilisation, whilst others within the
same genus are not so, or if they once were, have since lost such adaptation and
in consequence are now usually self-fertilised, I have endeavoured elsewhere to
explain to a certain limited extent. (6/4. ‘The Effects of Cross and Self-
fertilisation’ 1876 page 441.) If it be further asked why some species have been
adapted for this end by being made heterostyled, rather than by any of the above
specified means, the answer probably lies in the manner in which heterostylism
originated,--a subject immediately to be discussed. Heterostyled species,
however, have an advantage over dichogamous species, as all the flowers on the
same heterostyled plant belong to the same form, so that when fertilised
legitimately by insects two distinct individuals are sure to intercross. On the
other hand, with dichogamous plants, early or late flowers on the same
individual may intercross; and a cross of this kind does hardly any or no good.
Whenever it is profitable to a species to produce a large number of seeds and
this obviously is a very common case, heterostyled will have an advantage over
dioecious plants, as all the individuals of the former, whilst only half of the
latter, that is the females, yield seeds. On the other hand, heterostyled plants
seem to have no advantage, as far as cross-fertilisation is concerned, over
those which are sterile with their own pollen. They lie indeed under a slight
disadvantage, for if two self-sterile plants grow near together and far removed
from all other plants of the same species, they will mutually and perfectly
fertilise one another, whilst this will not be the case with heterostyled
dimorphic plants, unless they chance to belong to opposite forms.
It may be added that species which are trimorphic have one slight advantage over
the dimorphic; for if only two individuals of a dimorphic species happen to grow
near together in an isolated spot, the chances are even that both will belong to
the same form, and in this case they will not produce the full number of
vigorous and fertile seedlings; all these, moreover, will tend strongly to
belong to the same form as their parents. On the other hand, if two plants of
the same trimorphic species happen to grow in an isolated spot, the chances are
two to one in favour of their not belonging to the same form; and in this case
they will legitimately fertilise one another, and yield the full complement of
vigorous offspring.
THE MEANS BY WHICH PLANTS MAY HAVE BEEN RENDERED HETEROSTYLED.
This is a very obscure subject, on which I can throw little light, but which is
worthy of discussion. It has been shown that heterostyled plants occur in
fourteen natural families, dispersed throughout the whole vegetable kingdom, and
that even within the family of the Rubiaceae they are dispersed in eight of the
tribes. We may therefore conclude that this structure has been acquired by
various plants independently of inheritance from a common progenitor, and that
it can be acquired without any great difficulty--that is, without any very
unusual combination of circumstances.
It is probable that the first step towards a species becoming heterostyled is
great variability in the length of the pistil and stamens, or of the pistil
alone. Such variations are not very rare: with Amsinckia spectabilis and Nolana
prostrata these organs differ so much in length in different individuals that,
until experimenting on them, I thought both species heterostyled. The stigma of
Gesneria pendulina sometimes protrudes far beyond, and is sometimes seated
beneath the anthers; so it is with Oxalis acetosella and various other plants. I
have also noticed an extraordinary amount of difference in the length of the
pistil in cultivated varieties of Primula veris and vulgaris.
As most plants are at least occasionally cross-fertilised by the aid of insects,
we may assume that this was the case with our supposed varying plant; but that
it would have been beneficial to it to have been more regularly cross-
fertilised. We should bear in mind how important an advantage it has been proved
to be to many plants, though in different degrees and ways, to be cross-
fertilised. It might well happen that our supposed species did not vary in
function in the right manner, so as to become either dichogamous or completely
self-sterile, or in structure so as to ensure cross-fertilisation. If it had
thus varied, it would never have been rendered heterostyled, as this state would
then have been superfluous. But the parent-species of our several existing
heterostyled plants may have been, and probably were (judging from their present
constitution) in some degree self-sterile; and this would have made regular
cross-fertilisation still more desirable.
Now let us take a highly varying species with most or all of the anthers
exserted in some individuals, and in others seated low down in the corolla; with
the stigma also varying in position in like manner. Insects which visited such
flowers would have different parts of their bodies dusted with pollen, and it
would be a mere chance whether this were left on the stigma of the next flower
which was visited. If all the anthers could have been placed on the same level
in all the plants, then abundant pollen would have adhered to the same part of
the body of the insects which frequented the flowers, and would afterwards have
been deposited without loss on the stigma, if it likewise stood on the same
unvarying level in all the flowers. But as the stamens and pistils are supposed
to have already varied much in length and to be still varying, it might well
happen that they could be reduced much more easily through natural selection
into two sets of different lengths in different individuals, than all to the
same length and level in all the individuals. We know from innumerable
instances, in which the two sexes and the young of the same species differ, that
there is no difficulty in two or more sets of individuals being formed which
inherit different characters. In our particular case the law of compensation or
balancement (which is admitted by many botanists) would tend to cause the pistil
to be reduced in those individuals in which the stamens were greatly developed,
and to be increased in length in those which had their stamens but little
developed.
Now if in our varying species the longer stamens were to be nearly equalised in
length in a considerable body of individuals, with the pistil more or less
reduced; and in another body, the shorter stamens to be similarly equalised,
with the pistil more or less increased in length, cross-fertilisation would be
secured with little loss of pollen; and this change would be so highly
beneficial to the species, that there is no difficulty in believing that it
could be effected through natural selection. Our plant would then make a close
approach in structure to a heterostyled dimorphic species; or to a trimorphic
species, if the stamens were reduced to two lengths in the same flower in
correspondence with that of the pistils in the other two forms. But we have not
as yet even touched on the chief difficulty in understanding how heterostyled
species could have originated. A completely self-sterile plant or a dichogamous
one can fertilise and be fertilised by any other individual of the same species;
whereas the essential character of a heterostyled plant is that an individual of
one form cannot fully fertilise or be fertilised by an individual of the same
form, but only by one belonging to another form.
H. Muller has suggested that ordinary or homostyled plants may have been
rendered heterostyled merely through the effects of habit. (6/5. ‘Die
Befruchtung der Blumen’ page 352.) Whenever pollen from one set of anthers is
habitually applied to a pistil of particular length in a varying species, he
believes that at last the possibility of fertilisation in any other manner will
be nearly or completely lost. He was led to this view by observing that Diptera
frequently carried pollen from the long-styled flowers of Hottonia to the stigma
of the same form, and that this illegitimate union was not nearly so sterile as
the corresponding union in other heterostyled species. But this conclusion is
directly opposed by some other cases, for instance by that of Linum
grandiflorum; for here the long-styled form is utterly barren with its own-form
pollen, although from the position of the anthers this pollen is invariably
applied to the stigma. It is obvious that with heterostyled dimorphic plants the
two female and the two male organs differ in power; for if the same kind of
pollen be placed on the stigmas of the two forms, and again if the two kinds of
pollen be placed on the stigmas of the same form, the results are in each case
widely different. Nor can we see how this differentiation of the two female and
two male organs could have been effected merely through each kind of pollen
being habitually placed on one of the two stigmas.
Another view seems at first sight probable, namely, that an incapacity to be
fertilised in certain ways has been specially acquired by heterostyled plants.
We may suppose that our varying species was somewhat sterile (as is often the
case) with pollen from its own stamens, whether these were long or short; and
that such sterility was transferred to all the individuals with pistils and
stamens of the same length, so that these became incapable of intercrossing
freely; but that such sterility was eliminated in the case of the individuals
which differed in the length of their pistils and stamens. It is, however,
incredible that so peculiar a form of mutual infertility should have been
specially acquired unless it were highly beneficial to the species; and although
it may be beneficial to an individual plant to be sterile with its own pollen,
cross-fertilisation being thus ensured, how can it be any advantage to a plant
to be sterile with half its brethren, that is, with all the individuals
belonging to the same form? Moreover, if the sterility of the unions between
plants of the same form had been a special acquirement, we might have expected
that the long-styled form fertilised by the long-styled would have been sterile
in the same degree as the short-styled fertilised by the short-styled; but this
is hardly ever the case. On the contrary, there is sometimes the widest
difference in this respect, as between the two illegitimate unions of Pulmonaria
angustifolia and of Hottonia palustris.
It is a more probable view that the male and female organs in two sets of
individuals have been by some means specially adapted for reciprocal action; and
that the sterility between the individuals of the same set or form is an
incidental and purposeless result. The meaning of the term “incidental” may be
illustrated by the greater or less difficulty in grafting or budding together
two plants belonging to distinct species; for as this capacity is quite
immaterial to the welfare of either, it cannot have been specially acquired, and
must be the incidental result of differences in their vegetative systems. But
how the sexual elements of heterostyled plants came to differ from what they
were whilst the species was homostyled, and how they became co-adapted in two
sets of individuals, are very obscure points. We know that in the two forms of
our existing heterostyled plants the pistil always differs, and the stamens
generally differ in length; so does the stigma in structure, the anthers in
size, and the pollen-grains in diameter. It appears, therefore, at first sight
probable that organs which differ in such important respects could act on one
another only in some manner for which they had been specially adapted. The
probability of this view is supported by the curious rule that the greater the
difference in length between the pistils and stamens of the trimorphic species
of Lythrum and Oxalis, the products of which are united for reproduction, by so
much the greater is the infertility of the union. The same rule applies to the
two illegitimate unions of some dimorphic species, namely, Primula vulgaris and
Pulmonaria angustifolia; but it entirely fails in other cases, as with Hottonia
palustris and Linum grandiflorum. We shall, however, best perceive the
difficulty of understanding the nature and origin of the co-adaptation between
the reproductive organs of the two forms of heterostyled plants, by considering
the case of Linum grandiflorum: the two forms of this plant differ exclusively,
as far as we can see, in the length of their pistils; in the long-styled form,
the stamens equal the pistil in length, but their pollen has no more effect on
it than so much inorganic dust; whilst this pollen fully fertilises the short
pistil of the other form. Now, it is scarcely credible that a mere difference in
the length of the pistil can make a wide difference in its capacity for being
fertilised. We can believe this the less because with some plants, for instance,
Amsinckia spectabilis, the pistil varies greatly in length without affecting the
fertility of the individuals which are intercrossed. So again I observed that
the same plants of Primula veris and vulgaris differed to an extraordinary
degree in the length of their pistils during successive seasons; nevertheless
they yielded during these seasons exactly the same average number of seeds when
left to fertilise themselves spontaneously under a net.
We must therefore look to the appearance of inner or hidden constitutional
differences between the individuals of a varying species, of such a nature that
the male element of one set is enabled to act efficiently only on the female
element of another set. We need not doubt about the possibility of variations in
the constitution of the reproductive system of a plant, for we know that some
species vary so as to be completely self-sterile or completely self-fertile,
either in an apparently spontaneous manner or from slightly changed conditions
of life. Gartner also has shown that the individual plants of the same species
vary in their sexual powers in such a manner that one will unite with a distinct
species much more readily than another. (6/6. Gartner ‘Bastarderzeugung im
Pflanzenreich’ 1849 page 165.) But what the nature of the inner constitutional
differences may be between the sets or forms of the same varying species, or
between distinct species, is quite unknown. It seems therefore probable that the
species which have become heterostyled at first varied so that two or three sets
of individuals were formed differing in the length of their pistils and stamens
and in other co-adapted characters, and that almost simultaneously their
reproductive powers became modified in such a manner that the sexual elements in
one set were adapted to act on the sexual elements of another set; and
consequently that these elements in the same set or form incidentally became
ill-adapted for mutual interaction, as in the case of distinct species. I have
elsewhere shown that the sterility of species when first crossed and of their
hybrid offspring must also be looked at as merely an incidental result,
following from the special co-adaptation of the sexual elements of the same
species. (6/7. ‘Origin of Species’ 6th edition page 247; ‘Variation of Animals
and Plants under Domestication’ 2nd edition volume 2 page 169; ‘The Effects of
Cross and Self-fertilisation’ page 463. It may be well here to remark that,
judging from the remarkable power with which abruptly changed conditions of life
act on the reproductive system of most organisms, it is probable that the close
adaptation of the male to the female elements in the two forms of the same
heterostyled species, or in all the individuals of the same ordinary species,
could be acquired only under long-continued nearly uniform conditions of life.)
We can thus understand the striking parallelism, which has been shown to exist
between the effects of illegitimately uniting heterostyled plants and of
crossing distinct species. The great difference in the degree of sterility
between the various heterostyled species when illegitimately fertilised, and
between the two forms of the same species when similarly fertilised, harmonises
well with the view that the result is an incidental one which follows from
changes gradually effected in their reproductive systems, in order that the
sexual elements of the distinct forms should act perfectly on one another.
TRANSMISSION OF THE TWO FORMS BY HETEROSTYLED PLANTS.
The transmission of the two forms by heterostyled plants, with respect to which
many facts were given in the last chapter, may perhaps be found hereafter to
throw some light on their manner of development. Hildebrand observed that
seedlings from the long-styled form of Primula Sinensis when fertilised with
pollen from the same form were mostly long-styled, and many analogous cases have
since been observed by me. All the known cases are given in Tables 6.36 and
6.37.
TABLE 6.36. Nature of the offspring from illegitimately fertilised dimorphic
plants.
Column 1: Species and form.
Column 2: Number of long-styled offspring.
Column 3: Number of short-styled offspring.
Primula veris. Long-styled form, fertilised by own-form pollen during five
successive generations : 156 : 6.
Primula veris. Short-styled form, fertilised by own-form pollen : 5 : 9.
Primula vulgaris. Long-styled form, fertilised by own-form pollen during two
successive generations : 69 : 0.
Primula auricula. Short-styled form, fertilised by own-form pollen, is said to
produce during successive generations offspring in about the following
proportions : 25 : 75.
Primula Sinensis. Long-styled form, fertilised by own-form pollen during two
successive generations : 52 : 0.
Primula Sinensis. Long-styled form, fertilised by own-form pollen (Hildebrand) :
14 : 3.
Primula Sinensis. Short-styled form, fertilised by own-form pollen: 1 : 24.
Pulmonaria officinalis. Long-styled form, fertilised by own-form pollen : 11 :
0.
Polygonum fagopyrum. Long-styled form, fertilised by own-form pollen : 45 : 4.
Polygonum fagopyrum. Short-styled form, fertilised by own-form pollen : 13 : 20.
TABLE 6.37. Nature of the offspring from illegitimately fertilised trimorphic
plants.
Column 1: Species and form.
Column 2: Number of long-styled offspring.
Column 3: Number of mid-styled offspring.
Column 4: Number of short-styled offspring.
Lythrum salicaria. Long-styled form, fertilised by own-form pollen : 56 : 0 : 0.
Lythrum salicaria. Short-styled form, fertilised by own-form pollen : 1 : 0 : 8.
Lythrum salicaria. Short-styled form, fertilised by pollen from mid-length
stamens of long-styled form : 4 : 0 : 8.
Lythrum salicaria. Mid-styled form, fertilised by own-form pollen : 1 : 3 : 0.
Lythrum salicaria. Mid-styled form, fertilised by pollen from shortest stamens
of long-styled form : 17 : 8 : 0.
Lythrum salicaria. Mid-styled form, fertilised by pollen from longest stamens of
short-styled form : 14 : 8 : 18.
Oxalis rosea. Long-styled form, fertilised during several generations by own-
form pollen, produced offspring in the ratio of : 100 : 0 : 0.
Oxalis hedysaroides. Mid-styled form, fertilised by own-form pollen : 0 : 17 :
0.
We see in these two tables that the offspring from a form illegitimately
fertilised with pollen from another plant of the same form belong, with a few
exceptions, to the same form as their parents. For instance, out of 162
seedlings from long-styled plants of Primula veris fertilised during five
generations in this manner, 156 were long-styled and only 6 short-styled. Of 69
seedlings from P. vulgaris similarly raised all were long-styled. So it was with
56 seedlings from the long-styled form of the trimorphic Lythrum salicaria, and
with numerous seedlings from the long-styled form of Oxalis rosea. The offspring
from the short-styled forms of dimorphic plants, and from both the mid-styled
and short-styled forms of trimorphic plants, fertilised with their own-form
pollen, likewise tend to belong to the same form as their parents, but not in so
marked a manner as in the case of the long-styled form. There are three cases in
Table 6.37, in which a form of Lythrum was fertilised illegitimately with pollen
from another form; and in two of these cases all the offspring belonged to the
same two forms as their parents, whilst in the third case they belonged to all
three forms.
The cases hitherto given relate to illegitimate unions, but Hildebrand, Fritz
Muller, and myself found that a very large proportion, or all of the offspring,
from a legitimate union between any two forms of the trimorphic species of
Oxalis belonged to the same two forms. A similar rule therefore holds good with
unions which are fully fertile, as with those of an illegitimate nature which
are more or less sterile. When some of the seedlings from a heterostyled plant
belong to a different form from that of its parents, Hildebrand accounts for the
fact by reversion. For instance, the long-styled parent-plant of Primula veris,
from which the 162 illegitimate seedlings in Table 6.36 were derived in the
course of five generations, was itself no doubt derived from the union of a
long-styled and a short-styled parent; and the 6 short-styled seedlings may be
attributed to reversion to their short-styled progenitor. But it is a surprising
fact in this case, and in other similar ones, that the number of the offspring
which thus reverted was not larger. The fact is rendered still more strange in
the particular instance of P. veris, for there was no reversion until four or
five generations of long-styled plants had been raised. It may be seen in both
tables that the long-styled form transmits its form much more faithfully than
does the short-styled, when both are fertilised with their own-form pollen; and
why this should be so it is difficult to conjecture, unless it be that the
aboriginal parent-form of most heterostyled species possessed a pistil which
exceeded its own stamens considerably in length. (6/8. It may be suspected that
this was the case with Primula, judging from the length of the pistil in several
allied genera (see Mr. J. Scott ‘Journal of the Linnean Society Botany’ volume 8
1864 page 85). Herr Breitenbach found many specimens of Primula elatior growing
in a state of nature with some flowers on the same plant long-styled, others
short-styled and others equal-styled; and the long-styled form greatly
preponderated in number; there being 61 of this form to 9 of the short-styled
and 15 of the equal-styled.) I will only add that in a state of nature any
single plant of a trimorphic species no doubt produces all three forms; and this
may be accounted for either by its several flowers being separately fertilised
by both the other forms, as Hildebrand supposes; or by pollen from both the
other forms being deposited by insects on the stigma of the same flower.
EQUAL-STYLED VARIETIES.
The tendency of the dimorphic species of Primula to produce equal-styled
varieties deserves notice. Cases of this kind have been observed, as shown in
the last chapter, in no less than six species, namely, P. veris, vulgaris,
Sinensis, auricula, farinosa, and elatior. In the case of P. veris, the stamens
resemble in length, position and size of their pollen-grains the stamens of the
short-styled form; whilst the pistil closely resembles that of the long-styled,
but as it varies much in length, one proper to the short-styled form appears to
have been elongated and to have assumed at the same time the functions of a
long-styled pistil. Consequently the flowers are capable of spontaneous self-
fertilisation of a legitimate nature and yield a full complement of seed, or
even more than the number produced by ordinary flowers legitimately fertilised.
With P. Sinensis, on the other hand, the stamens resemble in all respects the
shorter ones proper to the long-styled form, whilst the pistil makes a near
approach to that of the short-styled, but as it varies in length, it would
appear as if a long-styled pistil had been reduced in length and modified in
function. The flowers in this case as in the last are capable of spontaneous
legitimate fertilisation, and are rather more productive than ordinary flowers
legitimately fertilised. With P. auricula and farinosa the stamens resemble
those of the short-styled form in length, but those of the long-styled in the
size of their pollen-grains; the pistil also resembles that of the long-styled,
so that although the stamens and pistil are of nearly equal length, and
consequently pollen is spontaneously deposited on the stigma, yet the flowers
are not legitimately fertilised and yield only a very moderate supply of seed.
We thus see, firstly, that equal-styled varieties have originated in various
ways, and, secondly, that the combination of the two forms in the same flower
differs in completeness. With P. elatior some of the flowers on the same plant
have become equal-styled, instead of all of them as in the other species.
Mr. Scott has suggested that the equal-styled varieties arise through reversion
to the former homostyled condition of the genus. This view is supported by the
remarkable fidelity with which the equal-styled variation is transmitted after
it has once appeared. I have shown in Chapter 13 of my ‘Variation of Animals and
Plants under Domestication,’ that any cause which disturbs the constitution
tends to induce reversion, and it is chiefly the cultivated species of Primula
which become equal-styled. Illegitimate fertilisation, which is an abnormal
process, is likewise an exciting cause; and with illegitimately descended long-
styled plants of P. Sinensis, I have observed the first appearance and
subsequent stages of this variation. With some other plants of P. Sinensis of
similar parentage the flowers appeared to have reverted to their original wild
condition. Again, some hybrids between P. veris and vulgaris were strictly
equal-styled, and others made a near approach to this structure. All these facts
support the view that this variation results, at least in part, from reversion
to the original state of the genus, before the species had become heterostyled.
On the other hand, some considerations indicate, as previously remarked, that
the aboriginal parent-form of Primula had a pistil which exceeded the stamens in
length. The fertility of the equal-styled varieties has been somewhat modified,
being sometimes greater and sometimes less than that of a legitimate union.
Another view, however, may be taken with respect to the origin of the equal-
styled varieties, and their appearance may be compared with that of
hermaphrodites amongst animals which properly have their sexes separated; for
the two sexes are combined in a monstrous hermaphrodite in a somewhat similar
manner as the two sexual forms are combined in the same flower of an equal-
styled variety of a heterostyled species.
FINAL REMARKS.
The existence of plants which have been rendered heterostyled is a highly
remarkable phenomenon, as the two or three forms of the same undoubted species
differ not only in important points of structure, but in the nature of their
reproductive powers. As far as structure is concerned, the two sexes of many
animals and of some plants differ to an extreme degree; and in both kingdoms the
same species may consist of males, females, and hermaphrodites. Certain
hermaphrodite cirripedes are aided in their reproduction by a whole cluster of
what I have called complemental males, which differ wonderfully from the
ordinary hermaphrodite form. With ants we have males and females, and two or
three castes of sterile females or workers. With Termites there are, as Fritz
Muller has shown, both winged and wingless males and females, besides the
workers. But in none of these cases is there any reason to believe that the
several males or several females of the same species differ in their sexual
powers, except in the atrophied condition of the reproductive organs in the
workers of social insects. Many hermaphrodite animals must unite for
reproduction, but the necessity of such union apparently depends solely on their
structure. On the other hand, with heterostyled dimorphic species there are two
females and two sets of males, and with trimorphic species three females and
three sets of males, which differ essentially in their sexual powers. We shall,
perhaps, best perceive the complex and extraordinary nature of the marriage
arrangements of a trimorphic plant by the following illustration. Let us suppose
that the individuals of the same species of ant always lived in triple
communities; and that in one of these, a large-sized female (differing also in
other characters) lived with six middle-sized and six small-sized males; in the
second community a middle-sized female lived with six large- and six small-sized
males; and in the third, a small-sized female lived with six large- and six
middle-sized males. Each of these three females, though enabled to unite with
any male, would be nearly sterile with her own two sets of males, and likewise
with two other sets of males of the same size with her own which lived in the
other two communities; but she would be fully fertile when paired with a male of
her own size. Hence the thirty-six males, distributed by half-dozens in the
three communities, would be divided into three sets of a dozen each; and these
sets, as well as the three females, would differ from one another in their
reproductive powers in exactly the same manner as do the distinct species of the
same genus. But it is a still more remarkable fact that young ants raised from
any one of the three female ants, illegitimately fertilised by a male of a
different size would resemble in a whole series of relations the hybrid
offspring from a cross between two distinct species of ants. They would be
dwarfed in stature, and more or less, or even utterly barren. Naturalists are so
much accustomed to behold great diversities of structure associated with the two
sexes, that they feel no surprise at almost any amount of difference; but
differences in sexual nature have been thought to be the very touchstone of
specific distinction. We now see that such sexual differences--the greater or
less power of fertilising and being fertilised--may characterise the co-existing
individuals of the same species, in the same manner as they characterise and
have kept separate those groups of individuals, produced during the lapse of
ages, which we rank and denominate as distinct species.