DARWIN’S THEORY OF SEXUAL SELECTION.
Darwin seems to have felt the necessity of giving some other explanation
for the secondary sexual differences between the male and female than
that such differences were only a by-product or concomitant of sex
itself. His reason for searching further was probably a part of the
general point of view he had reached in regard to the utility of special
structures of animals, namely, that their presence finds its explanation
on the basis of utility. Believing as he did that most of the
adaptations of plants and animals have been built up by the accumulation
of small steps, it must have appeared to Darwin inconceivable that the
highly developed ornamentation exhibited in the secondary sexual
characters could have been simply the by-product of sex itself,
especially when the ornamentation may have been entirely absent in males
of closely related species. To-day we are not, I think, so oppressed
with the difficulties of the situation, for we have become familiar with
the fact that very slight genetic differences may cause very great
differences in the end-product. In a word, the problem seems less
formidable to us than it did to Darwin.
Darwin appealed to three processes to account for the facts: (1) to
natural selection between the members of the same sex; (2) to choice on
the part of the “other” sex; (3) to the “inheritance of use.” Since each
of these appeals to a different procedure, let us take them up
separately.
Competition of the males with each other for the female would, Darwin
said, lead to the survival of those males best endowed with organs of
offense and defense. The spurs of the cock are weapons dangerous for
other birds; the horns of the bull and those of deer are used for
offense and defense; the mane of the lion is a protection against the
teeth of other lions. It is true that these same weapons and shields
serve for attack and defense outside the species; but since the female
lacks them or has them less developed, they would not seem necessary for
survival of the individual against aggression from without. They have
developed, then, through competition within the species.
Several objections of greater or less weight have been urged against
Darwin’s interpretation. It has been pointed out that the combats within
the species are seldom fatal and that the defeated rival finds another
mate. If, as a rule, there are as many females as males within the
species and monogamy is the rule, all males will find partners sooner or
later, all may have offspring, and the offspring have equally good
chances of survival. Under these circumstances it is not to be expected
that the combat would be likely to lead to the production of males with
longer spurs or larger horns.
Darwin realized this difficulty and tried to meet it by another
assumption, viz, that the better endowed males would _also_ be more
likely to have more offspring. How could this be made probable? Darwin
suggested that the strongest males would be in position to mate with the
first females to reach maturity, and if these were more likely to have
offspring, either because of maternal endowments that made them also
more prolific or because the earlier broods would have a better chance
of getting food, etc., then the successful competitor would sooner or
later impress his advantages on the race.
At other times Darwin suggested that the exceptional vigor that led to
the greater development of the character in question would itself be of
value and through transmission to the offspring lead to advance in the
development of the other character in question. But here the argument
shifts to another field of inquiry and survival is ascribed to greater
vigor, while the secondary sexual character is carried along in its wake
as a sort of correlated effect.
It will be conceded, I think, that such pleading does not help the
argument, but exposes rather its inherent weaknesses. There is, however,
a line of defense that is permissible. If monogamy is not the rule, if
the male captures or attracts several females and keeps a harem, as do
the fur seals and walruses, or rules a herd as does the bull, or has a
flock as does the cock, or mates more frequently with random females
than do some other males, then the advantage of his more developed
weapon might lead to more offspring. If it could be shown that such
intraspecific weapons prevail more frequently within polygamous species,
a fair argument for natural selection might be made. I do not know
whether such a census has been taken as yet, but it is true, I think,
that in most polygamous groups we find weapons of offense very highly
developed. The fur seal has a harem and the male is greater in size, in
strength, and in the development of his tusks than is the female.
Similarly for the walrus. The bull drives away rival bulls from the herd
until through age or injury, or through the development of a better
fighter, he is replaced. If the better endowment is due to a genetic
factor, we should expect natural selection to keep the race at the
highest possible level that variation supplies material for. If, then,
we confine the application of natural selection to cases of this sort,
the explanation is as valid as is the theory in other fields. Such a
conclusion becomes weakened when an attempt is made to apply it to other
groups of animals in which it appears improbable that the secondary
sexual characters of the male have any obvious value as organs of
offense. There are families of beetles, for example, in which the
development of the horns of the male are as striking as are those of the
ram or the stag. The males of these beetles are not known to fight with
each other, nor are they polygamous. It may seem that we must look here
for some other explanation, which, if found, might suffice to cover
also the case of birds and mammals. In answer to this criticism it may
be argued that it is also possible that the other explanation when found
need not necessarily apply to the higher animals, where the laws of
combat may still give the true explanation. On the whole, I think that,
for our present purpose, it will suffice to state it is consistent with
the theory of natural selection to accept _provisionally_ this part of
Darwin’s theory for those species in the higher groups in which polygamy
holds, conceding, however, that even here it may have to be altered when
fuller knowledge is gained.
We are more concerned with that special feature of Darwin’s theory of
sexual selection that is applied to those cases where the characters are
supposed to owe their special development to selection by the
individuals of the opposite sex. It is assumed that the female _chooses_
the better endowed males, _because_ of the strong appeal he makes to her
sense-organs. Here we must employ perforce or for brevity’s sake the
terms used in human psychology, and run the risk at every turn of
imputing to other animals the emotions and acquired associations which
man himself utilizes. Even granting that other animals possess somewhat
similar emotions to ours, there still remains always the danger, in the
absence of real evidence, of imputing to them the particular emotion
that we call “feeling for beauty”; and the greater danger of imputing an
esthetic sense so highly developed that the choice falls in the long run
on the suitor better ornamented than his rivals.
OTHER THEORIES TO ACCOUNT FOR SECONDARY SEXUAL CHARACTERS.
Wallace has always been an opponent of Darwin’s theory of sexual
selection in so far as it is based on female choice. As already stated,
he believes that the difference between the plumage of the male and
female in birds is due to natural selection keeping down the
ornamentation and high coloration in the female, because these would be
expected to expose the female while sitting on the nest to the attacks
of enemies, more especially of hawks. In support of this view he points
to a long series of species which build exposed nests and in them the
female is plainly and inconspicuously colored, while he also points out
that in such birds as parrots, toucans, woodpeckers, hangnests, and
starlings, which nest in holes or have covered nests, the female is
often as highly colored as the male. It can not be denied that he makes
out rather a strong case in support of this view, despite the fact that
there are other birds, like the Baltimore oriole, that have covered
nests and in which the sexes are very markedly different.
Wallace tries to meet cases like the last one by assuming that the
covering keeps off the rain; but, if so, why are the sexes still so
different? In the case of other highly colored birds, such as jays,
magpies, hawks, and crows, Wallace believes that these birds are all
aggressive, hence can protect their nests if attacked. As a further
support of his view, Wallace points out that in the few cases where the
female is more highly colored than the male (as the dotterel, species of
phalarope, an Australian creeper) the male incubates the eggs.
Wallace’s suggestion still leaves unexplained the ornamentation of the
male, which he tries to account for as the direct result of the greater
vitality of the male. He tries to show that excessive ornaments and high
coloration develop especially in those parts of the body to which there
is an unusual supply of blood or where nerves and blood-vessels emerge
to go to the skin or to the muscles.
“If we have found a _vera causa_ for the origin of ornamental
appendages of birds and other animals in a surplus of vital energy,
leading to abnormal growths in those parts of the integument where
muscular and nervous action are greatest, the continuous
development of these appendages will result from the ordinary
action of natural selection in preserving the most healthy and
vigorous individuals, and the still further selective agency of
sexual struggle in giving to the very strongest and most energetic
the parentage of the next generation. And, as all the evidence goes
to show that, so far as female birds exercise any choice, it is for
‘the most vigorous, defiant, and mettlesome male,’ this form of
sexual selection will act in the same direction, and help to carry
on the process of plume development to its culmination. That
culmination will be reached when the excessive length or abundance
of the plumes begins to be injurious to the bearer of them; and it
may be this check to the further lengthening of the peacock’s train
that has led to the broadening of the feathers at the ends, and the
consequent production of the magnificent eye-spots which now form
its crowning ornament.
“The display of these plumes will result from the same causes which
led to their production. Just in proportion as the feathers
themselves increased in length and abundance, the skin-muscles
which serve to elevate them would increase also; and the nervous
development as well as the supply of blood to these parts being at
a maximum, the erection of the plumes would become a habit at all
periods of nervous or sexual excitement. The display of the plumes,
like the existence of the plumes themselves, would be the chief
external indication of the maturity and vigor of the male, and
would, therefore, be necessarily attractive to the female. We have,
thus, no reason for imputing to her any of those esthetic emotions
which are excited in us, by the beauty of form, color, and pattern
of these plumes; or the still more improbable esthetic tastes,
which would cause her to choose her mate on account of minute
differences in their forms, colors, or patterns.”
Wallace says, referring to the immense tuft of golden plumage in the
best known birds of paradise (_Paradisea apoda_ and _P. minor_) that
springs from a very small area on the side of the breast, that Mr. Frank
E. Beddard, who has kindly examined a specimen, says that “this area
lies upon the pectoral muscles, and near to the point where the fibers
of the muscle converge towards their attachment to the humerus. The
plumes arise, therefore, close to the most powerful muscle of the body,
and near to where the activities of that muscle would be at a maximum.
Furthermore, the area of attachment of the plumes is just above the
point where the arteries and nerves for the supply of the pectoral
muscles, and neighboring regions, leave the interior of the body. The
area of attachment of the plume is, also, as you say in your letter,
just above the junction of the coracoid and sternum.” “Ornamental plumes
of considerable size rise from the same part in many other species of
paradise birds, sometimes extending laterally in front, so as to form
breast shields. They also occur in many hummingbirds, and in some sun
birds and honey-suckers; and in all these cases there is a wonderful
amount of activity and rapid movement, indicating a surplus of vitality,
which is able to manifest itself in the development of these accessory
plumes.”[7]
There are two serious defects in such an attempt to explain the facts.
In the first place, it has been shown in several cases that have been
studied that it is not the lessened “vitality” of the female but the
suppression caused by the ovary that keeps down the development of the
full plumage in that sex. In the second place, the anatomical influences
appealed to are imaginary rather than real, for it is by no means
apparent that the local exits of blood-vessels and nerves to muscles are
at all correlated with the location of the ornamental parts, in the
skin. Even when larger blood-vessels run to the region of excessive
development of feather ornaments it may well be that they go there
because the ornaments in question use them for their nourishment; in
other words, Wallace puts the cart before the horse. The top of the
head, where crests so often develop, the throat coloration and throat
shields of hummingbirds and birds of paradise, the two long tail
feathers of several species of hummingbirds, etc., do not arise, so far
as known, from regions which are conspicuous for a rich supply of blood
and nerves. Wallace’s appeal to underlying organs such as muscles that
supposedly influence the special development of the feathers in the skin
above does not strike one as a fortunate appeal to physiological
principles.
Hudson, in his interesting book, “The Naturalist in La Plata,” has also
criticized Darwin’s theory of sexual selection. He has brought together
a considerable number of interesting observations that go to show that
the displays--dancing, singing, and combats--of males and females have
no relation to mating. Many of them involve birds already mated,
sometimes several males participating, sometimes males and females
together. Some of the tourneys he describes are more elaborate than the
mating instincts themselves, yet are not concerned with mating. He
attempts to explain them as overflow phenomena, _i. e._, as expressions
of the high vitality of the males, especially at this time. If he is
right, then elaborate exhibitions of these kinds have evolved that have
no special connection with mating. Are we called upon for a different
explanation for other differences that distinguish the sexes? One
example will suffice to bring out a curious emotional (?) display that,
elaborate as it is, has no apparent connection with mating (p. 269):
“The lapwing display, called by the natives its ‘dance’ or ‘serious
dance’--by which they mean square dance--requires three birds for
its performance, and is, so far as I know, unique in this respect.
The birds are so fond of it that they indulge in it all the year
round, and at frequent intervals during the day, also on moonlight
nights. If a person watches any two birds for some time--for they
live in pairs--he will see another lapwing, one of a neighboring
couple, rise up and fly to them, leaving his own mate to guard
their chosen ground; and instead of resenting this visit as an
unwarranted intrusion on their domain, as they would certainly
resent the approach of almost any other bird, they welcome it with
notes and signs of pleasure. Advancing to the visitor, they place
themselves behind it; then all three, keeping step, begin a rapid
march, uttering resonant drumming notes in time with their
movements; the notes of the pair behind being emitted in a stream,
like a drumroll, while the leader utters loud single notes at
regular intervals. The march ceases; the leader elevates his wings
and stands erect and motionless, still uttering loud notes; while
the other two, with puffed-out plumage and standing exactly
abreast, stoop forward and downward until the tips of their beaks
touch the ground, and sinking their rythmical voices to a murmur
remain for some time in this posture. The performance is then over
and the visitor goes back to his own ground and mate, to receive a
visitor himself later on.”[8]
Cunningham, who has brought together many interesting cases of secondary
sexual differences in his book on “Sexual Dimorphism in the Animal
Kingdom,” attempts to show that the development of the secondary sexual
characters of the males are due directly to the use of certain parts of
the body during courtship--the use of the parts leading to the
enlargement and excessive growth of the parts. The effects are believed
by him to be inherited, and he tries, furthermore, to show the way in
which such acquired characters could be inherited. He makes use of the
modern idea of hormones--substances that are elaborated in many organs
of the body, whose effects are often most conspicuously produced in
other parts of the body. He imagines these hormones to be collected in
the germ-cells and transmitted to the next generation, where their
presence contributes to the further development of the special region
(when it develops) that corresponds to the region in its parent in which
the hormone was made. His speculation meets in the first place with the
general objections inherent in Lamarck’s theory--objections so well
recognized to-day that I need not go over them here. His special appeal
to the hormone theory makes use of that theory in a way to which it was
never intended to be put, by assuming that an internal secretion formed
in one organ can be stored up in another organ, eggs and sperm--an
assumption not only unsupported by any evidence, but, as I have stated,
one quite foreign to the hormone theory. In fact, Cunningham’s
suggestion is nothing more than Darwin’s old idea of pangens, which,
being imaginary, could be endowed with all desirable properties. But one
can not invoke a chemical substance, even a hormone, and then at the
critical moment endow it with special virtues.
A rather unique explanation of the origin of secondary sexual characters
is made by Stolzmann. His argument runs as follows: (1) There is a great
excess of males in birds; (2) the males left over after mating are
useless to the species, since they can not propagate and they consume
food needed by the reproducing part of the population; (3) the
conspicuous coloration of the male has been evolved in order that he
could be seen more readily by birds of prey and the objectionable excess
of males removed; the comb of the cock has developed in order that he
may be the more easily killed by other cocks.
Stolzmann’s account of the origin of the plumes of the birds of paradise
should be immortalized in the literature of the subject:
“Nous comprendrons aussi facilement la présence de longues plumes
chez les males de nombreuses espèces, comme p. e. chez les oiseaux
de paradis, chez les veuves (_Vidua_) et chez l’engoulevent
africain (_Cosmetornis_). Telles plumes ont probablement pour but
de relantir le vol des males. J’ai constate chez la _Loddigesia
mirabilis_ (oiseaumouche péruvien), que le vieux male posséde
l’aile quelques millimetres plus courte que le jeune male ou la
femelle. Cet avortement des remiges provient assurément a cause de
développement extraordinaire de retrices externes chez le vieux
male de cet oiseaumouche. Si donc d’une part les retrices allongees
rendent le vol plus difficile et d’hautre les ailes plus petites
diminuent sa vélocité, le vol du male doit ètre plus lent que celui
de la femelle, le poids du corps restant la même. Le développement
extraordinaire soit des remiges soit des rectrices, en
_relantissant_ le vol des males, rend leur rôle plus difficile, en
facilitant en même temps celui des femelles. Nous pouvons prendre
comme exemple le _Cosmetornis_, qui, comme tous les engoulevents,
se nourrit d’insectes, qu’il attrape au vol. Chez cet oiseau
quelques plumes des ailes se developpent extraordinairement pendant
l’époque de reproduction, en retardant visiblement son vol. Il est
donc facile a remarquer, qu’alors le male, ayant les mouvements
plus lourds, n’est pas en êtat de se procurer la même quantité
d’insectes qu’auparavant; ainsi donc la femelle a plus de chances
de trouver une nourriture plus abondante.”[1]
Equally worthy of perpetuation is Stolzmann’s explanation of dancing and
singing birds:
“Toutes les réunions des males, leurs danses bizarres, leur chant,
enfin, ne servent pas probablement a séduire les femelles, mais
pour distraire les males, ce qui rend plus faciles les besognes
maternelles des femelles et au surplus les protege contre
l’assiduite nuisible des célibataires. Darwin lui-mème constate le
fait, qu’ordinairement pendant les réunions des males, quand ces
derniers sont trop occupes par le combat ou la danse, la femelle
s’echappe avec un d’eux pour copuler. Ainsi donc dans ce cas c’est
bien la selection naturelle et non la selection sexuelle, qui agit
pour la conservation d’équilibre sexuel.”[9]
DISPLAY OF THE MALE.
The antics of male birds at the mating season, their courtship
so-called, has played an important rôle in Darwin’s theory of sexual
selection. The behavior of many birds at this time is of such a kind as
to suggest that the male is exhibiting his plumage before the female for
the “purpose” of influencing her choice. The whole paraphernalia of
human psychology is imported into the situation and both the
consciousness of the male, his intentions so to speak, and the supposed
esthetic response or choice of the female is invoked. Even though it be
granted that the words that we must make use of, borrowed from human
behavior, are such as to imply much more in the direction of
consciousness and purpose than is desirable, and that most of the
behavior of animals should be stated in a more roundabout and objective
way, yet the theory will only work out on the assumption that the female
_chooses_ in some sense the more brilliant or ornamental (or effective)
male, whether she is “conscious” or unconscious of intention. I doubt if
anyone to-day would care to defend seriously the theory on the grounds
of consciousness or esthetic value of the exhibition, despite the fact
that Darwin’s language often takes this turn and the less-guarded
statements of some of his disciples, such as Romanes, show little
hesitation in anthropo-morphologizing the entire situation. It is,
however, not necessary for the working out of the theory that this
complication be introduced into it, for if the female is more likely to
mate with a more brilliantly colored than a less brilliantly colored
male, the theory may be made to apply regardless of whether she is
“conscious” or not of the difference to which she responds.
But there are weighty arguments against such an interpretation of the
behavior of the male and female during courtship. In the first place,
there is almost no direct evidence to show that the female mates with
the more ornamental male. As this is the all-essential requirement of
the theory, the almost complete absence of facts in its support leaves
the theory resting on a theoretical assumption. It can scarcely pass
unnoticed that while there exists a large mass of data describing the
secondary sexual characters, there is practically nothing in this
accumulation to show that the female makes her selection on differences
in coloration or ornamentation. And on the other hand, there is some
evidence showing that the female is ready to succumb to the
aggressiveness of the male rather than that she “chooses” him.
The behavior of the male under sexual excitement is often described to
be of a kind to exhibit before the female his peculiar adornments. That
the “purpose” of his exhibition is to show himself off before the female
may be conceded, with reservations as to what is meant here by
“purpose.” That the male is conscious of the probable results of his
conduct is scarcely probable the first time he courted; but that he may
have found out the most probable result after the first attempt through
“associative memory” is in accord with what the study of “animal
behavior” has shown to be possible. In this sense purpose would mean a
line of conduct that experience had shown to lead to a certain end.
Anticipation or far-sightedness would henceforth characterize such a
reaction. Here, however, we venture on very dubious grounds. But the
display of the male may be purposeful in a much simpler sense. His
activity may be an inborn reflex to visual or other sensory stimuli that
is a part of his attack on the female, or possibly a series of reflexes
that we may register under the old unanalyzed terms of “desire and
fear.” The action calls forth a responsive reflex in the female, for the
sexual act is not entirely active on one side, passive on the other, but
consists of a series of interreactions on the part of each sex, which,
if they pursue a given course, leads to the final mating. The mutual
responses appear to follow an automatic course in many cases if the
individuals are sexually ready to mate and the environment is
propitious. Types of behavior of this kind must be familiar to anyone
who has observed domesticated and semi-domesticated animals. The purpose
of the display may mean no more than a reaction that leads to a result
propitious to the perpetuation of the species if the situation is ripe
for such an outcome.
This conclusion still leaves open the question as to whether the display
is more likely to be successful, if certain special characters possessed
by the species are exhibited. In the absence of any sufficient evidence
to show that this is so, and in the light of the very great danger of
projecting “our human standards” into the world of other animals, and in
view of the fact that related species without such marks are as
successful in maintaining themselves, I can not but think that at
present we have a good deal to lose in the way of scientific procedure
and nothing to gain of scientific value in accepting Darwin’s
interpretation of sexual selection based on the display of the male as
furnishing an opportunity to the female to make the “best” selection
amongst her suitors on the basis of his adornment.
An excellent opportunity to study the problem as to “choosing” by the
female is furnished by the mutant races of _Drosophila_, some of which,
differing in a single mutant gene, have wings as different in coloration
as black, yellow, or gray, and eyes as differently colored as white,
vermilion, or red. Sturtevant put a yellow female with a gray
(wild-type) male and a yellow male. The male that first mated was noted
and the trio discarded. The female “chose” the gray males 25 times and
the yellow only 8 times. In the control combination, where a gray female
“chose” between the same two kinds of males, she took the gray male 60
times and the yellow male 12 times. In both cases it “appears” that the
female “prefers” the gray male, but this deduction may give an entirely
wrong impression as to what is taking place, for the result would be
the same in kind if the gray male were more active and mated quicker.
This was tested by putting a gray and a yellow female with a gray male
and then for control a gray and a yellow female with a yellow male. The
result was as follows:
Red ♂ {Gray ♀ 25 Yellow ♂ {Gray ♀ 12
{Yellow ♀ 31 {Yellow ♀ 30
Here the gray male mated slightly oftener with the yellow female than
with the other, whereas the yellow male mated much oftener with the
yellow female than with the gray one. Both results are explicable on the
view that the yellow female, being less active, is more easily captured
by the yellow male than is the gray female. This view fits in also with
the former experiment, where the yellow male is much less successful
than the more active gray male. Such a conclusion gives a more
consistent explanation of all the facts than does the theory of female
choice, for on the latter we must suppose that the yellow females prefer
the gray males and the yellow male prefers the yellow females, etc.
The following results were obtained by Sturtevant when red and white
eyed flies were competing:
Red ♂ {Red ♀ 54 Red ♀ {Red ♂ 53
{White ♀ 82 {White ♂ 14
White ♂ {Red ♀ 40 White ♀ {Red ♂ 62
{White ♀ 93 {White ♂ 19
The outcome can be interpreted in the same way as the yellow-gray
competition. The red male wins by virtue of his greater activity, while
the white female is chosen more often, especially by the white male,
because of her passivity (or weaker resistance). It may be claimed that
these results do not show that the female does not choose, for such
choice, if made, would be swamped by another condition of the
experiment, viz, the greater aggressiveness of one kind of male and
greater passivity of the other kind of female. This, of course, is true,
but the experiment still shows that in these flies other influences are
so much greater than “choice” by the female, if it exists, that the
postulated effect of the latter practically disappears from the
situation.
Mayer’s experiments with the large moth _Callosamia promethea_ furnish
important information as to the factors involved in mating. The results
are all the more significant from our present point of view because the
colors of male and female are in this species markedly different. The
wings of the male are black, those of the female reddish brown; the
antennæ of the male are large and bushy, those of the female small and
slender. Mayer found that the males are attracted by the female from
some distance when the latter are put into a glass jar covered by only
coarse mosquito-netting, but if the same jars are turned upside down the
males are unable to find the female. Females concealed in loose cotton
attracted males. Females were put into a box with an open chimney at one
end, the other open end being covered by mosquito-netting. A current of
air blew into the open end and out of the chimney. The males flew to the
end of the chimney from which the air came and fluttered about in the
neighborhood. Males are attracted to places where a female has been kept
even several hours after her removal. The male finds the female through
the sense-organs in his antennæ, for a male whose abdomen has been cut
off and the sides of whose thorax are covered with shellac will still
fly to the female, but if his antennæ he coated with any substance he no
longer seeks the female. If the eyes of the males are blackened they
will mate with females “in the normal manner.”
Mayer cut off the wings of females and glued male wings in their places,
so that the female looked like a male. Males readily mated with these
females. The wings of males were cut off and female wings glued in their
place. Mating occurred “with normal frequency, and I was unable to
detect that the female displayed any unusual aversion” to such males.
Males with female wings pass unnoticed by other males.
In a later paper (1901) Mayer and Soule describe how, when the wings of
the male were painted scarlet or green, the males were accepted as
readily as normals in competition with them. Experiments were also made
by them with the gipsy moth. Wingless males met with more “resistance”
from the female than do normal males, but when the eyes were covered the
wingless males succeeded as often as the normal males, but the number of
observations on which this statement is were far too few to be of any
value, and there are several other observations that make any such
conclusion from the evidence highly uncertain.
That it is the odor of the females that attracts the male can not be
doubted. It might still be claimed that the female chooses amongst her
suitors the darkest males, but the evidence gives no grounds for
inferring such a choice, and since she will even accept males with
female wings when they attempt to mate with her, it does not appear
probable that the color of the male is a factor in the result, or at
least if it is, then it must be entirely subordinate to the sense of
smell in finding the female and of touch after he arrives. There is
little or nothing in the behavior of these moths, or in that of the
silkworm moth, according to Kellogg, to suggest that vision plays any
significant rôle in courtship.
Concerning the genetic situation in insects, there are only a few cases
that have been studied. The most instructive are those in which more
than a single kind of male exists (two or three), one of which may be
like the female, the other quite different. The best worked out cases
are _Papilio memnon_ and _P. polytes_. De Meijere and Punnett have
shown from the breeding data that it is possible to frame an explanation
of such a sort that the aberrant female differs from the female
resembling the male in only a single genetic factor--one not sex-linked
(_i. e._, not carried by an X chromosome), but autosomal. The gene would
be of such a sort that it affects the female only--producing no visible
effect on the male. Such a conclusion, if established, helps,
theoretically at least, toward simplifying the situation in other
species, for it shows that genetic factors occur whose influence is on
one sex alone; hence the difference between the male and one type of
female does in such cases result from a single gene present in both but
causing them to be differently colored. There would be no need, then, to
assume that the difference had been slowly built up by selection, but
rather that the difference arose at some time by a single mutant step.
The incorporation of the step in the species would then follow if the
effect of the gene were useful in mating or if it had some other primary
significance for the welfare of the species, the different effect
produced on the male and female being only an unimportant by-product of
its action. On the other hand, it should be emphasized that because a
single factor difference between the two kinds of females will explain
the genetic results, it does not necessarily follow that the difference
did arise as a single mutation. The foregoing argument does no more than
imply that the difference in question may have arisen in this way, and
if so, that the situation, as it exists, would be the more easily
comprehended.
In insects and spiders, where dimorphism is as marked as in birds, the
mating habits have been studied by a number of naturalists. Here also
there are numerous accounts of the display of the male during courtship.
The account given by Dr. and Mrs. Peckham are particularly detailed and
call for careful consideration on account of their well-recognized
accuracy in observational work. Moreover, as a result of their
observations, along with those of Montgomery, Petrunkewitsch, and
others, we have really fuller information concerning the courtship of
spiders than of birds and of mammals.
In the great majority of species where the sexes are different the male
is more brightly colored or more ornamental. For example, in a group
such as the Attidæ of France, where both sexes are known, the Peckhams
state that in 26 cases the male is more conspicuous than the female; in
55 cases the sexes are alike, or if they differ the male is more
conspicuous. It appears that in other genera there are cases where the
female is more conspicuous than the male. The Peckhams state that
possibly as many as 250 species are in this condition. Those females
with brighter colors than the males are usually well armed by strong
spines. When very young they are like the males and begin to assume the
adult form and color when they are a quarter to a third grown. Whether
the change depends on changes in the ovary is not known.
The mating behavior of _Saitis pulex_, a species in which the males and
females are much alike, is described by the Peckhams as follows:
“On May 24th we found a mature female and placed her in one of the
larger boxes, and the next day we put a male in with her. He saw
her as she stood perfectly still, twelve inches away; the glance
seemed to excite him and he at once moved toward her; when some
four inches from her he stood still and then began the most
remarkable performances that an amorous male could offer to an
admiring female. She eyed him eagerly, changing her position from
time to time so that he might be always in view. He, raising his
whole body on one side by straightening out the legs, and lowering
it on the other by folding the first two pairs of legs up and
under, leaned so far over as to be in danger of losing his balance,
which he only maintained by sidling rapidly toward the lowered
side. The palpus, too, on this side was turned back to correspond
to the direction of the legs nearest it. (Fig. 13.) He moved in a
semi-circle for about two inches and then instantly reversed the
position of the legs and circled in the opposite direction,
gradually approaching nearer and nearer to the female. Now she
dashes toward him, while he, raising his first pair of legs,
extends them upward and forward as if to hold her off, but withal
slowly retreats. Again and again he circles from side to side, she
gazing toward him in a softer mood, evidently admiring the grace of
his antics. This is repeated until we have counted 111 circles made
by the ardent little male. Now he approaches nearer and nearer and
when almost within reach whirls madly around and around her, she
joining and whirling with him in a giddy maze. Again he falls back
and resumes his semi-circular motions, with his body tilted over;
she, all excitement, lowers her head and raises her body so that it
is almost vertical; both draw nearer; she moves slowly under him,
he crawling over her head, and the mating is accomplished.
“After they have paired once, the preliminary courtship is not so
long. When this same pair mated a second time, there was no
whirling movement, nor did the female lift her body, as at first.”
(pp. 37-38).[10]
The courtship of another species, _Dendryphantes capitatus_, in which
the sexes are entirely different, is described as follows:
“The males of _capitatus_ are very quarrelsome, sparring whenever
they meet, chasing each other about, and sometimes clinching. It is
a very abundant spider with us, so that we often put eight or ten
males into a box to see them fight. It seemed cruel sport at first,
but it was soon apparent that they were very prudent little
fellows, and were fully conscious that ‘he who fights and runs away
will live to fight another day.’ In fact, after two weeks of hard
fighting we were unable to discover one wounded warrior. When the
males are approaching each other, they hold the first legs up in a
vertical direction. Sometimes they drop the body on to one side as
they jump about each other. These movement are very quick, and they
are always ready for a passage at arms. When courting the females
they have another movement. They approach her rapidly until within
two to five inches, when they stop and extend the first legs
directly forward, close to the ground, the legs being slightly
curved with the tips turned up. (Fig. 18). Whether it be
intentional or not, this position serves admirably to expose the
whole of the bronze and white face to the attentive female, who
watches him closely from a little distance. (Fig. 19.) The males
also give their palpi a circular movement, much as a person does
when washing his hands. As he grows more excited, he lies down on
one side with his legs still extended. These antics are repeated
for a very long time, often for hours, when at last the female,
either won by his beauty or worn out by his persistence, accepts
his addresses.” (Pp. 45, 46.)
In another species, _Dendryphantes elegans_, both sexes are brilliantly
colored.
“The male is covered with iridescent scales, his general color
being green; in the female the coloring is dark, but iridescent,
and in certain lights has lovely rosy tints. In the sunlight both
shine with the metallic splendor of hummingbirds. The male alone
has a superciliary fringe of hairs on either side of his head, his
first legs being also longer and more adorned than those of his
mate. The female is much larger, and her loveliness is accompanied
by an extreme irritability of temper which the male seems to regard
as a constant menace to his safety, but his eagerness being great,
and his manners devoted and tender, he gradually overcomes her
opposition. Her change of mood is only brought about after much
patient courting on his part. While from three to five inches
distant from her he begins to wave his plumy first legs in a way
that reminds one of a wind-mill. She eyes him fiercely and he keeps
at a proper distance for a long time. If he comes close she dashes
at him and he quickly retreats. Sometimes he becomes bolder and
when within an inch, pauses, with the first legs outstretched
before him, not raised as is common in other species; the palpi
also are held stiffly out in front with the points together. Again
she drives him off, and so the play continues. Now the male grows
excited as he approaches her, and while still several inches away
whirls completely around and around; pausing, he runs closer and
begins to make his abdomen quiver as he stands on tip-toe in front
of her. Prancing from side to side, he grows bolder and bolder,
while she seems less fierce, and yielding to the excitement lifts
up her magnificently iridescent abdomen, holding it at one time
vertically and at another sideways to him. She no longer rushes at
him, but retreats a little as he approaches. At last he comes close
to her, lying flat, with his first legs stretched out and
quivering. With the tips of his front legs he gently pats her; this
seems to arouse the old demon of resistance, and she drives him
back. Again and again he pats her with a caressing movement,
gradually creeping nearer and nearer, which she now permits without
resistance until he crawls over her head to her abdomen, far enough
to reach the epigynum with his palpus”. (Pp. 46-47.)
If we lay no emphasis on the implied emotional elements in the behavior
of the spiders in this description--terms of emotion borrowed direct
from human psychology--there still remain the several types of
apparently significant reactions associated with courtship. The
statements leave no room for doubt that vision plays an important rôle
in the complex reflexes that lead gradually to successful mating. The
Peckhams insist that the display of the male is always of a kind to
bring before the female the special adornments of the male in whatever
part of the body they may lie. The chance of subjective interpretation
here is so great that unless the results are carefully checked up by
studies of the attitudes assumed by males in species in which the males
are without ornament, their interpretation must be taken with the
greatest reserve. Assigning, as our authors do, so much by gratuitous
implication to the emotional side of the picture prejudices one,
perhaps too greatly, against accepting a special (even an implied
intentional) exhibition of the specially ornamented parts. On the other
hand, if it be conceded that the conspicuousness of the male is an
element in the reaction, the very special adornments visible from the
front might be supposed to enhance the effect produced in the female.
Similar displays of special ornamentation in the male have been
described both for birds and insects, but here, too, the question has
been raised as to whether such exhibitions are more than an accidental
accompaniment of the posturing of the male, for the same kind of
behavior is known to occur in other cases where the male is unornamented
and resembles the female. Had such a male special ornamentation it would
no doubt appear to us that his behavior was “calculated” to display his
ornaments.
Dr. and Mrs. Peckham point out that their observations are entirely
inconsistent with Wallace’s interpretation of the origin of secondary
sexual characters. They find no evidence in favor of his view that the
male possesses greater “vital activity.” On the contrary, the female is
the more active and pugnacious of the two. They also object to Wallace’s
statement of a total absence of any evidence that the female notices the
display of the male. In spiders the females “_observe_” the males with
close attention during their courtship. They point out also that, in
spiders at least, as the female gradually becomes adult, a male if
preferred will have a chance of mating with several females, “and as the
mating season lasts for two or three weeks the more brilliant males may
easily be selected again and again.” In regard to Wallace’s argument as
to the distribution of accessory plumes in humming birds, the Peckhams
point out that--
“The pectoral muscles reach their highest development in the
hummingbirds, the diurnal birds of prey, and the swallows, and we
may, therefore, fairly use these groups to test Mr. Wallace’s
explanation of breast plumes. In the swallows and birds of prey we
find no such appendages, in spite of their further claim to them,
on the ground of great vigor and activity. As to the humming-birds,
we find in the genus _Aglæactis_ six species with more or less
developed breast-plumes, which are also found in nine other
species, scattered through different genera--in all, only fifteen
species out of four hundred and twenty-six; while we find in
fifty-six species the lengthened and modified tail-feathers, which,
according to Mr. Wallace’s view, should be peculiar to the
Gallinaceæ.
“Again, there are elongated feathers from the throat or from the
side of the neck in thirty-five species, while seventeen have
crests from the top of the head, and seventeen, downy puffs from
the tarsi.”[11]
From this brief survey of the family we see that, contrary to what we
should expect from Mr. Wallace’s theory, although the breast muscles are
the seat of the highest activity, breast plumes are the least frequent
of all the forms of ornamental plumage.
“We may fairly say, then, that the humming-birds completely refute
the proposition that there is any relation between the development
of color and accessory plumes and ‘surfaces where muscular and
nervous development is considerable.’”[12]
What is true for birds is even more obvious for spiders where the
special ornaments are not confined to parts of the body with high
muscular development, etc. The writers make the very pertinent criticism
that while Wallace objects to assuming the emotional states in females,
he is less careful in regard to the males’ emotions when he speaks of
the display “under the influence of jealousy or sexual excitement....
The males, in their rivalry with each other, _would see what plumes were
most effective; and each would endeavor to excel his enemy_ as far as
voluntary exertion would enable him.”[13]
“If the males have so complex an emotion as jealousy, and further,
if they are conscious of the value of the plumes, may it not be
asked why the female is unable to ‘see what plumes are most
effective?’ The mental state in the male is without meaning unless
we suppose the female to be affected and pleased.” (Peckham, _loc.
cit._, p. 144.)
In regard to another interpretation of the courtship, the Peckhams point
out:
“Mr. Pocock has suggested that the attitude of observant interest
on the part of the female spider might be taken to indicate that
she was preparing to spring upon her mate and devour him; or that
it might simply mean that she was warily guarding herself from his
approach. Neither of these suppositions is admissible. In some
species the male is not attacked by the female, and when she does
wish, as frequently happens, either to avoid or to destroy him, her
attitude is totally different. In the former case she turns about
and runs rapidly away, or suspends herself by a thread of web. In
the second, there is a contraction of all the muscles, the legs are
drawn together, and in this crouching position she creeps slowly
toward him, as she might if he were a fly, only with something more
malignant in her aspect. When she takes this stand the male
incontinently flees. When, on the contrary, the female is
interested in the male display, she seems perfectly absorbed in
watching him, the muscles are all relaxed, unconscious of herself
she directs her glance now here, now there, as he moves about; as
he continues his mad antics, her appearance gives every indication
of pleasurable excitement, and as he comes closer and closer, she
yields herself to the impulses which he has awakened in her, and,
as in _pulex_, joins in his dance and whirls around and around as
though intoxicated. We claim, then, to have completely answered Mr.
Wallace’s first objection.” (Peckham, _loc. cit._, pp. 145, 146.)
Finally, in regard to the specific character of the display of the
males, the Peckhams make the following significant statement:
“The spider has four pairs of legs, and all are equally available
for display or locomotion, and since all the movements are slow and
on the ground they are entirely open to observation and study, and
we are thus in a position to decide by facts whether their activity
is simply an outlet for superfluous energy, and therefore
meaningless, or whether there is a purpose in it. If the purpose of
the antics is only to let off energy, then we should expect one
pair to be flourished around quite as often as another, and that
the pair flourished should as frequently be one that was not
ornamented as one that was; and, moreover, their movements ought
not to be of such a nature as to display the color or ornament,
more frequently than the law of chance would explain. If the spider
almost always moves the ornamented legs, and in such a way, too, as
to bring out their beauty, it would seem to us, to say the least,
highly improbable that the dance of the spider was merely a
meaningless overflow of surplus energy. Such an explanation leaves
much that needs explanation. The facts are, that the best foot is
put forward; and this is just what Darwin’s theory requires and
explains. Under Mr. Wallace’s view the facts are inexplicable. The
better to show that these movements are not simply meaningless
outlets of high vigor, we illustrate the several positions by
figures taken from nature (figs. 7-12). The figures would seem to
prove that the legs that are ornamented or contrasted in color are
also the legs that are usually flourished; that where none of the
legs have special ornament, then all are used; or, as sometimes
happens, when an unornamented leg is used the movements are of such
a character as to display some ornament that would otherwise have
been more or less hidden from the female.” (Peckham, _loc. cit._,
p. 147.)
In the tarantula, Petrunkewitsch finds that sight plays no rôle in
mating--that it is due entirely to accidental contact between the male
and female. Here the sexes are closely alike, except for a pair of hooks
on the front legs of the male, by means of which he grasps the mandibles
of the female, holding them during the elaborate process of transference
to her genital opening the sperm that he has already collected in the
genital spoon on his palpi. The hooks serve to guard the male against
injury or death, while at the same time they aid him in the act of
coitus.
In a common spider, _Mœvia villata_, two kinds of males exist. Both have
been seen to mate with the same female. No preference is given to either
type. The difference between them, according to Painter, is connected
with or caused by an additional pair of chromosomes in the gray male.
The two types may therefore have no connection with sexual selection,
but be directly due to a difference in the chromosome group.
Montgomery, who made observations on the courting habits of several
species of spiders, states that his “general theoretical conclusions
were quite different from those of the Peckhams.” It turns out, however,
that his objection to their view is based entirely on their assumption
that the male is conscious of his display and that the female is guided
by an esthetic sense in selecting the more beautiful male. It should be
pointed out that even after the removal of these gratuitous assumptions
as to the cause of the evolution of the male and female, enough still
remains in Montgomery’s own observations to include his results on
courtship under Darwin’s theory of sexual selection. For example,
Montgomery says:
“The adult male is excited simultaneously by fear of and desire for
the female, and his courtship motions are for the most part
exaggerations of ordinary motions of fear and timidity. By such
motions he advertises himself to the female as a male, but there is
no proof that he consciously seeks to arouse her eagerness by
esthetic display--there seems to be no good reason to hold that the
female is actuated in her choice by sensations of beauty.... Thus
my opinion was opposed to Darwin’s theory.”
Now, it is obvious that if a more brightly colored male has a better
chance of “advertising himself” to the female all the essential
requirements of Darwin’s theory are fulfilled, regardless of whether the
male is conscious of his ornamentation or the female makes use of an
“esthetic sense.” In another passage (p. 173) Montgomery concedes all
that any modern critical advocate of Darwin’s theory is likely to ask:
“We have previously seen that conscious aesthetic choice by the
female probably does not account for such male characters
[secondary sexual characters with their ‘conspicuous color
markings’]; that they are accordingly, probably not due to sexual
selection. These characters of the males may be most readily
explained as being conceived by simple natural selection. Peculiar
ornamentation would be selected because unusually greater sex
recognition therefore prompted mating.”
It is evident that Montgomery has only shifted the situation, although
to advantage, I think, but is essentially in accord with Darwin’s theory
of sexual selection, despite his protest to the contrary. The difference
lies in Darwin’s and especially in the Peckhams’ use of the term
“choice,” “aesthetic sense,” etc., to stand for the fact that the female
more promptly mates (as Montgomery prefers to put it) with a male
peculiarly ornamental.
The most critical observations on sexual selection that have been made
in the group of insects are those by Sturtevant on the pomace fly. The
courtship is described as follows:
“The first and most noticeable act in courtship occurs when the
male, being near the female, extends one wing at about right angles
to his body, and vibrates it for a few seconds. The wing is then
returned to the normal position and the process is repeated,
usually with the other wing. But between times there is a
scissors-like movement of the wings repeated several times. This
vibrating of the wings is often repeated many times, and may be
done in any position relative to the female, though the male always
faces her. Usually, in fact, he swings quickly around her in a
semicircle once, or oftener, during the process. Soon the male
begins to protrude his genitalia and, if the female remains quiet,
to lick her posterior end. Some white matter now protrudes from her
ovipositor, and other males in the same vial are usually observed
to become excited now and begin courting, indicating odor as a
cause of sexual excitement. If the female runs or flies away the
male is excited, moves his wings jerkily, and walks around
rapidly, but seems unable to follow the female accurately or to
locate her quickly. The penis is directed forward by bending up the
abdomen underneath, towards the thorax, and is jerked toward the
female (the male always standing facing her at this stage), but not
always toward her genitalia, as I have seen it strike her in the
eye. (The male in this case, however, had white eyes, and so was
perhaps blind. Normally the aim is accurate.) If it does strike the
mark the male mounts on the female’s back, between her wings.
Mounting never takes place until after the actual copulation has
occurred, in which respect _Drosophila_ differs from some related
flies (_e. g._, Muscidæ, Anthomyidæ, Sepsidæ, Borboridæ, and
Ephydrichæ, so far as my observations go). In these forms the male
flies and lights on the female, after which copulation may or may
not take place, probably depending upon the way the female
responds.”[14]
To test whether the wings have any significance in courtship, the wings
of a male were clipped off and he was put into competition with a normal
male of the same stock, age, and size. A virgin female sexually mature
was given to these two males. The normal male mated 72 times before the
other, the clipped male 53 times. It might appear that the female
selected the normal male in preference to the clipped one, or possibly
that the male with normal wings drove the other male away. That the
operation on the wings may have an influence on the male himself is
shown in McEwen’s results. He found that clipped males lost their
heliotropism. It was also possible that the courtship of the normal male
might make the female ready to copulate and then she would mate with
either male. Sturtevant tested the last supposition by placing single
pairs in vials, testing each day an equal number of normal and clipped
males. The length of time before copulation was noted. The clipped male
began to court as soon as the normal, but a larger number of normal
males mated in the first 12 minutes than clipped males (50 to 25). Had
the females discriminated against the clipped males to an equal extent
we would have expected a much greater excess than 72 to 53 when they
were in competition. It appears, then, that the wings are useful in
shortening the time between the meeting of the individuals and
copulation. The display acts, however, almost as favorably for the other
male as for the exhibitor himself. The results show, therefore, that
here an esthetic sense of the female need not be postulated, for she
actually shows little preference when she has been brought to the point
of mating between the male that aroused her and the other male that did
not. This critical test puts the problem in a different relation from
that which Darwin’s theory of female choice was meant to throw light
upon.
The reverse experiment--a clipped and a normal female of the same age,
size, etc.--showed that the mate did not discriminate between them, for
in 52 first trials the normal female was paired with 25 times, the
clipped 27 times.