The Mating Mind: How Sexual Choice Shaped the Evolution of Human Nature (7 page)

This means that evolution must include some form of creative, trait-shaping selection other than natural selection. Darwin reasoned that in a sexually reproducing species, any traits that help in competing for sexual mates will tend to spread through the species. These traits may evolve even if they reduce survival ability. While natural selection adapts species to their environments, sexual selection shapes each sex in relation to the other sex. In
The Origin,
Darwin argued that sexual selection depends "not on a struggle for existence in relation to other organic beings or to external conditions, but on a struggle between the individuals of one sex, generally the males, for the possession of the other sex. The result is not death to the unsuccessful competitor, but few or no offspring."

Darwin didn't know about genes or DNA. But he understood that in a sexually reproducing species, the only way to pass a trait from one generation to the next was, by definition, through sexual reproduction. If an animal doesn't have sex, its heritable traits will die with it, and it will leave no hereditary trace in the next generation. As far as evolution is concerned, the animal may as well have died in infancy. Survival without reproduction means evolutionary oblivion. On the other hand, reproduction followed by death can still translate into evolutionary success. Sexual inheritance puts sexual reproduction at the heart of evolution. The concept of sexual selection is simply a way of describing how differences in reproductive success lead to evolutionary change.

Sexual, Natural, Artificial

To explain sexual selection, Darwin used the familiar metaphor of artificial selection. Victorian England was still mostly agricultural and pastoral. People knew about artificial selection, in which farmers domesticate plants and animals by allowing some individuals to breed and others not. Darwin had already used this barnyard type of artificial selection as a metaphor to explain how natural selection worked. Sexual selection he compared to a rather different sort of artificial selection more familiar to the leisured classes, and more relevant to gorgeous ornamentation: breeding pet birds to make them look unusual and attractive. In
The Origin
he argued that "if man can in a short time give beauty and an elegant carriage to his bantams, according to his standard of beauty, I can see no good reason to doubt that female birds, by selecting, during thousands of generations, the most melodious or beautiful males, according to their standard of beauty, might produce a marked effect."

The analogy between artificial selection by human breeders and sexual selection by female animals may seem strained. But for Darwin there was no essential difference between human minds and animal minds: both could work as selective forces in evolution. As a dog-lover and an experienced horseman, Darwin felt comfortable attributing intelligence to animals. He reasoned

that if humans can breed dogs, cats, and birds according to our aesthetic tastes, why shouldn't these animals be able to breed themselves according to their own sexual tastes?

Biology students now are usually taught that sexual selection is a subset of natural selection, and that natural selection is only loosely analogous to artificial selection by human breeders. This was not Darwin's view: he saw sexual selection as an autonomous process that was midway between natural and artificial selection. Darwin was fairly careful about his terms. For him, artificial selection meant the selective breeding of domesticated species by humans for their economic, aesthetic, or alimentary value. Natural selection referred to competition within or between species that affects relative survival ability Sexual selection referred to sexual competition within a species that affects relative rates of reproduction. Darwin knew that Herbert Spencer's term "survival of the fittest" could be misleading Heritable differences in reproduction ability were as important in evolution as heritable differences in survival ability.

However, whereas natural and artificial selection can apply equally well to mushrooms, lemon trees, and oysters, Darwin believed that sexual selection acts most strongly in the higher animals. This is because courtship behavior and selective mate choice behavior are best carried out by mobile animals with eyes, ears, and nervous systems. The mate choice mechanisms that drive sexual selection are much more similar to artificial selection by humans than to blind forms of natural selection by physical or ecological environments. Darwin understood that sexual selection's dependence on active choice might create distinct evolutionary patterns such as fashion cycles and rapid divergence between closely related species.

Males Court, Females Choose

Darwin was more interested in explaining ornamentation than in explaining sex differences. Still, he could not help but notice that male animals are almost always more heavily ornamented than females. He also noticed that most of the differences between

males and females are either specializations for making eggs or sperm, or specializations in the weaponry and ornamentation used during sexual competition. Sexual selection was not only useful in explaining ornamental traits that natural selection could not explain. It could also account for almost all differences between the sexes.

This made a rather neat story. Males usually compete to inseminate females. They do this by intimidating other males with weaponry and by attracting females with ornaments. Females exercise sexual choice, picking the stronger and more attractive males over the weaker and plainer. Over generations, male weaponry evolves to be more intimidating and male ornamentation evolves to be more impressive. There are two results. First, within each sexual species, males diverge from the female norm. Mature males become more strongly differentiated, compared with females, compared with young animals, and compared with their own ancestors. The other result is very fast divergence between species. The weaponry and ornamentation of one species can go off in a very different direction from the weaponry and ornamentation of a closely related species. Thus, Darwin's sexual selection idea could explain three enigmas: the ubiquity across many species of ornaments that do not help survival, sex differences within species, and rapid evolutionary divergence between species.

Darwin had no real explanation of why males court and females choose. Why aren't males choosier? Why don't females evolve weapons and ornaments equally? The fact was that they don't. Darwin felt obligated to report his findings even though, as he admitted, his sexual selection theory was incomplete.
The Descent of Man
is mostly a report on sex differences in ornamentation in non-human animals. Darwin gathered hundreds of examples of males growing larger ornaments than females, and fighting for sexual access to females. He offered a staggering amount of evidence that this typical pattern of sex differences holds from insects through humans. As we shall see, however, critics tended to ignore Darwin's evidence and focus on the gaps in his theory

What Females Want

Darwin envisioned two main processes of sexual selection: competition among males for the "possession" of female mates, and selection by choosy females among male suitors. Male weapons and pugnacity evolved for fighting other males, and male ornaments and courtship displays evolved for attracting females. The second process, sexual selection through female choice, interested him far more than male contests of strength. The hypothesis of female choice was, Darwin knew, among his most daring and unanticipated. The theory of sexual selection was an intellectual bolt from the blue, and sexual selection through female choice was especially shocking. Darwin understood that his hypothesis of female choice among animals would challenge Victorian social attitudes.

To bolster the case for female choice in
The Descent,
Darwin relied heavily on the analogy with artificial selection. His two-volume study of domestication in 1868 showed how human breeders of chickens, horses, or dogs can select over many generations for greater egg yield, running speed, or emotional stability. If human choice can have such dramatic evolutionary effects, then surely female animals choosing mates can unconsciously select for longer tails, louder songs, or brighter colors in their male suitors. In
The Descent,
Darwin argued that female choice could produce traits as extravagant as those shaped by artificial selection:

All animals present individual differences, and as man can modify his domesticated birds by selecting the individuals which appear to him the most beautiful, so the habitual or even occasional preference by the female of the more attractive males would almost certainly lead to their modification; and such modifications might in the course of time be augmented to almost any extent, compatible with the existence of the species.

could drive traits to a very high degree of elaboration.

The only limit is extinction: if the courtship trait becomes so costly that it imperils the survival of too many individuals, the species may simply die out. Darwin presented this conclusion with admirable sang-froid: so be it. Sexual selection may drive species to extinction, but that is no argument against its existence. Species do
go
extinct, appallingly often. Perhaps the ancient Irish elk went extinct because their sexual ornaments—antlers over six feet wide—proved too burdensome. There is no balance of nature that keeps this from happening. The extinction process merely lets us make this prediction: the sexual ornaments of species that have not yet gone extinct are not yet so costly that they kill off almost every male in every generation. Only if the costs of ornamentation result in the deaths of an extremely high proportion of males does a species have trouble maintaining its numbers.

Darwin did not speculate about how female preferences evolve, but he did pay considerable attention to how they apparently work in selecting mates. His analysis of the plumage of the Argus pheasant, spanning almost ten pages of
The Descent,
is a tour de force. The male Argus grows feathers with eyespots like that of the peacock. But each Argus eyespot, though spread out in a fan shape, is shaded to give a spherical appearance, as if illuminated from above. The direction of shading on each eyespot, relative to the feather's axis of growth, must vary in accordance with the typical angle at which the feather is displayed. Darwin thought it extraordinary that evolution could render such an optical illusion so perfectly on a bird's plumage, but he was confident that generations of female choice could account for it:

The case of the male Argus is eminently interesting, because it affords good evidence that the most refined beauty may serve as a charm for the female, and for no other purpose.... Many will declare that it is utterly incredible that a female bird should be able to appreciate fine shading and exquisite patterns. It is undoubtedly a marvellous fact that she should possess this almost human degree of taste, though perhaps she admires the

general effect rather than each separate detail. He who thinks he can safely gauge the discrimination and taste of the lower animals, may deny that the female Argus pheasant can appreciate such refined beauty; but he will then be compelled to admit that the extraordinary attitudes assumed by the male during the act of courtship, by which the wonderful beauty of his plumage is fully displayed, are purposeless; and this is a conclusion which I for one will never admit.

Darwin remained true to his conviction. Despite heavy opposition to the idea of female choice from his scientific peers, Darwin maintained that the biological evidence was overwhelming, and documented hundreds of male traits that seemed inexplicable in any other way. He reasoned that the function of an evolved adaptation is often revealed in its manifest use by the organism. If an eye is used conspicuously by an animal to see things, and for no other purpose, then the eye probably evolved for vision. If a male animal uses its horns to fight other males, and for no other purpose, then the horns probably evolved for male competition. If a tail is wagged energetically and saliently during courtship, and under no other conditions, and if the tail shows special features that render it visually impressive (e.g. bright coloration, complex patterning, large size), and if the females of the species prefer males with more impressive tails, then the tail probably evolved to court potential mates. The adaptationist logic is the same in each case. But where Darwin was willing to apply the same pragmatic standards of evidence and argument to courtship traits that he applied to other evolved adaptations, his more skeptical colleagues would demand much stronger evidence for female choice than they ever asked for natural selection.

Darwin's evidence for female choice was indirect because Victorian biology lacked methods for experimentally testing animal preferences. Wilhelm Wundt's experimental psychology laboratory in Leipzig, the first in the world, was not established until shortly before Darwin's death in 1882. For indirect evidence of female choice, Darwin had to analyze the marks such choice

left on males. In hundreds of species, he analyzed the bodily and behavioral ornaments of males that may have been shaped through female choice.
The Descent
presented such overwhelming evidence for the use of male ornaments in courtship to attract females, that it seems incredible that Darwin's peers doubted the power of female choice. The main biological questions after Darwin should have been, "Why does mate choice evolve, why are females choosier than males, and what kinds of adaptations can be produced by mate choice?" The main psychological question should have been "What role did mate choice play in the evolution of the human mind?" Instead, most biologists after Darwin have asked, "How can we possibly believe that female animals choose with whom they mate?" The history of sexual selection theory is largely a history of this skepticism.