The Mating Mind: How Sexual Choice Shaped the Evolution of Human Nature (8 page)

The skepticism about female choice is doubly odd because Darwin took such pains to explain what he meant by female choice. Again and again in
The Descent
he said that mate choice by females need not be conscious and deliberative, but can still be quite accurate, perceptive, and finely tuned. Most biologists accepted that predators choose which prey to chase, that birds choose where to build nests, and that apes choose where to look for food. Are such decisions "conscious"? It doesn't much matter whether we call animal decision-making conscious; what matters is the evolutionary effects of the choice on the animal's own fitness and on the reproductive success of others. Since Darwin freed himself from human prejudices about conscious decision-making, he could see that female choice probably extends to every animal species with a reasonably complicated nervous system. He wrote about female choice in crustaceans, spiders, and insects. The whole point of having a nervous system is to make important adaptive decisions. What decision could be more important than with whom to combine one's inheritance to produce one's offspring?

Mate choice is limited by an animal's senses. Darwin knew that some species have senses quite different from ours. To appreciate their sexual ornaments, we sometimes have to overcome our

assumptions about what is perceivable and what is attractive. Usually we can appreciate the beauty of sexual ornaments in other species only because our senses happen to respond to some of the same stimuli as the senses of those other species. Our primate color vision overlaps in sensitivity with that of many birds, so we can appreciate the colors and forms of bird plumage. But, as Darwin pointed out, our noses may be insensitive to the appealing scents that have been sexually selected in other mammals. We mistakenly perceive most mammals as relatively unornamented.

Even where our senses coincide with those of other species, our aesthetic tastes may differ. Darwin explained that some bird songs sound unmelodic and harsh to our ears, but may still seem attractive to females of the species. Male bitterns (relatives of herons) produce mating calls that sound like guttural gulping, belching, braying, and booming, giving rise to their vernacular names "thunder pumper" and "stake driver." Humans do not enjoy listening to bitterns, but Darwin understood that our tastes are irrelevant in the evolution of bittern mating calls; what matters is the tastes of female bitterns. Their tastes have been forceful enough over time that the male bittern esophagus used to produce their gulpy belches has evolved to thicken every spring just in time for courtship.

Darwin the Radical Psychologist

Sexual selection was a revolutionary idea in several respects. First, it was a truly novel concept. Darwin's theory that species evolve had been anticipated by many 18th- and 19th-century thinkers such as Jean-Baptiste de Lamarck, Étienne Geoffroy Saint-Hilaire, Frédéric Cuvier, and Robert Chambers. Darwin's own grandfather, Erasmus Darwin, had written rather erotic poems about the evolution of flowers. Darwin's theory of natural selection was co-discovered by Alfred Russel Wallace. Sexual selection was quite different. Darwin's notion that mate choice could shape organic form was without scientific precedent.

Second, sexual selection embodied Darwin's conviction that

evolution was a matter of differences in reproduction rather than just differences in survival. Animals expend their very lives in the pursuit of mates, against all the expectations of natural theology. Far from a Creator benevolently fitting each animal to prosper in its allotted niche, Nature shaped animals for exhausting sexual competition that may be of little benefit to the species as a whole.

Finally, Darwin recognized that the agents of sexual selection are literally the brains and bodies of sexual rivals and potential mates, rather than the mindless pressures of a physical habitat or a biological niche. Psychology haunts biology with the specter of half-conscious mate choice shaping the otherwise blind course of evolution. This psychologizing of evolution was Darwin's greatest heresy. It was one thing for a generalized Nature to replace God as the creative force. It was much more radical to replace an omniscient Creator with the pebble-sized brains of lower animals lusting after one another. Sexual selection was not only atheism, but indecent atheism.

Perhaps the least appreciated irony of Darwin's life is that, despite being recognized as the major advocate of natural selection, he seems to have lost interest in the process after publishing
The Origin
in 1859. Perhaps the ease with which the young naturalist Alfred Russel Wallace independently discovered natural selection during a bout of Malaysian malaria, and the need to acknowledge Wallace as a co-discoverer, may have soured Darwin's attitude to his most famous brainchild. In any case, Darwin did not follow up
The Origin
with the sort of research his Victorian colleagues expected. He did not produce a series of detailed case studies of natural selection showing how the external conditions of organic life shape the adaptations of animals and plants.

Instead, he embarked on a seemingly peculiar quest. He wanted to understand how the senses, minds, and behaviors of organisms influence evolution. His 1862 book
On the Various Contrivances by Which British and Foreign Orchids Are Fertilized by Insects
showed how the perceptual and behavioral abilities of pollinators shape the evolution of flower color and form. In 1868 his massive

two-volume work
The Variation of Animals and Plants under Domestication
was published, in which he detailed how human needs and tastes have shaped the evolution of useful and ornamental features in domesticated species. Most provocatively, he combined sex with mind and the enigma of human evolution in his two-volume masterpiece
The Descent of Man, and Selection in Relation to Sex.
The trend continues with further works on animal emotions in 1872 and on the behavior of climbing plants in 1875. Even Darwin's final, wry insult to the doctrine of bodily resurrection, his 1881 book on how worms eat the dead to produce fertile soil, was obsessed with the evolutionary and ecological effects of animal behavior.

From
The Origin
until his death, Darwin was as much an evolutionary psychologist as an evolutionary biologist. Except for seven revisions of
The Origin
that successively weakened the role of natural selection in evolution, Darwin wrote little on natural selection. He was confident that he had established the fact of evolution (descent from a common ancestor) and the mechanism of adaptation (cumulative selection on minor heritable variations). He was also confident that other biologists would continue his work on natural selection. So Darwin turned to the really hard problem: how the mysteries of mind and matter interact over the depths of evolutionary time to produce the astonishing pinnacles of beauty manifest in nature, such as flowers, animal ornamentation, and human music.

His theory of sexual selection through mate choice was the crowning achievement of these investigations—yet it was the one most vehemently rejected by his contemporaries. In the last passage that Darwin wrote on sexual selection in
The Descent,
he portrayed mate choice as a psychological process that guides organic evolution:

He who admits the principle of sexual selection will be led to the remarkable conclusion that the cerebral system not only regulates most of the existing functions of the body, but has indirectly influenced the progressive development of various bodily structures and of certain mental qualities. Courage,

pugnacity, perseverance, strength and size of body, weapons of all kinds, musical organs, both vocal and instrumental, bright colors, stripes, and marks, and ornamental appendages, have all been indirectly gained by the one sex or the other, through the influence of love and jealousy, through the appreciation of the beautiful in sound, color or form, and through the exertion of a choice; and these powers of the mind manifestly depend on the development of the cerebral system.

Modern critics who accuse Darwin of reducing all of nature's beauty to the blind, dumb action of natural selection could not have read this far. Darwin spent decades thinking about aesthetic ornamentation in nature, realizing that natural selection cannot explain most of it, and developing his sexual selection ideas precisely to describe how animal psychology leads to the evolution of animal ornamentation.

Wallace Versus Female Choice

Alfred Wallace was an unlikely critic of Darwin's sexual selection theory. He independently discovered the principle of natural selection while Darwin was still reluctant to publish. He was even more of a hard-core adaptationist than Darwin, constantly emphasizing the power of selection to explain biological structures that seem inexplicable. He was the world's expert on animal coloration, with widely respected theories of camouflage, warning coloration, and mimicry He was more generous than Darwin in attributing high intelligence to "savages." Where Darwin was of the landed gentry and fell into an easy marriage to a rich cousin, the working-class Wallace struggled throughout his early adulthood to secure a position sufficiently reputable that he could attract a wife. One might think that Wallace would have been more sensitive to the importance of sexual competition and female choice in human affairs. One might have expected Wallace to use those insights into human sexuality to appreciate the importance of female choice in shaping animal ornamentation. Yet Wallace was utterly hostile to Darwin's theory of sexual selection through mate choice.

The fallacious criticisms developed by Wallace are worth outlining because they continue to be reinvented even now. Wallace distinguished between ornaments that grow in both sexes, and those that grow only in males. The first he explained as identification badges to help animals recognize which species others belonged to. This species-recognition function continues to be advocated by most biologists today to explain ornaments that show minimal sex differences. On the other hand, Wallace did not consider male ornaments to be proper adaptations that evolved for some real purpose. Instead, he suggested that they were unselected side-effects of an exuberant animal physiology that has a naturally predilection for bright colors and loud songs unless inhibited by the sensible restraint of natural selection.

Take a random animal, cut it in half, and you may see some brightly colored internal organs. Wallace pointed out that internal coloration cannot usually result from mate choice because skin is usually opaque. He argued that organs have a natural tendency to assume bright colors just because of their chemistry and physiology. Ordinarily, natural selection favors camouflage on the outside, so animals often look dull and drab.

Wallace then made an additional claim: the more active an organ, the more colorful it tends to be. He observed that males are generally more vigorous, and, confusing correlation with causation, he proposed that this explains why males are brighter. Male ornamentation for Wallace was the natural physiological outcome of inherently greater male health and vigor. In his 1889 book
Darwinism,
he argued, "The enormously lengthened plumes of the birds of paradise and the peacock ... have been developed

to so great an extent [because] there is a surplus of strength, vitality, and growth-power which is able to expend itself in this

way without injury." Males become even more worked up in the

mating season, which he thought explains why their ornaments grow more colorful just at the time when females happen to be

looking at them. The surplus of energy that males build up in the mating season also tends to get released in ardent songs and extravagant dances.

Females, Wallace thought, are under stronger natural selective pressures to remain discreetly camouflaged because they are so often found near their vulnerable offspring. For example, he showed that female birds that brood in open nests have usually evolved dull camouflage, whereas those that brood in enclosed nests tend to have colors as bright as the males of the species. In Wallace's view, this implied that sexual courtship by males—one of the riskiest, most exhausting, most complex activities in the animal world—must be the default state of the organism, and that the camouflaged laziness shown by young animals, female animals, and males outside the breeding season is something maintained by natural selection. He seems to have envisioned all organic tissue as bursting with color, form, song, dance, and self-expression, which the prim headmistress of natural selection must keep under control.

Wallace understood camouflage and warning coloration. He knew that the perceptual abilities of predators could influence the evolution of prey appearance. So why was he so hostile to female choice, in which the perceptual abilities of females influence the evolution of male appearance? He seems to have forgotten that half of all predators are female. If a female predator can choose to avoid prey that have bright warning colors, why should she be unable to choose a sexual partner based on his bright ornamentation?

Moreover, Wallace's alternative to mate choice begged important questions. Why would males automatically be stronger and more vital than females? Why would they waste surplus energy in such displays? Wallace's arguments along these lines were implausible, ad hoc, and untested. Yet many Victorian biologists considered them at least as plausible as Darwin's mate choice theory. Even more strangely, Wallace's energy-surplus idea foreshadowed Freud's speculation that human artistic display results from a sublimation of excess sexual energy. They also foreshadowed Stephen Jay Gould's claim, first sketched out in his 1977 book
Ontogeny and Phytogeny,
that human creative intelligence is a side-effect of surplus brain size. However, these energy-surplus