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 th e 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 arguments make little evolutionary sense. In most species surplus energy is converted into fat, not creativity. Surplus brain-mass that yielded no survival or reproductive advantages would quickly be eliminated by selection.
If Darwin had found that male animals choose female mates selectively and that many females are highly ornamented to attract male attention, would Wallace and his contemporaries have been so skeptical about sexual choice? I think not. For male Victorian scientists, it was taken for granted that young single ladies should wear brilliant dresses and jewels to attract the attention of eligible bachelors. Male scientists had direct personal insight into male mate choice. They might easily have sympathized with male animals had Darwin credited them with powers of sexual discernment. They did sympathize with male animals engaged in violent contests with other males for the "possession" of females, which is presumably why they were able to accept Darwin's theory that male weaponry evolved for sexual competition. They simply did not like to think of males as sexual objects accepted or rejected by female choice. (This point is often overlooked by Darwin's feminist critics, who unfairly portray him as embodying Victorian social attitudes.)
The rejection of Darwin's female choice theory was, I think, due to ideological biases in 19th-century natural history, especially the unthinking sexism of most biologists other than Darwin. The rejection was cloaked in scientific argumentation, but the motivations for rejection were not scientific. Many male scientists at the time wrote as if female humans were barely capable of cognition and choice in any domain of life. Female animals were held in even greater contempt, as mere egg repositories to be fought over by males. Male scientists were willing to believe that combat between males, analogous to careerist economic competition in capitalist society, could account for many bodily and behavioral features of male animals. But they could not accept that the sexual whims of female animals could influence the stately progress of evolution.
Wallace paid a high price for his rejection of female choice. He recognized that the human mind contains many biological adaptations, such as elaborate language, music, and art, that seem impossible to explain as outcomes of natural selection for survival value. With more field experience among the primitive tribes of Oceania than Darwin ever amassed on his Beagle voyage, Wallace appreciated more acutely than Darwin how striking these adaptations were. He held the musical talents of the Pacific Islanders and African tribal peoples in the highest regard, but could find no survival value in their songs and dances. By rejecting sexual selection for ornamentation, he rejected the one process that might have explained such adaptations. Wallace found himself allied with anti-Darwinians who claimed that evolution could never account for human consciousness, intelligence, or creativity. Though he remained an evolutionist about everything else, Wallace became a creationist about the "human spirit." He went to seances. He developed interests in mesmerism and spiritualist charlatans. He died convinced that science could never fathom the origins or nature of the human mind.
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