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 byWhich 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.
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