Evolution: Sexual Selection and Aesthetic selection
A little over a decade after he published “On the Origin of Species,” in which he described his theory of natural selection shaped by “survival of the fittest,” Darwin published another troublesome treatise — “The Descent of Man, and Selection in Relationship to Sex.” This expanded on an idea he mentioned only briefly in “Origin.” Sometimes, he proposed, in organisms that reproduce by having sex, a different kind of selection occurs: Animals choose mates that are not the fittest candidates available, but the most attractive or alluring. Sometimes, in other words, aesthetics rule.
Darwin conceived this idea largely because he found natural selection could not account for the ornaments seen in many animals, especially males, all over the world — the bright buttocks and faces of many monkeys and apes; the white legs and backside of the Banteng bull, in Malaysia; the elaborate feathers and mating dances of countless birds including bee-eaters and bell-birds, nightjars, hummingbirds and herons, gaudy birds of paradise and lurid pheasants, and the peacock, that showboat, whose extravagant tail seems a survival hindrance but so pleases females that well-fanned cocks regularly win their favor. Only a consistent preference for such ornament — in many species, a “choice exerted by the female” — could select for such decoration. This sexual selection, as Darwin called it, this taste for beauty rather than brawn, constituted an evolutionary mechanism separate, independent, and sometimes contrary to natural selection.
To Darwin’s dismay, many biologists rejected this theory. For one thing, Darwin’s elevation of sexual selection threatened the idea of natural selection as the one true and almighty force shaping life — a creative force powerful and concentrated enough to displace that of God. And some felt Darwin’s sexual selection gave too much power to all those females exerting choices based on beauty. As the zoologist St. George Jackson Mivart complained in an influential early review of “Descent,” “the instability of vicious feminine caprice” was too soft and slippery a force to drive something as important as evolution.
Darwin’s sexual selection theory thus failed to win the sort of victory that his theory of natural selection did. Ever since, the adaptationist, “fitness first” view of sexual selection as a subset of natural selection has dominated, driving the interpretation of most significant traits. Fancy feathers or (in humans) symmetrical faces have been cast not as instruments of sexual selection, but as “honest signals” of some greater underlying fitness. Meanwhile, the “modern synthesis” of the mid-1900s, which reconciled Darwinian evolution with Mendelian genetics, redefined evolutionary fitness itself not in terms of traits, but as the survival and spread of the individual genes that generated the traits. Genes, rather than traits, became what natural selection selected.
And so things largely remained until now. This summer, however, almost 150 years after Darwin published his sexual selection theory to mixed reception, Richard Prum, a mild-mannered ornithologist and museum curator from Yale, has published a book intended to win Darwin’s sex theory a more climactic victory. With , Prum, drawing on decades of study, hundreds of papers, and a lively, literate, and mischievous mind, means to prove an enriched version of Darwin’s sexual selection theory and rescue evolutionary biology from its “tedious and limiting adaptationist insistence on the ubiquitous power of natural selection.” He feels this insistence has given humankind an impoverished, even corrupted view of evolution in general, and in particular of how evolution has shaped sexual relations and human culture.
As Prum knows, he’s in for a fight. The biologists who most militantly defend the adaptationist Darwinian view of evolution, such as Richard Dawkins, do not gladly suffer dissent. But true to his argument, Prum seeks to prevail less through brute force of attack than by making his case with clarity, grace and charm. Like a bowerbird arranging its display for potential mates, he seeks not to best his chesty, chattering rivals, but to persuade the open-minded. The result is a delicious read, both seductive and mutinous.
Richard Prum is first and foremost an obsessive birder. Having personally seen over a third of the world’s 10,000 known bird species, he draws on his observations and wide reading to defeather and gut the adaptationist view that beauty is an “honest signaling” of evolutionary fitness. His attention never strays far from nature, and his writing in these bird passages is minutely detailed, exquisitely observant, deeply informed, and often tenderly sensual. When describing, say, the “throbbing” display of the lavishly decorated argus bird, he delivers a feathery brush of the erotic.
Prum is also an expert on the evolution of feathers, and he writes of them with the insight and appreciation one hears in the funnest art critics — think Kenneth Clark crossed with Sister Wendy. Prum makes an elegant, plausible argument that rather than having evolved for flight, feathers may actually have first evolved as a decorative surface for sexual display: fitness as a downstream benefit of beauty. The art-critic overtones come not by chance. Prum considers birds artists. Manakins (Prum’s study group) carefully choreograph their dances. Bowerbirds mastered perspective in their bower building eons before human painters grokked it during the Renaissance.
Bowerbird males provide Prum some of his most convincing examples. These remarkable birds woo their potential mates by constructing circles, cones, or maypole-like structures out of twigs, then ornamenting both the structures and the ground within and around them with stones, shells, beetle cases, colorful fungi and other found art. Both the architecture and the male’s behavior invite the female to observe and consider while leaving her both the space to do so and a clear escape path. In some bowerbird species the male laboriously arranges and rearranges his display, examining it from various angles and making small fixes, writes Prum, with the care of a “fussy florist.” The males of several species observe the female examining their work while half-hidden behind a tree or some fencelike part of the bower. If she likes what she sees, she stretches her neck and raises her tail in invitation, and the male comes to mate. (This takes only seconds, and the two will never meet again.) If she doesn’t, she leaves.
Prum believes these and similar courtship appeals in other species have arisen from a long, multigenerational, co-evolutionary conversation between mating partners. The male’s aesthetic and social qualities are repeatedly tested, judged and (through selection) modified according to whether they please potential mates. Thus the females’ individual preferences, says Prum, help drive evolution.
Like all selection, this is not intended to reach any particular goal; it just unfolds according to the demands of either fitness, or in this case, beauty. A trait selected for its beauty, of course, might create problems by selecting for ornaments that work against fitness. But, most crucially in the end, and often offsetting these problems, this “aesthetic” courtship, says Prum, creates an environment, temperaments and rituals — a sort of culture — that give the female sexual choice, autonomy and safety. (As noted, she doesn’t get ; once she and the male mate and part, she raises the offspring by herself.)
Prum sees such aesthetic choices as driving a gradual “aesthetic remodeling” — an evolutionary reshaping of mating behavior, and even of male social behavior more widely, by the civilizing pressure of female preference. Prum stresses this is not about emasculating males, or dominating them; it’s simply about selecting for males who allow females autonomy and choice.
By this point in the book, Prum, having made his case so well in birds, turns to the implications of sexual selection for Homo sapiens. He nimbly mines both the animal and human literature to show how, for one human trait after another, adaptationist explanations miss the mark while aesthetic explanations hit home. His catalog of Things Natural Selection Can’t Explain but Sexual Selection Easily Can includes homosexuality, a tendency toward monogamy, both sex’s taste and capacity for sex outside of female fertility periods, the deweaponization of the human male through the evolutionary shrinkage of almost every body part except the brain and the evolution of human paternal care, which is highly unusual among our fellow apes and close primate cousins. To name just a few.
Consider, for instance, this handful of well-known distinguishing human traits: our constant interest in sex, permanent breasts, big penises, and, last but hardly least, women’s orgasms. Except for constant sexual interest (and possibly female orgasm) in bonobos, none of these traits evolved in our fellow ape species. Prum argues that they evolved in humans because they help women evaluate men’s prosocial-pleasure potential. When sex offers orgasm at relatively low pregnancy risk, it provides a way not just to reproduce but to assess potential mates’ attention to female desires, tastes and choices. Essentially, Prum says, humans evolved to negotiate and have sex as a sort of display ritual. The boudoir is our bower.
One of Prum’s takeaways is that, given all this, we have choices to make. All sexual selection, he says, is shaped by conflicts between male and female anatomy, physiology, and agendas. Prum argues that sexual species tend to evolve toward one of two responses to this conflict. One evolutionary response is for males to use greater size to control or coerce the female and curb her power over whether, with whom, and how often she will mate and reproduce. This approach is common in many duck species and gorillas, whose dominant males use the threat of force to command exclusive mating access to the females in their groups and of their predecessors. The other evolutionary answer is the aesthetic route — the resolution of differences between male and female needs and desires by behaviors and rituals that respect the other sex’s priorities and their decisions about how to pursue them.
Prum proposes that we humans have evolved along the latter path, and that, given our powers of thought, conscience and agency, we can accelerate that aesthetic and social evolution. This, he asserts, is why beauty should not be seen as merely the stamp of quality assurance that conventional evolutionary theory thinks it is. Beauty, rather, forms the foundation of an entire, complex evolutionary dynamic — one that can influence how we treat each other.