Red Deer stand in in Richmond Park in London. The ornithologist Richard Prum argues that beauty, song and and genetic fitness are not always entwined. (Dan Kitwood/Getty Images)

Nick Romeo is a critic and journalist whose work has appeared in the New Yorker, the New Republic, and other publications.

Can female preferences shape the behavior and appearance of males? This is a scientific question with a long, controversial history.

Shortly after the 1871 publication of Charles Darwin’s “The Descent of Man,” a biologist named St. George Mivart wrote a review criticizing its proposed theory of sexual selection: Mivart refused to believe that the preferences and choices of females could constitute a selective pressure that shaped the behavior and physiology of male animals. Relying more on Victorian male prejudice than scientific reasoning, Mivart concluded that “the instability of vicious feminine caprice” could never shape the evolution of males.

Darwin, however, believed that female preferences could in fact shape the evolution of ornamental traits in males (deer antlers, peacock feathers and the like). He even described sexual selection occurring through the mechanism of female agency: “The male Argus Pheasant acquired his beauty gradually through the preference of the females during many generations for the more highly ornamented males,” he wrote in “Descent.”

"The Evolution of Beauty: How Darwin's Forgotten Theory of Mate Choice Shapes the Animal World - and Us," by Richard O. Prum (Doubleday)

Darwin’s was a minority opinion, and it remains one to this day. Alfred Russel Wallace, the co-discoverer of evolution by natural selection, first articulated what has become a dominant view — that female animals simply prefer traits that are proxies for health and fitness. Beauty, in short, is just a sign of good genes, and females select mates on this basis alone.

A new book by Yale University ornithologist Richard O. Prum revives and expands Darwin’s provocative notion that beauty and genetic fitness are not always entwined. In “The Evolution of Beauty: How Darwin’s Forgotten Theory of Mate Choice Shapes the Animal World — and Us,” Prum develops a theory of aesthetic evolution that shows how the females of many species select male traits not for their fitness value but simply because they are pleasing.

This might sound like an esoteric distinction within evolutionary biology, but its consequences are far-reaching. If animals prefer mates based on criteria that are not simply proxies for genetic fitness, then evolution is a far more expansive process than generally imagined. It can even accommodate some maladaptive features and behaviors, so long as they have sufficient aesthetic appeal.

Darwin and Prum present evolution as more than an engine that selects organisms with adaptive advantages. They claim that sexual selection operates in part through individual aesthetic preferences for songs, dances, displays, ornaments and even behaviors. Animals are not only shaped by the natural world, they also shape their own evolution through their preferences.

It makes sense that an ornithologist would be a champion of the aesthetic dimensions of evolution. Prum has observed more than a third of the roughly 10,000 species of birds in the world. The vast variety of distinctive avian colorations and song patterns is difficult to explain solely in terms of adaptive fitness. The club-winged manakin, for instance, is a species from the Ecuadorian Andes that “sings” by rubbing its wings together at high frequencies. These wing songs require evolutionary changes that are actually maladaptive. While other species of birds have hollow bones, the club-winged manakins have solid ulnas that help enhance the sound production of their wing songs. This decreases their flight capacity and efficiency, but these disadvantages seem to be offset by the mating opportunities that the songs create.

This is just one of many examples. Spotted bowerbirds from Australia have precise preferences for the types and colors of materials they use to build bowers, the ornamental structures they use to attract mates. One species favors a particular shade of royal blue, while another uses an optical illusion known as forced perspective that makes objects appear to be a different size than they actually are. The birds are not simply advertising their physical strength by collecting bower construction materials that are more difficult to find. They use very common materials — the skill is in the arrangement. “There is no compelling evidence that bower decorations are costly, honest signals of male quality,” Prum writes. “Rather, they appear to vary like any other aesthetic styles among species.” Males with better-constructed and more elaborately decorated bowers are rewarded with more mating opportunities.

The particulars of avian architecture, courtship dances and songs are thus somewhat contingent and arbitrary. Rather than functioning as signals of health or genetic quality, these complex behaviors develop over generations through the selective pressure of countless individual choices by avian females. Prum argues convincingly that the subjective experience of animals — the pleasure they take in aesthetic display — is a major evolutionary force. What is less clear and never really considered is whether animals are conscious of this pleasure and what it means when we say they experience beauty.

Prum opens his argument with avian examples, but he closes it by considering how the same principles might have shaped human evolution. He speculates that a broad range of features and behaviors — such as deweaponized canine teeth, eyebrows and pubic hair — may have originated through aesthetic evolution. Perhaps human females preferred some of these traits in males on purely aesthetic grounds: It’s hard to account for eyebrows as a highly functional indicator of genetic quality.

Prum is particularly eager to emphasize the role that female mating preferences may have played in human evolution, as if feminist arguments were simply waiting for the imprimatur of a biologist. While some of these conjectures are more plausible than others, the book is a major intellectual achievement that should hasten the adoption of a more expansive style of evolutionary explanation that Darwin himself would have appreciated.

The evolution of beauty
How Darwin’s Forgotten Theory of Mate Choice Shapes the Animal World — and Us

By Richard O. Prum Doubleday. $30