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 THE EVOLUTION OF BEAUTY (Doubleday, $30), 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.