Too sexy to survive
In a mossy forest in the western Andes of Ecuador, a small, cocoa-brown bird with a red crown sings from a slim perch. Bip-Bip-WANNGG! It sounds like feedback from an elfin electric guitar. Three rival birds call back in rapid response. These male clubwinged manakins are showing off to attract female mates.
Their strange songs are associated with an even stranger movement. Instead of opening their beaks, they flick their wings open at their sides to make the Bips, and then snap their wings up over their backs to produce the extraordinary WANNGG . They are singing with their wings, and their potential mates seem to find the sound very alluring.
This is an evolutionary innovation — a whole new way to sing. But the evolutionary mechanism behind this novelty is not adaptation by natural selection, in which only those who survive pass on their genes, allowing the species to become better adapted to its environment over time. Rather, it is sexual selection by mate choice, in which individuals pass on their genes only if they’re chosen as mates. From the peacock’s tail to the haunting melodies of the wood thrush, mate choice is responsible for much of the beauty in the natural world.
Most biologists believe that these mechanisms always work in concert — that sex appeal is the sign of an objectively better mate, one with better genes or in better condition. But the wing songs of the club-winged manakin provide new insights that contradict this conventional wisdom. Instead of ensuring that organisms are on an inexorable path to self-improvement, mate choice can drive a species into what I call maladaptive decadence — a decline in survival and fecundity of the entire species. It may even lead to extinction.
To make those songs, the male club-wing needs unusual wing feathers. Those closest to his body are thickened and twisted, giving the species its name. Two are also twisted into knobs, like the handles of tiny shillelaghs, while the adjacent feather ends in a bent, sharp blade.
It took 145 years after the first description of these feathers to discover how they make their sounds. In 2005, high-speed video of singing males captured by the biologist Kimberly Bostwick in the Ecuadorean forest revealed that the male’s wing feathers oscillate over the bird’s back. With each oscillation, the blade-shaped feather rubs against the feather next to it, as if bowing a violin, causing the thickened feathers to resonate. This mechanism, called stridulation, is also used by crickets, katydids and cicadas. These birds could appropriately be called cricket-winged manakins.
But manakin beauty is not only skin deep. In subsequent research, Bostwick and colleagues demonstrated that the birds’ songs involve more than just unusual feathers and movements. They require evolutionary changes in the shape of their bones.
Avian wing bones are surprisingly uniform among species, because flight places such precise demands on the design of the wing. The 10,000 species of flying birds have tinkered only slightly with the design perfected more than 135 million years ago, when Mesozoic birds evolved the modern flight stroke.
By comparison, the wing bones in male club-winged manakins are startling. The trailing bones in the midsection of their wings, or the ulnas, are nearly unrecognizable. They are four times wider than those of other manakin species. The surface of their ulnas also features a shelf with huge bumps for the attachments of ligaments that hold the vibrating wing feathers. As far as we know, there is nothing like it in any other bird in the world.
More surprising, their wing bones are solid, while every other species of flying bird has hollow ulnas. Even velociraptors hadhollow ulnas. Sexual selection for these songs has forced male clubwinged manakins to abandon a design that predates bird flight itself.
The male club-wings cannot have it both ways: They cannot evolve simultaneously for the most efficient flight and the most beautiful wing songs. Because the birds are rare and live far from major research laboratories, we have no data yet on how their wings affect their flight. But it’s obvious they do: In the wild, it is easy to see that male club-wings fly awkwardly. Most likely they have diminished maneuverability and efficiency.
In other words, they have evolved to be worse at flying in order to be more attractive to mates.
Evolutionary biologists have tried to explain away the survival costs of sexual ornaments by imagining that beauty is an honest handicap: By surviving despite his awkward wing bones, the male is displaying his superior quality to mates with every Bip-WAANGG.
Recently, I tested this handicap hypothesis by examining the wing bones of female clubwings. Although their feathers are normal, their wing bones are not — the females’ ulnas have the same distorted shape as the males’. (They are, however, hollow in the center.)
So although they never sing, by selecting mates that produce attractive wing songs, female club-winged manakins have transformed both male and femalewing bones.
The clumsy wings of males could be rationalized as a handicap that provides information about the birds’ condition or genetic quality. But the observation that female club-wings have also probably made themselves less capable fliers can only be described as decadent — sexual selection leading to a decline in the capacity for survival.
How could this happen? Developmentally, avian wing bones take shape early in the life of an embryo, before sexual differentiation has begun. This prevents females from evolving a different wing-bone shape from males.
Of course, females do not harm their own survival by choosing males with attractive songs; the costs are deferred to their sons and daughters. Although their daughters will inherit more awkward wing bones, their sons will inherit sexually attractive songs, resulting in more grandchildren.
In the absence of direct costs to the choosers, the population will not be saved by natural selection. Because the cost is deferred, the whole population can ease further and further into maladaptive dysfunction, generation by generation.
Evolved decadence may turn out to be common. For instance, the male Wilson’s bird of paradise has a bright blue, bald crown — a disadvantage when hiding from predators, but handy when it comes to courting a female. The females have the same risky tonsure, albeit in a deeper violet hue. The male wire-tailed manakin has elongated tail feathers, which he swipes across the face of the female during courtship, and which may impede flight. Once again, the females sport the same long feathers. Even the peafowl has a longer tail than she needs.
The wing songs of the clubwinged manakin teach us that adaptation by natural selection does not control everything that happens in evolution. Some of the evolutionary consequences of sexual desire may notbe adaptive. Rather, they can be truly decadent. Despite the ubiquity of natural selection, organisms are not always getting better at surviving. Natural selection is not the only source of design in nature.
Once organisms evolve the capacity for subjective evaluation, and the freedom of choice, then animals become agents in their own evolution. One of the hallmarks of autonomy, of course, is the freedom to mess up.
Richard O. Prum is a professor of ecology and evolutionary biology at Yale and the author of the forthcoming “The Evolution of Beauty: How Darwin’s Forgotten Theory of Mate Choice Shapes the Animal World — and Us,” from which this essay is adapted.