by Michio Kaku
After graduating from Harvard in 1982, Prum traveled to Suriname to study manakins, a family of intensely colored birds that compete for mates with high-pitched songs and gymnastic dance routines. In 1984, he began graduate studies in biology at the University of Michigan, Ann Arbor, where he planned to reconstruct the evolutionary history of manakins through careful comparisons of anatomy and behavior. In the process, a colleague introduced him to some research papers on sexual selection, piquing his interest in the history of this fascinating yet seemingly neglected idea.
Darwin was contemplating how animals perceived one another’s beauty as early as his thirties: “How does Hen determine which most beautiful cock, which best singer?” he scribbled in a note to himself sometime between 1838 and 1840. In The Descent of Man, published in 1871, he devoted hundreds of pages to sexual selection, which he thought could explain two of the animal kingdom’s most conspicuous and puzzling features: weaponry and adornment. Sometimes, males competing fiercely for females would enter a sort of evolutionary arms race, developing ever greater weapons—tusks, horns, antlers—as the best-endowed males of each successive generation reproduced at the expense of their weaker peers. In parallel, among species whose females choose the most attractive males based on their subjective tastes, males would evolve outlandish sexual ornaments. (It’s now well known that all sexes exert numerous different evolutionary pressures on one another and that in some species males choose ornamented females, but to this day, many of the best-studied examples are of female preference and male display.)
Unlike natural selection, which preserved traits that were useful “in the struggle for life,” Darwin saw sexual selection as exclusively concerned with reproductive success, often resulting in features that jeopardized an animal’s well-being. The peacock’s many-eyed aureole, mesmerizing yet cumbersome, was a prime example and remains the mascot of sexual selection today. “A great number of male animals,” Darwin wrote, “as all our most gorgeous birds, some fishes, reptiles and mammals, and a host of magnificently colored butterflies have been rendered beautiful for beauty’s sake.”
Darwin’s peers embraced the idea of well-armed males dueling for sexual dominance, but many scorned the concept of animal aesthetics, in part because it was grounded in animal consciousness and female desire. In one critique, the English biologist St. George Mivart stressed “the fundamental difference which exists between the mental powers of man and brutes” and the inability of “vicious feminine caprice” to create enduring colors and patterns. The English naturalist Alfred Russel Wallace, who independently formed many of the same ideas about evolution as Darwin, was also deeply critical. Wallace was particularly tormented by Darwin’s suggestion of beauty without utility. “The only way in which we can account for the observed facts is by the supposition that color and ornament are strictly correlated with health, vigor and general fitness to survive,” Wallace wrote. In other words, ornamentation could be explained only as a heuristic that animals use to judge a potential mate’s fitness—a view that came to dominate.
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In the early 1980s, while researching the history of sexual selection, Prum read a seminal 1915 paper and a 1930 book on the subject by the English biologist and statistician Ronald Fisher, who buttressed Darwin’s original idea with a more sophisticated understanding of heredity. At first, Fisher argued, females might evolve preferences for certain valueless traits, like bright plumage, that just happened to correspond with health and vigor. Their children would tend to inherit the genes underlying both their mother’s preference and their father’s trait. Over time, this genetic correlation would reach a tipping point, creating a runaway cycle that would greatly exaggerate both preference and trait, glorifying beauty at the expense of the male’s survival. In the early 1980s, the American evolutionary biologists Russell Lande and Mark Kirkpatrick gave Fisher’s theory a formal mathematical girding, demonstrating quantitatively that runaway sexual selection could happen in nature and that the ornaments involved could be completely arbitrary, conveying no useful information whatsoever.
Although Fisherian selection was certainly not ignored, it was ultimately overshadowed by a series of hypotheses that seemed to rescue beauty from purposelessness. First, the Israeli biologist Amotz Zahavi proposed a counterintuitive idea called the handicap principle, which put a new spin on Wallace’s utilitarian explanation for sexual ornaments. Extravagant ornaments, Zahavi argued, were not merely indicators of advantageous traits as Wallace had said—they were a kind of test. If an animal thrived despite the burden of an unwieldy or metabolically expensive ornament, then that animal had effectively demonstrated its vigor and proved itself worthy of a mate. Similarly, in 1982, the evolutionary biologists W. D. Hamilton and Marlene Zuk proposed that some ornaments, in particular bright plumage, signaled that a male was resilient against parasites and would grant his children the same protection. Many scientists began to think of sexual selection as a type of natural selection. Scores of researchers joined the hunt for measurable benefits of choosing an attractive mate: both direct benefits, like better parenting or more desirable territory, and indirect benefits, namely some evidence that more alluring males really did have “good genes” underlying various desirable qualities, like disease resistance or higher-than-average intelligence.
After more than thirty years of searching, most biologists agree that although these benefits exist, their prevalence and importance is uncertain. A few compelling studies of frogs, fish, and birds have shown that females who choose more attractive males typically have children with more robust immune systems and a greater chance of survival. On the whole, however, the evidence has not equaled the enthusiasm. A 2012 meta-analysis of ninety studies on fifty-five species found only “equivocal” support for the good-genes hypothesis.
Prum thinks the evidence for the heritable benefits of choosing a beautiful mate is scant because such benefits are themselves rare, whereas arbitrary beauty is “nearly ubiquitous.” Over the years, the more he contemplated runaway selection, the more convinced he became that it was a far more powerful and creative evolutionary force than natural selection, which he regards as overhyped and boring. “Animals are agents in their own evolution,” he told me during one conversation. “Birds are beautiful because they are beautiful to themselves.”
In the summer of 1985, around the same time that biologists were rekindling their interest in sexual selection, Prum and the nature documentarian Ann Johnson (who would later choose him as her husband) traveled to Ecuador to continue studying manakins. The first morning, while hiking through a cloud forest, Prum heard odd bell-like notes, which he took to be the murmurings of parrots. Later that day, on the same trail, he heard the strange sounds again and followed them into the forest. He was astonished to find that the source was a male club-winged manakin, a small cinnamon-bodied species with a red cap and black-and-white mottled wings. The manakin was jumping around in a showy manner that suggested he was courting females. Instead of singing with his throat, he repeatedly lifted his wings behind his back and vibrated his feathers furiously against one another, producing two electronic blips followed by a shrill buzzing ring—a sound Prum transcribes as “Bip-Bip-WANNGG!”
At the time, Prum had not fully developed his evolutionary theory of beauty, but he immediately suspected that the club-winged manakin was emblematic of nature’s capacity for pushing creatures to aesthetic extremes. The bird’s singular vibrato haunted him for years. In the early 2000s, when Prum had become a professor of biology at the University of Kansas, he and his graduate student Kimberly Bostwick revealed that the demands of courtship had drastically altered the bird’s anatomy, turning it into a living violin. Male club-winged manakins had feathers with contorted shafts that rubbed against each other 100 times a second—faster than a hummingbird beats its wings. Whereas a vast majority of birds have light, hollow bones in service of flight, Bostwick has recently shown via CT scans that male club-winged manakins have
solid ulnas—wing bones—which they need to withstand the intense quivering. Female manakins have inherited related anomalies as well.
Although there are no published studies of the club-winged manakin’s aeronautics, Prum says it’s obvious from observation that the birds fly awkwardly—even the females. The self-perpetuating pressure to be beautiful, Prum argues, has impeded the survival of the entire species. Because the females do not court males, there can be no possible advantage to their warped bones and feathers. “Some of the evolutionary consequences of sexual desire and choice in nature are not adaptive,” Prum writes in his recent book. “Some outcomes are truly decadent.”
In the following decade, as Prum’s hearing declined, he withdrew from field research and birding, but he still managed to make a series of groundbreaking scientific discoveries: he helped confirm that feathers evolved in dinosaurs long before the emergence of birds, and he became one of the first scientists to deduce the colors of a dinosaur’s plumage by examining pigment molecules preserved in fossilized feathers. All the while, he never stopped thinking about sexual selection. Prum formally presented his theory of aesthetic evolution in a series of scientific papers published between 1997 and 2015, proposing that all sexual ornaments and preferences should be regarded as arbitrary until proven useful.
Despite his recent Pulitzer nomination, Prum still stings from the perceived scorn of his academic peers. But after speaking with numerous researchers in the field of sexual selection, I learned that all of Prum’s peers are well aware of his work and that many already accept some of the core tenets of his argument: namely that natural and sexual selection are distinct processes and that, in at least some cases, beauty reveals nothing about an individual’s health or vigor. At the same time, nearly every researcher I spoke to said that Prum inflates the importance of arbitrary preferences and Fisherian selection to the point of eclipsing all other possibilities. In conversation, Prum’s brilliance is obvious, but he has a tendency to be dogmatic, sometimes interrupting to dismiss an argument that does not agree with his own. Although he admits that certain forms of beauty may be linked to survival advantages, he does not seem particularly interested in engaging with the considerable research on this topic. When I asked him which studies he thought offered the strongest support of “good genes” and other benefits, he paused for a while before finally responding that it was not his job to review the literature.
Like Darwin, Prum is so enchanted by the outcomes of aesthetic preferences that he mostly ignores their origins. Toward the end of our bird walk at Hammonasset Beach State Park, we got to talking about club-winged manakins. I asked him about their evolutionary history. Prum thinks that long ago, an earlier version of the bird’s courtship dance incidentally produced a feathery susurration. Over time, this sound became highly attractive to females, which pressured males to evolve adaptations that made their rustling feathers louder and more noticeable, culminating in a quick-winged strumming. But why, I asked Prum, would females be attracted to those particular sounds in the first place?
To Prum, it was a question without an answer—and thus a question not worth contemplating. “Not everything,” he said, “has this explicit causal explanation.”
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Prum’s indifference to the ultimate source of aesthetic taste leaves a conspicuous gap in his grand theory. Even if we were to accept that most beauty blooms from arbitrary preferences, we would still need to explain why such preferences exist at all. It’s entirely conceivable that an animal might be inherently partial to, say, a warbling mating call or bright yellow feathers, and that these predilections would have nothing to do with advantageous genes. Yet such inclinations are inarguably the product of an animal’s neurobiology, which is itself the result of a long evolutionary history that has adapted the animal’s brain and sensory organs to specific environmental conditions. In the past two decades, a cohort of biologists have dedicated themselves to studying how an animal’s “sensory bias”—its ecological niche and its particular way of experiencing the world—sculpts its appearance, behavior, and desires. Like Prum, they don’t think beauty has to be adaptive. But where Prum celebrates caprice, they seek causality.
Molly Cummings, a professor of integrative biology at the University of Texas at Austin, is a leading researcher in the field of sensory ecology. When I visited her last spring, she drove us to one of her field laboratories: a grassy clearing populated with several large concrete basins. The surface of one basin was so packed with woolly algae and pink-flowered water lilies that we could hardly see the water. Cummings began pushing some of the vegetation out of the way, forming shady recesses that permitted our gaze at the right angle. “Let me see if I can find a big, beautiful boy,” she said.
A paper-clip-size fish swam toward us. I leaned in for a closer look. His silver body was decorated with a single black dot and a stripe of iridescent blue; his lengthy tail, shaped like a knight’s blade, was streaked with yellow. “Oh, yeah, there’s a guy courting,” Cummings said. “He’s coming up to that female, trying to impress her.” The fish, a male swordtail, seemed almost manic in his effort to be noticed. He darted back and forth in front of the female, shimmying as he went, his scales reflecting whatever light managed to breach the murk.
A little while later, we drove the few miles back to her campus laboratory, where shelves of fish tanks lined several rooms and Ernst Haeckel’s resplendent illustrations of jellyfish undulated across the walls. As we toured the facilities, Cummings told me about the arc of her career. While an undergraduate at Stanford University, she spent a summer scuba diving in the giant kelp forests at Hopkins Marine Station, adjacent to the world-renowned Monterey Bay Aquarium. After college, she moved to James Cook University in Townsville, Australia, where she studied marine ecology and discovered the work of the biologists John Lythgoe and John Endler, both of whom were interested in how the type of light in an animal’s environment shaped its visual system.
Cummings thought about the fish she had observed in California and Australia. She was astounded by the dynamic beauty of surfperch in the kelp forest: the way they communicate through the color and brightness of their skin, flashing blue, silver, and orange to attract mates. Equally impressive was the diversity of their aquatic habitats. Some patches of water were sparkling and clear; others were cloudy with algal muck. In Australia, sunlight bathed the many vibrant species of reef fish almost constantly, but they lived against a kaleidoscopic backdrop of coral. How did fish evolve effective and reliable sexual ornaments if the lighting and scenery in their homes were so variable?
After earning a postgraduate degree in Australia in 1993, Cummings began a PhD at the University of California at Santa Barbara. For several years, she studied various species of surfperch, repeatedly diving in the kelp forests with a Plexiglas-protected spectrometer to quantify and characterize the light in different habitats. At night, she would use powerful diving lights to stun surfperch and take them back to the lab, evading the hungry seals that routinely trailed her in hopes of making a meal of the startled fish. After hundreds of dives and careful measurements, Cummings discovered that water itself had guided the evolution of piscine beauty. A female’s preference for a blaze of silver or blue was not arbitrary; it was a consequence of the particular wavelengths of light that traveled farthest through her underwater niche. Whichever males happened to have scales that best reflected these wavelengths were more likely to catch the eye of females.
In her studies, Cummings showed that surfperch living in dim or murky waters generally preferred shiny ornaments, while surfperch inhabiting zones of mercurial brightness favored bold colors. Later, Cummings found that Mexican swordtails occupying the upper layers of rivers, where the clear water strongly polarized incoming sunlight, had ornaments that were specialized to reflect polarized light—like a stripe of iridescent blue. These findings parallel similar studies suggesting that female guppies in Trinidad prefer males with orange patches because th
ey first evolved a taste for nutritious orange tree fruits that occasionally fell into the water. “Some people think female preferences just somehow emerge,” Cummings say, “but what has been overlooked is that in many cases, it’s a result of environmental constraints. It’s not always random.”
What a creature finds attractive depends on more than the unique qualities of its environment, however; attraction is also defined by which of those qualities cross the threshold of awareness. Consider the difference between what we see when we look at a flower and what a bumblebee sees. Like us, insects have color vision. Unlike us, insects can also perceive ultraviolet light. Many plants have evolved flower parts that absorb or reflect ultraviolet light, forming patterns like rings, bull’s-eyes, and starbursts. Most creatures are oblivious to these ornaments, but to the eyes of many pollinators, they are unmistakable beacons. There is an entire dimension of floral beauty invisible to us, not because we are not exposed to ultraviolet light, but because we do not have the proper biological hardware to perceive it.
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Michael Ryan, a professor of zoology whose lab and office are just a few floors below Cummings’s, has spent more than thirty years investigating how the quirks of an animal’s anatomy determine its aesthetic preferences—a career he details in his recent book, A Taste for the Beautiful. Since 1978, Ryan has been traveling to Panama to study a mud-colored frog called the túngara. Like the club-winged manakin, the túngara has a unique form of beauty that is not visual but aural. At dusk, male túngara frogs gather at the edges of puddles and sing to seduce females. Their mating call has two elements: the main part, dubbed the whine, sounds precisely like a miniaturized laser gun; sometimes this is followed by one or more brief barks, known as chucks. A long and complex mating call is risky: it attracts frog-eating bats. Yet there is a high payoff. Ryan has shown that whines followed by chucks are up to five times as appealing to females as whines alone. But why?
