The bird-filled world of Richard Prum

Gopal Vijayaraghavan

A white-bellied sea eagle. View full image

If you observe nature closely, says Prum, you will find out what questions to ask. He made several important discoveries by taking his cue from a couple of dead birds from Madagascar.

He’d asked his colleague Steve M. Goodman to send him specimens of a small creature called a velvet asity. This was in 1991, when Prum was a newly hired professor at the University of Kansas. He was studying the anatomy of the syrinx—the avian vocal organ—in groups of related birds, and he had borrowed all four of the world’s known sets of velvet asity parts, preserved in jars in museums. Since they dated from the 1920s, he needed fresh specimens. But the two male birds that arrived puzzled him: they didn’t match the detailed notes on their tags. Goodman had described the fleshy lobes (or wattles) over the birds’ eyes as brilliant fluorescent green. But they weren’t remotely green. They were blue.

Prum began to investigate the color change. He knew that the blue of birds’ skin and feathers is produced not by pigments, but by tiny structures that scatter light waves in a way that favors a particular hue. This “structural color” would explain things—if the wattles had always been blue. Prum remembers thinking: “This doesn’t make sense.”

In solving the mystery, he discovered a new mechanism of avian structural color. The wattles, he showed, had gotten their original green from nanostructures made of parallel collagen fibers. Prum was the first to describe the structures and show how they selectively scatter green light to make it visible. And he found out that the reason those collagen fibers in Goodman’s velvet asities scattered blue light, instead of green, was that the birds had become dehydrated on the trip from Madagascar, and their skin cells had shrunk.

His work on the wattles opened up an entirely new area of investigation for Prum: the physics of color. He began a long-running partnership with Kansas mathematician Rodolfo Torres. Together they analyzed the asity’s wattles and the blue of the plum-throated cotinga. They also discovered that shades of ultraviolet occur in avian skin. Eventually, Avian Field Studies even came to include some non-avians, as Prum and colleagues studied structural color in dragonflies, butterflies, and mammals, like the vivid blue of the vervet monkey’s scrotum.

Prum’s career as a field biologist ended early. In the mid-1990s, he began to lose the hearing in his “bionic” left ear to Ménière’s disease, a progressive autoimmune disorder that he thinks was a reaction to his Senegal virus. Ann Johnson Prum remembers that period as “a slow bleed.” The Ménière’s gave her husband bouts of vertigo that left him nauseated and bedridden for as long as three days. During one bad spell, when she was off filming in Antarctica, he had to call a neighbor to care for their three sons.

In October 1998, Prum went to Madagascar to follow up on field studies of velvet asities he’d done four years earlier. He took a team of researchers to a trail where he’d banded some birds and was elated to find one of the banded asities right away. “I lift up the binoculars, and there he is, and I’m showing all these guys their first velvet asity. He opens up his mouth and goes”—a silence—“and I couldn’t hear a damned thing. I knew that my hearing loss had started, but I didn’t realize this bird, whose song I had described to science, was now inaudible to me.”

Ann Prum says that early in his illness, her husband would dream that he could hear birds singing. The dreams have stopped. But “what’s really haunting,” says Rick Prum, “is that I spent decades learning bird songs. I can identify hundreds of bird songs that it’s impossible for me to hear.”

At first he worried about how he could progress in his career. Gradually, “I realized that the challenge for me was to connect—to reconnect—myself to my life’s work in a new way. Fortunately, it was right at the time when I was already starting to be intrigued by structural color and then, later on, by the origin of feathers.”

Prum’s groundbreaking work on feather evolution began under duress. On the night he taught himself how feathers grow, his only goal was to make it through the next morning’s ornithology lecture. He was a new assistant professor at Kansas, and he couldn’t imagine why he’d included feather development in his syllabus.

“What was I thinking? Because in fact I didn’t know anything about the topic.” Feather development had never interested him in the least. “It was a Sunday night. We had a new baby at home, nobody’s sleeping, and I’m far behind—typical disorganized professor—and I cracked open Lucas and Stettenheim [1972], perhaps one of the most boring books in the history of ornithology, and I tried to understand what was going on. When I finally did understand, it was just phenomenal.” Since that day, Prum says, he has been “totally obsessed with feathers.”

Like human hair, fingernails, porcupine quills, and reptile scales, feathers are organs of the skin made of durable proteins called keratins. Unlike these structures, however, a growing feather is tubular. It begins with a thickening of the bird’s skin that elongates into a tube. As the feather cells mature, die, and harden, they are pushed up by the live cells below, and the branching feather gets longer. Throughout, the outermost layer of the tube provides protection. In the final step, this protective sheath disintegrates, and the feather unfurls. Prum has described this process as “an elaborate choreography that is one of the wonders of nature.”

Two days after first teaching how feathers develop, he lectured on how they evolved. “I basically repeated what was a very cloudy twentieth-century view. And I criticized it, saying that it doesn’t make sense for a bunch of reasons. But it’s not like I had an alternative.”

The theory Prum repeated was that feathers first formed from the scales of ancient reptiles: as the scales of these reptiles evolved, they grew longer, then frayed, and gradually altered to form feathers. The underlying assumption was that scales had evolved into proto-feathers so that early birdlike creatures could glide, and those proto-feathers gradually became more complex so that the proto-birds could fly.

But as he stood at the chalkboard, Prum recognized a problem. Scales couldn’t have evolved into feathers, because the two grow quite differently. A scale is basically a flat outgrowth of epidermis with top and bottom surfaces. But a feather is “totally tubular,” as Prum likes to say: a hollow tube of epidermis with dermis in the middle. Given the complex way branched feathers grow, when a feather unfurls, cells from the outer surface of the tube become the top or outer side of the feather, while cells from the inner surface of the tube become the underside of the feather. This difference in development means that elongated scales could not have evolved into feathers. “Like they say in the old Bert and I records,” he offers, imitating a heavy Down East Maine accent, “You cahn’t get they-ah from hee-ah.”

By the second time Prum taught ornithology at Kansas, two years later, he had worked out his own theory of feather evolution, drawing on the way modern feathers develop. This time, he told his students that feathers didn’t come from scales. They evolved from the skin in several stages. Each stage produced an evolutionary leap (what biologists call an evolutionary novelty), and each stage made the emergence of the next novelty possible. In time, the process orchestrated increasingly diverse structures: first a hollow tube, then tufted down, and then further changes, culminating in modern-looking feathers—including the wing feather, with its asymmetrical shape conducive to flight. The early feathers may have provided insulation or added color, but Prum reasoned that they must have emerged long before flight; the first feathers that could function as flight feathers didn’t evolve until “way, way down the line.”

At the end of the feather evolution lecture, a Chinese graduate student named Zhou Zhonghe (now a prominent Chinese paleontologist) approached Prum and said, “You should write this stuff up.” Zhou had actually seen fossils with dinofuzz—the same ones Prum would examine at the Peabody two years later—but at that time they were known only to a small group of Chinese scientists. Prum had predicted the existence of dinofuzz without ever seeing it. “I had a complete theory of the evolution of feathers in my class notes,” he says. He wrote it up in 1999, and it has become the mainstream view.

Not that everyone agrees. University of Kansas paleontologist Larry Dean Martin, for instance, believes that birds divided out of the family tree early in the late Triassic period, long before the time of the theropods found in China. Furthermore, he doesn’t subscribe to Prum’s theory, because “it’s unlikely that some of the proto-feather structures that he based it on are in fact feathers.” But as more and more feathered dinosaur fossils turn up, most ornithologists have signed on to the theory of the theropod origin of birds.

By the time Prum was hired at Yale, in 2004, his left ear was “totally fired out.” The vertigo of Ménière’s had stopped, but now all he had was the ear that had been damaged in Senegal.

In the late ’90s, he had begun taking flute lessons, but three years on, he realized he couldn’t hear the notes he was playing. “It was louder through the bone conduction through my jaw than it was through the air. So I had to quit. And I really went into mourning.” People often ask him if there’s a silver lining to his near-deafness. The answer: “No. I think it’s totally bad.”

But he recovered. Four months after he gave up flute, he took up the cello, a more difficult instrument for most novices. But starting a musical instrument in midlife is the kind of thing Prum thrives on. “Here I am—I’m very accomplished in what I do”—but as a beginning musician, “I realize that I suck at this. It’s incredibly humbling. I think every adult ought to do this regularly. Do something new.”

It’s the same in the lab: Prum feels exhilarated when he enters new territory. Ann Prum says that’s when her husband is most likely to rush into the house in the evening, “eyebrows all flashy,” and talk animatedly about his work.

That has been happening often recently. Last year Prum and graduate student Vinodkumar Saranathan booked time at a particle accelerator in Illinois to figure out how birds’ feather cells build structures that scatter blue light. They found that the structures self-assemble: like bubbles rising in champagne, beta-keratin protein separates from a cellular soup during feather formation, and then organizes into lattices. Since that discovery, Prum has been working with a team of engineers and physicists to develop a blue paint that will get its hue from structural color.

Another project: detective work on dinosaur coloring. A team including Yale graduate student Jakob Vinther ’08MPhil and paleontologist Derek Briggs analyzed the fossilized pigment granules in the feathers of a Jurassic dinosaur to map its coloration. The pigeon-sized Anchiornis huxleyi turns out to have had a rust-colored crest, black-and-white wing feathers, and grey legs trailing long feathered fringes—like a woodpecker crossed with a chicken. Toys ’R’ Us, take note.

Prum’s most flamboyant venture into new territory is his theory-in-progress of beauty. The work began with his studies of manakins, which “lek” to find mates: the males gather in one place to show off their acrobatic displays and striking plumage, trying to attract females. According to the mainstream theory of how sexual selection evolves, sexually attractive traits provide information about genetic fitness. In males courting females, those traits might include a moonwalk or an eye-catching golden feather hairdo, if you are a manakin; or an exceptionally flamboyant train if you are a peacock; or a chiseled jaw and symmetrical face if you are a Homo sapiens.The “honest signaling” theory holds that these good looks advertise such reproductive advantages as robust health or a high sperm count. But from an early point in his career, Prum found himself doubting that the traits embody much “honest” information.

In a 1997 paper, he showed that the honest signaling model doesn’t fit manakin males, because of the speed (and other factors) with which they’ve evolved their wildly diverse ornamental plumage and aerial performances. Prum argued instead for a theory put forward in 1915 by the eminent English biologist Ronald A. Fisher: that females prefer some male traits not because they might promote survival of future offspring, but simply because they’re attractive. (One possible example of the “Fisherian process” is the peacock’s tail—a heavy, calorie-intensive, highly visible ornament that hardly helps a male peacock escape from its predators.)

Over time, as Prum talked with colleagues about his interest in Fisher’s now-unfashionable theory, he consistently met resistance. Many thought the idea that a species could evolve complex traits for no particularly sensible reason was just too arbitrary. “People would say to me, when they finally understood my idea, ‘But that’s nihilism.’” At first Prum didn’t understand this reaction to a concept he found entirely fulfilling. And then he recognized that he had left something out—“that what it really was about was beauty.”

This realization brought Prum into the field of aesthetic philosophy. He hasn’t published on his ideas yet, but he is at work on an article that will take on age-old questions: “What is beauty, what is art? How does aesthetic change happen? What determines what is good?”

He proposes “that art is a form of communication that co-evolves with its evaluation.” Take Mozart: he transformed the formulas of classical music so skillfully that he changed the musical tastes of his audience. In turn, as Mozart’s patrons flocked to his concertos and operas, they influenced his compositions. The result was “an ongoing aesthetic process which is the co-evolution or the historical entrainment of production and evaluation.” Art is, Prum says, “a kind of dance.”

And he is thinking not only of the aristocracy of late-eighteenth-century Vienna, but also of manakin females. He believes sexual selection is only rarely influenced by information about genetic fitness encoded in a physical feature or courtship behavior. Honest signaling plays a role, “but it’s not a complete story.” (As he put it in a 2010 essay in the journal Evolution: “I do not claim that the ‘Emperor wears no clothes.’ Rather, I would predict that the ‘Emperor wears a loincloth.’”) Sexual choices in birds and other animals stem mostly, he says, from a preference for the “merely beautiful.”

These are profound, somewhat unsettling ideas: golden-winged manakins have taste? Vervet monkeys appreciate art? But Prum isn’t trying to argue that manakins or vervets have minds like humans’, or experience beauty in the same way we do. Rather, “the process is the same. Every time you find co-evolution between advertisement or expression and evaluation, then I propose that you have art. And that means that flowers are art, most of them; and that birdsong is art; and lots of aspects of bird plumage are art. And crickets chirping.”

During his 12 years at Kansas, Prum wondered if he’d ever be recognized for his research. “There was a time when I felt like, ‘Oh, I’m too behavioral for that evolution job. And I’m too systematic for that behavioral job. I’m too evolutionary for that museum position. And now I’ve got this physics stuff: what the hell is that?’ And it never added up. It looked kind of fragmented.”

Then in 2004, he was hired by Yale, and in 2009, he received the MacArthur award—both signal career validations. The MacArthur citation even praised his meandering itinerary: “Prum habitually synthesizes concepts from disparate fields and follows surprising paths to reach carefully reasoned conclusions.”

He now believes that the multidisciplinary approach is “the way science will progress in the next bunch of years.” It has come naturally to Prum, who has been led by “nature’s delightful unexpectedness,” he says. “The birds are my muse.”