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Ornithologist is Reshaping Ideas of How Beauty Evolves

After illness made him deaf to birdcalls, Richard Prum became the first to reconstruct the plumage of feathered dinosaurs and trace the evolution of feathers to beauty instead of flight.

By Veronique Greenwood
Apr 5, 2013 5:00 AMNov 12, 2019 6:10 AM
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Mark Ostow

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Growing up in southern Vermont, Richard Prum developed an ear for birdcalls and learned from the ladies of the local garden club how to tell a warbler from a migratory hawk. Opening a field notebook at random, the Yale University evolutionary ornithologist puts his finger on the day — Nov. 17, 1974 — when he first went bird-watching at the ocean and added 20 new species to his “life list,” bringing the count to 182. That day in the seventh grade, he says, “was the greatest of my life. I’ve spent a huge amount of effort reliving that in greater depth.”

The thrill of the hunt has never faded. After graduating from Harvard in the 1980s, he set off to study South American manakins, whose courtship behaviors had never been fully described. He spent his graduate school career, and many years beyond, constructing a family tree showing how every species of manakin had evolved. 

After a brilliant early career traveling the globe to record avian mating songs and dances, a devastating hearing loss forced Prum to set aside fieldwork. A less bird-obsessed man might have quailed, but Prum re-emerged with a string of discoveries that have reshaped the field’s understanding of such fundamental questions as what feathers are for and how mating rituals drive avian evolution.

If one trait has defined Prum’s scientific pursuits, it is his insistence on rejecting scientific dogma and finding answers from nature itself. Partly in recognition of his skill at bridging disciplines, Prum was awarded a MacArthur Foundation genius grant in 2009. 

Recently, Prum sat down with DISCOVER correspondent Veronique Greenwood to discuss what gives some birds their astonishing colors; how modern birds descended from dinosaurs; and the evolutionary importance of beauty and female choice.

Club-winged Manakin | Nick Athanas

How did you get into birds? 

I was an amorphously nerdy kid who did silly things like memorize food-eating records from the Guinness Book of World Records. Then in fourth grade I got a pair of glasses, and suddenly the world came into focus. Soon after, I saw the Peterson Field Guide to Birds in the Johnny Appleseed Bookstore in Manchester, Vt., and thought, “Wow, this is really cool.” My mom filed that away, and I got a bird guide for my birthday, and I just took off with birding. We lived in a very rural place, and there were woods and fields right outside my back door, and I became obsessed with birds. I knew a bunch of older garden club ladies who were into birds, and they had cars. So I did a lot of bird-watching with fantastic ladies who taught me plants, flowers, ferns — field biology — and I pined away for the future prospect of traveling and knowing more birds. 

A career in ornithology must have felt like a natural choice.

I had no idea what real ornithology was. Through high school, I thought I was destined to be a park ranger. It wasn’t till I was an undergrad at Harvard that I was exposed to the world of science, through a freshman seminar. One of my roommates freshman week said, “Hey, here’s a course for you: Biogeography of South American Birds.” I almost fell out of my chair. I was already obsessed with South America, the most diverse place on the planet for birds — and a real challenge for the subject of speciation.

What was so surprising about the large variety of avian species in South America?

You have a huge number of birds in lowland tropical rainforests, and no obvious geographic isolation barriers that would nudge lineages to evolve differently. If you have a mountain range in the way, it’s easy to understand how speciation took place. But if you have a continuous patch of forest, it’s a conundrum. 

So in South America, there is a real issue of how these many species evolved. And that was the subject of the seminar. It was given by Ray Paynter, who was a very minor figure in ornithology and, by many secondhand accounts, a really unpleasant guy. 

But he had one special thing that he loved, and that was the people who took his freshman seminar. He knew exactly what it was to be a young bird-obsessive, and he welcomed me completely — gave me keys to the joint, the Museum of Comparative Zoology, which I still have in my desk drawer. I’m sure they changed the locks many decades ago, but I still have my keys, damn it. 

That was a fantastic collection of birds — 300,000 or so specimens. I had turned 18 a week before, and I have been associated with a world-class collection of birds of the world continuously since then. I can’t function intellectually unless I have a couple hundred-thousand dead birds across the hall. That is my library.

The golden-winged manakin is one of about 50 manakin species, all endemic to South America. Manakins are notable for their elaborate courtship displays. | Nick Athanas (left); J. Dunning/Viro (right)

How did you picture your scientific career unfolding after taking Paynter’s class?

At that point, the science I had the most view of was ecology: what birds eat, where they migrate, how they feed their young. But in my sophomore year, I learned there was a debate raging about classification. 

I already knew the Linnaean classification of birds — the classical system of taxonomy that placed chickadees and titmice in one family in an order with thrushes, while ducks were in another family in a different order. The traditional view of most of the 20th century was that classification was a convenient filing system. 

But this new theory, called phylogenetic systematics, proposed that the classification of organisms should reflect their actual evolutionary history. This made this rather arcane art form into a new discovery-based science, the goal of which was to discover phylogeny, or what Darwin called the “tree of life,” in all its details. It got me excited about evolutionary biology because people were saying, “You can be part of this scientific revolution.” That was heady stuff.

After you graduated from Harvard, you went to Suriname for six months, and then elsewhere in South America to study the courtship display behaviors of manakins short, stubby South American birds. Watching the manakins, what stood out for you?

One of my favorite manakins is the golden-winged manakin, Masius chrysopterus. The male is velvety black, except his crown is yellow and red, and the inner webs of his wing and tail feathers are bright golden yellow. So when he flies, you see these flashes of bright yellow. In his courtship display, he flies through the forest and lands down on a mossy, fallen log, then rebounds, turns around in midair and lands with his bill down and his tail up. 

Often he’ll then fluff up his plumage like a little ball, cock his tail and bow from side to side, like a little windup toy. All of this is associated with a series of vocalizations — as he flies, he gives a single long “ceeeeeeeeee” note, and then as he jumps off a log, he goes, “ceee ceee aaak,” then ends with a sort of froggy “nerk” note. 

What did you learn from studying such elaborate displays of

different South American birds?

When I looked at the different species of manakins and the associated male behaviors, I saw a history of what females preferred in various lineages. It’s sort of an evolutionary version of Freud’s classic question, “What do women want?” In some bird species, like manakins, females do all the parental care, so they can mate with whichever males they prefer. 

In these species, what often evolves is a courtship display arena, or what ornithologists call a lek, where males aggregate to do their dances and females choose among the available males. Under these conditions, the males’ display behaviors, songs and plumages are important in female mate choice.

Sexual selection is about who gets the opportunity to reproduce. There are a lot of males that fail every breeding season, and whatever it is about them that females don’t prefer doesn’t get represented in the next population. As a result, those features that females use in order to choose their mates evolve very rapidly. 

If the females like long tails, tails are going to evolve to be longer. If the females like colorful plumage, the plumage is going to be more colorful. If they like this or that kind of movement, then that’s what is going to happen. 

As the male plumage and displays and songs diversify, the mating preferences of the females are also evolving and diversifying among species. Darwin described sexual selection by mate choice specifically: Each species evolves its own standard of beauty by which it chooses mates. 

What you are suggesting, then, is that birds’ sexual displays are not about solving an explicit environmental challenge to aid survival, like avoiding a predator or cracking open a seed. 

Right. The beak of the finch is marvelous in that it can crack open seeds. As the seed changed and evolved in size and hardness in the environment, the beak also has to evolve in order to face that challenge. But the sexual display of a manakin functions in the mind of female birds, not in the outside world. 

To understand how these aspects of biodiversity evolve, we must understand that the challenge is one of seducing a mind that has the capacity to evolve nearly infinite preferences. We see in sexually selected traits a much greater diversity than we see in those traits that are under strict natural selection. 

Throughout graduate school at the University of Michigan and into your first professor job at the University of Kansas, you were still spending a lot of time in the field. But then something happened that changed everything. 

It was in the ’90s, when I was in Kansas, that I started to lose my hearing. I had a sudden hearing loss in one ear, which was likely viral. And then in the opposite ear, I developed Meniere’s disease, which is a problem with controlling fluid inside the cochlea, progressively damaging the hair cells there. 

By the late ’90s, I was essentially ornithologically deaf. I can’t hear anything over 2,000 cycles per second. If you think of a piano, if you go about a third of the way, maybe halfway from middle C to the end, by about there, I start to lose it, and at the top of the piano, I can’t hear anything at all.

So you could no longer hear the birdcalls of the manakins and other avian species you’d been studying. Was that crucial to your work in the field?

It was essential. Often in the rainforests, or even in deciduous forests in the United States during migration, more than 50 percent of what you detect you’ll detect by song. I wore the grooves out of bird records in elementary school, and my brain grew up to learn birdsongs, with fine ability to differentiate and then remember variations in sound. That was always my edge in field ornithology — the capacity to hear and learn birdsongs, and then find the birds. 

I’ll tell you a story. I got interested in a bird from Madagascar called the velvet asity. I had a suspicion that it was a lekking bird, where males gather and perform mating dances, so in 1994 I went to Madagascar to look at it, and I confirmed that it was. Later I got a National Geographic grant to go do a more detailed study, and I brought over three people from the University of Kansas. 

I get on the trail with them, and I go to my old reliable: this one color-banded male that I’d studied four years before. There he was, in the exact same place in the trail as before. The three assistants have never seen a velvet asity before, and they’re all watching with binoculars. He kicks back his head and opens up his mouth — and I don’t hear anything. At that point, I realized: This is a song that I had described in ’94, and by ’98, I couldn’t hear it anymore. It hadn’t occurred to me that it was happening so fast.

So that made fieldwork difficult to do. Now I’m a tourist. I mean I still love bird-watching, but I had to find a new connection to my life’s work, intellectually.

One direction you took to fill that chasm was investigating coloration in birds. How did you become interested in that?

Back in 1992, when I had started losing my hearing, a friend lent me a jar full of newly collected velvet asities preserved in ethanol to use for some anatomical research. The velvet asity has this incredible fleshy fold of skin, or wattle, over its eye. The wattles of the birds in the jar were this deep royal blue, with opalescent highlights. And yet the label said that the wattles were fluorescent green.

I snipped off a piece of wattle and sent it to a microscopist, and we discovered a mechanism for the production of color that had never been observed before. Most organisms’ colors are produced by pigments that absorb certain wavelengths of light, but not others, to create a color. Other times, colors are made by nanostructures that scatter light, a phenomenon called structural color. 

I knew that’s what was going on in the wattle, but what we discovered was that the structures creating the velvet asities’ green wattle were made of collagen, a protein that we hadn’t seen used in this way before. The collagen fibers were straight and parallel, like uncooked spaghetti in a box, arranged in a perfect hexagonal array. The distance between the fibers affects how light waves interfere with each other to cancel out some wavelengths of light and not others, thus affecting what colors you perceive. 

In the velvet asity, the reason why the wattle was blue by the time it got to me was that it had been treated with formalin and ethanol, and it had dehydrated so that the tissue had shrunk in size. The spaghetti strands were closer than before, changing the color from green to blue.

And this phenomenon played out in other birds as well?

We started looking at the skins of closely related birds, and we had another surprise: Yes, they had structural colors made by collagen fibers, too, but the collagen fibers there were not arranged in a perfect crystalline order. We called them “quasi-ordered” and discovered that they also produced color by interference. 

But they had this other interesting optical property, which is that they’re not iridescent; they don’t change color with angle of observation, like the colors in a peacock or hummingbird do. Normally, iridescence — that quality of changeable color that you see in an oil slick, or a peacock’s feathers — is the clue that interference is at work. But here, it’s different. 

Once we discovered that, we started looking more broadly at structurally colored feathers that were not iridescent. Many of them had this similar property. Before that, nobody had really created intellectual tools for understanding how less ordered materials could produce these structural colors. 

The reason is that people were interested in order, because it’s mathematically simple, and it made the problems easy to solve. But if you look at nature, new questions will arise that won’t have been obvious if you’re just following the intellectual path of some field as it develops.

Your next major project was also about feathers not their coloration, but their evolution. How did you get interested in that?

The idea grew out of a lecture in my ornithology class I was teaching at Kansas, on how feathers grow. A day or two after that, I was doing a lecture on how feathers evolve. I was up at the board, jamming, when I realized that if you actually look at how a feather grows, the main 20th-century, enduring-for-80-years hypothesis about how feathers evolved couldn’t be true.

What was the contradiction?

For most of the past century, people hypothesized that feathers had evolved from elongated scales, like shingles on a house that got longer and longer until they hung off the body and provided aerodynamic function, catching air and enabling gliding and ultimately flying. But saying that feathers evolved for flight is like saying that fingers evolved to play the piano. 

And what we know now about how feathers develop refutes it. A feather begins, in a chick, as a tube of epidermis that has grown out of the skin, sort of like a tubular pasta being extruded by a pasta machine. Then the tube opens up, and the outer surface of the tube becomes the top of the feather, and the inner surface of the tube becomes the underside of the feather. 

So the two sides of a feather are not the same as the two sides of a scale. Like they say in the old Bert and I records, “You can’t get there from here.” Evolution cannot go through a series of elongated scales and ever end up with something that looks like a feather. 

What were the implications for avian evolution?

That early feathers would have looked like tubes. Slightly later, feathers would have looked like fuzzy down … and so on through the steps of feather development until you get a full planar feather. The important implication of this theory is that feathers did not initially evolve for flight because you can’t fly with down.

As it happened, in 1998  not long after you had started to formulate your theory of feather evolution  Chinese paleontologists discovered dinosaurs covered in fuzz, and there was quite a debate about what this stuff was. How did you get involved in that issue?

A lot of people were resistant to the hypothesis that dino fuzz could be feathers because these things don’t look like elongated scales. With several colleagues at the Chinese Academy of Sciences’ Institute of Vertebrate Paleontology and Paleoanthropology, we were able to establish that certain key raptor dinosaurs were fully plumaged, with feathers that were entirely modern in structure. 

That was a huge discovery, which we published in 2001 in Nature. Along with other research, this absolutely established that feathers evolved in dinosaurs prior to the origin of flight and prior to the origin of birds.

Why did dinosaurs evolve feathers, if not for flight?

They may have just looked really cool. I think that it’s quite likely that the appearance of feathers played a major role in their evolutionary origin and their diversification — that sexual selection, mate choice and other kinds of social communication were critical. 

There’s a great punch line here. For over a century, we knew exactly why feathers had evolved: Feathers had evolved for flight. But all during that time, we learned absolutely nothing about how feathers actually evolved. My research has approached it from a different direction. As a result of not asking what feathers were good for, we actually made tremendous progress in understanding how they evolved.

After Darwin proposed natural selection, he had a problem: There were all these things that were obviously not helpful to an individual’s survival, like elk antlers and the peacock’s tail. They were clearly a pain, or attractive to predators. He proposed that these things evolved because they provide differential success not in survival, but in the animal’s opportunity to mate and reproduce. 

He also proposed that different species evolved distinct standards of beauty, and that those are what led to the evolution of secondary sexual traits in diversity within organisms. Overwhelmingly, he used aesthetic language to describe what he meant — he described males as charming the females. He described females as having a taste for the beautiful. Charm, beauty — these are words that don’t usually appear in science.

To the modern ear, those terms do seem like dated, pseudoscientific Victorianisms. Today the consensus seems to be that if you want to talk about aesthetics, you shouldn’t be a scientist.

Right, and I think that’s a terrible mistake. What Darwin was really saying is that female sexual autonomy is an evolutionary force of nature, and one of the consequences of sexual autonomy through mate choice is beauty. He also was very explicit that sexual selection was distinct from natural selection. 

Very early on, his model got criticized and ultimately was ignored. The study of sexual selection was revived starting around 1975, but it’s been laundered of any aesthetic content. What most biologists studying sexual selection today believe is that the peacock’s tail, say, is preferred because it encodes information about quality that the female needs to know. 

That’s very distinct from Darwin’s hypothesis, which was that it evolves because it is beautiful to that particular female. And Darwin was explicit in proposing that the traits of the male and the preferences of the female coevolve with one another; that they mutually change with one another over time.

Are you saying that there’s no utility to these traits beyond their beauty  that they play no role in the animal’s survival?

I think there is a huge amount of support for the notion that most of the ornament in these secondary sexual traits is actually just arbitrarily beautiful. The way in which arbitrary sexual selection has been eliminated or rejected by the field is explicitly anti-Darwinian. I’m working on the idea that we need to revive Darwin’s explicitly aesthetic view of sexual selection.

These concepts, which explain how speciation could take place without physical barriers in the outside world, make you a maverick in the field.

A few years back I was describing my ideas to a well-informed behavioral ecologist in this field, and when he got my core idea, he said, “But that’s nihilism.” I realized, “Wow, this idea is incredibly threatening to many people’s core rationale for why they study evolutionary biology.” A huge number of those in the field think the mission is establishing the importance and breadth of natural selection in nature — not describing the processes that make nature the way it is.


Web Extra: Richard Prum describes how he and his team discern color from feathers' fossil remains in this video.

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