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The Evolution of Beauty

How Darwin's Forgotten Theory of Mate Choice Shapes the Animal World and Us

by Richard O. Prum

Hardcover, 428 pages, Random House Inc, List Price: $30 |

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Title
The Evolution of Beauty
Subtitle
How Darwin's Forgotten Theory of Mate Choice Shapes the Animal World and Us
Author
Richard O. Prum

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Book Summary

A major reevaluation of how evolutionary forces work examines how mating preferences, what Darwin termed, "the taste for the beautiful," have driven adaptive evolution and created an extraordinary range of aesthetic and elaborate ornament in the animal world.

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Excerpt: The Evolution Of Beauty

CHAPTER 3
Manakin Dances

How, and why, has beauty changed within and among bird species over the course of millions of years? What determines what any given species finds beautiful? What, in short, is the evolutionary history of avian beauty?

These questions might seem impossible to answer, but we actually have many of the scientific tools we need to address them productively. One of the challenges to understanding the evolution of beauty is the complexity of animal displays and mating preferences. Fortunately, we do not need to invent a trendy new brand of “systems science” in order to investigate these complex aesthetic repertoires, because the science of natural history—the observation and description of the lives of organisms in their natural environments—provides us with exactly the tools we need. Natural history was a critical component of Darwin’s scientific method and remains a bedrock foundation of much of evolutionary biology today. 

Once we have gathered information about individual species, we need other scientific methods to compare and analyze them and to uncover their complicated, often hierarchical evolutionary histories. The scientific discipline that enables us to do that is called phylogenetics. Phylogeny is the history of evolutionary relationships among organisms—what Darwin called the “great Tree of Life.”

Darwin proposed that discovery of the Tree of Life should become a major branch of evolutionary biology. Unfortunately, research interest in phylogeny was largely abandoned by evolutionary biology during most of the twentieth century. However, powerful new methods for reconstructing and analyzing phylogenies have been developed in recent decades, which has led to a revival of interest. So, now that the two critical intellectual tools necessary to study the evolution of beauty—natural history and phylogenetics—are available, there has never been a better time to be asking questions about how beauty, and the taste for it, evolve. 

Doing so will help us to understand the process of evolutionary radiation—diversification among species—in a new way. In evolutionary biology, adaptive radiation is the process by which a single common ancestor evolves through natural selection into a diversity of species that have a great variety of ecologies or anatomical structures. The amazing diversity of Darwin’s Finches (Geospizinae) on the Galápagos Islands is a canonical example of adaptive radiation. In this chapter, however, we will investigate another group of birds—the neotropical manakins—in order to understand a different kind of evolutionary process: aesthetic radiation. Aesthetic radiation is the process of diversification and elaboration from a single common ancestor through some mechanism of aesthetic selection—especially mate choice. Aesthetic radiation does not preclude the occurrence of adaptive mate choice, but also includes arbitrary mate choice for sexual beauty alone, with all of its often dramatic coevolutionary consequences. 

The science of beauty requires that we get out of the laboratory and the museum and into the field. Fortunately, my bird-watching youth was great basic training for doing natural history research on birds in the field. I discovered the second critical element of this branch of beauty studies—phylogenetics—as an undergraduate at Harvard University. My immersion in formal ornithological studies began in the fall of 1979 with a freshman seminar, the Biogeography of South American Birds taught by Dr. Raymond A. Paynter Jr., the curator of birds at the Museum of Comparative Zoology (MCZ). Dr. Paynter introduced me to the intellectual magic of natural history museums. Up on the fifth floor of the huge and ancient brick building that housed the Bird Department was a series of rooms where hundreds of thousands of scientific bird specimens were curated. During my undergraduate years, the MCZ was my intellectual home. I hung out a lot in the bird collections doing bibliographic work and curatorial tasks for Paynter and generally smelling like mothballs.

Dr. Paynter himself was far too intellectually conservative and cautious to be interested in the revolutionary new field of phylogenetics. But I soon discovered that the latest concepts and methods in this field were being hotly debated downstairs in the Romer Library in the weekly meetings of the Biogeography and Systematics Discussion Group. In retrospect, this time at Harvard was a golden era for phylogenetics. From the meetings of this “revolutionary cell” in the Romer Library, multiple graduate students went out into the world and made fundamental contributions to the field, helping to bring phylogeny back into the mainstream of evolutionary biology.

My own work was profoundly shaped by those weekly discussions in the early 1980s. I became fascinated by phylogenetic methods and eager to reconstruct avian family trees. For my senior honors project, I worked on the phylogeny and biogeography of toucans and barbets. Working at a desk I made for myself on a big table beneath the towering skeleton of an extinct moa in room 507 of the bird collection, I was excited to make observations of toucan plumage and skeletal characters and to construct my first phylogenies. I am happy to say that I have been continuously associated with world-class scientific collections of birds ever since. Only, I don’t smell like mothballs anymore.

As graduation approached, I was casting about for what to do next, searching for a research program that would combine my bird-watching skills and passion with my new obsession with avian phylogeny. Before going on to graduate school, I was desperate to get to South America and to see more of the birds I had met in the drawers at the MCZ. (There were very few tropical bird field guides in those days, so browsing through a museum collection was actually the best way to learn about the birds before actually seeing them in real life.) Intrigued by the Harvard graduate student Jonathan Coddington’s research using the phylogeny of spiders to test hypotheses about the evolution of orb-web-weaving behavior, I wanted to make a similar use of phylogeny to study the evolution of bird behavior.

At about that time, I met Kurt Fristrup, a Harvard graduate student, who had worked on the behavior of the flamboyantly orange Guianan Cock-of-the-Rock (Rupicola rupicola, Cotingidae) (color plate 5), one of the planet’s most amazing birds. Kurt suggested, “Why don’t you go to Suriname to map manakin leks?” In retrospect, this was one of the most consequential pieces of professional advice I ever received.

On a thin branch twenty-five feet high in the sun-dappled understory of a tropical rain forest in Suriname perches a tiny glossy black bird with a brilliantly golden yellow head, bright white eyes, and ruby-red thighs—a male Golden-headed Manakin (Ceratopipra erythrocephala)(color plate 6). He weighs about a third of an ounce (ten grams), or a bit less than two U.S. quarters. He has a short neck and short tail, giving him a compact body, but he has a nervous energy that belies his almost dumpy appearance. He sings a high, soft, descending whistled puuu and peers intently around, hyperaware of his surroundings. In moments, a second male whistles back from his perch in an adjacent tree, and then a third nearby. The male answers immediately. His social environment is obviously the focus of his keen attention. In all, there are five males clustered together in the forest. They are obscured from one another by foliage, but they are all within earshot of each other.

In response to the neighboring calls, the first male draws himself up into a statuesque upright posture with his light-colored bill pointing upward. After singing an energetic, syncopated, and raspy puu-prrrrr-pt! call, he suddenly flies from his perch to another branch twenty-five yards away. After a few seconds, he flies rapidly back to his main perch singing an accelerating crescendo of seven or more kew calls in flight. His flight path traces a subtle S-curve trajectory, first down below the level of the perch and then up above it. He lands on the perch from above while uttering a sharp buzzy szzzkkkt! Immediately upon landing, the male lowers his head, holds his body horizontal to the branch, and raises his rear up with his legs extended, revealing bright red thighs against his black belly, like a provocatively colored pair of breeches. He then slides backward along the perch in the tiny rapid steps of an elegant “moonwalk,” as if on roller skates. In the middle of the moonwalk, he flicks his rounded black wings open vertically above his back for a moment. After sliding backward for twelve inches along the branch, the male suddenly lowers and fans his tail, flicks his wings vertically again, and resumes his normal posture.

Moments later, the second male Golden-headed Manakin flies in and perches on another branch about five yards away. The first male immediately flies to join him, and they sit quietly side by side—but facing away from each other—in the dramatic upright posture. Intense, competitive, but mutually tolerant, the two males are deeply engaged with each other.

This scene is just a few moments in the bizarre social world of a Golden-headed Manakin lek. A lek is an aggregation of male display territories. Lekking males defend territories, but these territories lack any resources that females might need for reproduction other than sperm: no significant food, nest sites, nest materials, or other material assistance to the female. Golden-headed Manakins defend individual territories between five and ten yards wide, with two to five such territories grouped together. Leks are essentially sites where males put themselves on display in order to lure females to mate with them. Over the breeding season, individual females visit one or more leks, observe male displays, evaluate these displays, and then choose one of those males as their mate.

 Lek breeding is a form of polygyny (one male with many potential mates) that results from female mate choice. In a lek-breeding system, females can select any mate they want, and they are often nearly unanimous in preferring a small fraction of the available males. So a relatively few males get to mate with a relatively large number of females. The skew in mating success is rather like the contemporary skew in income distribution. The most sexually successful males are very successful and account for half or more of all the matings, while other males will never have any opportunity to mate in a given year. Some males go their whole lives without mating.

After mating, female manakins build nests, lay clutches of two eggs, incubate them, and care for the developing young entirely on their own without any help from the males, whose contributions to reproduction end with their sperm donations. Because females do all the work, they don’t depend on the males for anything, and their independence allows them almost total sexual autonomy. This freedom of mate choice has allowed extreme preferences to evolve; females only choose the few males whose behavioral and morphological features meet their very high standards. The rest will be losers in the mating game. Thus the aesthetic extremity of male manakins is an evolutionary consequence of extreme aesthetic failure, which results from strong sexual selection by mate choice.

Female manakins have been choosing their mates in leks for about fifteen million years. Over the course of time, the features they have preferred have evolved into an extraordinary diversity of traits and behaviors among the approximately fifty-four species of manakins distributed from southern Mexico to northern Argentina. Manakin leks are among nature’s most creative and extreme laboratories of aesthetic evolution. For me, they proved the perfect place to study Beauty Happening.