"In this engaging book, Michael Ryan explores why all animals look for beauty in the opposite sex. Using his studies of Central American frogs as a jumping-off point, he expertly guides us through new discoveries and ideas about how brains have evolved to yearn for the beautiful. Surprisingly, what female frogs admire in their male suitors illuminates our own desires and attractions."--Virginia Morell, author of the New York Times bestseller Animal Wise: How We Know Animals Think and Feel

"We say ‘beauty is in the eye of the beholder.' Turns out, beauty is in the brain. The brain decides what strikes us as beautiful. This book raises and answers an astonishing set of questions: What is the perception called beauty? How did our brains acquire it? On what basis do our brains inform us about what is beautiful? And why does a peacock's tail seem beautiful to both a peahen and a person? This is a profound, often amazing, book. It's, well, beautiful."--Carl Safina, author of Beyond Words: What Animals Think and Feel

"Written by a distinguished scientist and filled with fascinating stories, this book presents the revelation that, for very good evolutionary reasons, beauty is in the mind, as well as the eye, of the beholder."--Peter R. Grant, coauthor of 40 Years of Evolution: Darwin's Finches on Daphne Major Island

"This lovely book delves into the origins and perception of beauty--sensations that generate specific reward responses in the brain. Ranging from neurobiology to behavior and psychology, Mike Ryan seamlessly integrates animal and human data. He also describes how science works, which is more important now than ever."--John Endler, Deakin University, Australia

"This is a superb book on one of the most powerful selective forces in nature--the taste for beauty, especially the female preference for male beauty. Want to learn about smell and sex, the deeper meaning of bodily symmetry, or color vision as a route to emotionally understanding others? You have come to the right place. Michael Ryan weaves together all of this and much more to produce a beautiful tapestry on the meaning of beauty in nature."--Robert Trivers, author of Deceit and Self-Deception: Fooling Yourself the Better to Fool Others

"I loved this book! In this authoritative, informative, and entertaining popular science account of the biological basis of sexual beauty, Michael Ryan, a master of the subject, draws on his own pioneering work and seamlessly integrates it with other studies. The book shows how a deep understanding of the mechanisms of mate choice in nature help us to better understand ourselves."--Daniel T. Blumstein, University of California, Los Angeles

"This is a book for anyone who wants to know more about the mysteries of sexual selection. Michael Ryan guides readers through the complex and fascinating path of the evolution of beauty with the authority of somebody who is responsible for some of the subject's most important milestones."--Leonida Fusani, University of Vienna and University of Veterinary Medicine, Vienna, Austria

A Taste for the Beautiful

The Evolution of Attraction

PRINCETON UNIVERSITY PRESS

Contents

Why All the Fuss about Sex?

The sight of a feather in a peacock's tail, whenever I gaze at it, makes me sick!

— Charles Darwin

NATURE USUALLY GETS DOWN TO BUSINESS. Let's think about sleep. When I go to bed, I pull back the sheets, put my head on the pillow, and I'm in dreamland. I do not have a sleeping ritual, I don't dance, sing, chant, or perfume myself. I just go to sleep. So do most animals. Eating is the same way. When a howler monkey finds an edible leaf, she plucks it and eats it; a heron just throws back his head and swallows the fish he speared out of the water; and a cheetah doesn't do a celebratory dance before she starts to devour the gazelle she just brought down, even though she sprinted at her personal best of 75 mph to do so. Granted, in our own species we can sometimes make a bigger deal out of eating, especially when a meal coincides with a special event. But for the most part, we are little different from the howler, the heron, and the cheetah. Take a bite, give it a good chew, and gulp it down. Much of life for most animals is like that — the job is to just get it done.

Sex is different: a just-get-it-done policy won't get it done. In humans and most other animals, extensive courtship rituals precede the sex act. Most of our sexual rituals are laden with accessories, including candles and music, poems and flowers, and even special wardrobes. The list goes on, but it is no less diverse for animals. Animals sing and dance, they perfume themselves, they show off their colors and even light themselves up, all in the hope of attracting a mate. Although we distinguish ourselves in the language and technology we deploy in courtship, all animals have evolved spectacular, even obscene, morphologies and behaviors as both sexual lures and strategies for consummation. The colors of butterflies and fishes, the songs of insects and birds, the sexual odors of moths and mammals all evolved in the service of sex. The same is true for many of the traits in our own species that make women sigh and men gasp when someone of striking beauty crosses their paths. These aspects of sexual beauty evolved not because they make their bearers live longer but because they enable them to mate more and thus pass on more offspring and genes to the next generation.

Sexual beauty is everywhere, woven through the fabric of all sexually reproducing animals. We humans strive for beauty; we pay for it; we judge whether others have it; and if they do, we treat them better. Animals and humans both go to extreme lengths to appear beautiful to those who judge them. Peacocks evolve magnificent tails that cause peahens to sway, fishes sport bright colors that catch the eye of the other sex, crickets chirp endearingly to their mates, and spiders dance and vibrate their webs to show off. We humans take a more active role in engineering our beauty than do most other animals. Perfumes, fashion, cars, and music have all been employed in the service of sexual beauty, as have the surgeon's knife and a pharmacopeia of drugs. But to enhance one's beauty, either through the painstakingly slow process of evolution or the more immediate gratification of beauty-engineering, one must have some notion of what is beautiful.

This book is about sexual beauty, where it comes from and what it is for. Of course, many have been inspired to write in appreciation of natural beauty and the enchanting mating behaviors that occur in wild animals. Their emphasis is usually on the details of beautiful male traits: How does having such a long tail benefit the peacock? How many carotenoids does the male guppy need to eat to be so brilliantly orange? How many syllables can a songbird pack into his complex vocal repertoire to make him even more sexy to females? These are interesting questions, but they represent only one-half of the equation of sexual beauty, because they ignore what is going on inside the head of those who actually judge beauty. Such studies often assume that the female brain must evolve tools to figure out what is beautiful. But instead, the converse is often true. The brain has a long evolutionary history that biases how it assesses the entire world around it, not just the world of sex; and it functions within the framework of numerous neurobiological and computational constraints. I argue that instead of the brain having to evolve to detect beauty, the brain determines what is beautiful, and all of its constraints and contingencies give rise to a breathtaking diversity of sexual aesthetics throughout the animal kingdom. In this book, I will show that to understand what beauty is, we need to understand the brain that perceives it.

I will expand our understanding of sexual beauty by asking how the details of an animal's brain give rise to its sexual aesthetics, which, in turn, drive the evolution of beauty in that species. Specifically, I argue that beauty only exists because it pleases the eyes, ears, or noses of the beholder; more generally, that beauty is in the brain of the beholder. Some of the brain's neural circuitry has evolved to sense and respond to sexual beauty so that animals can find a good mate. But the brain also has other things on its mind besides sex. Other adaptations of the brain, such as those that help an animal find food, avoid becoming food, or recognize the difference between its mother and its father, can have unintended but important consequences on how that brain defines beauty. Only when we understand the biological basis of sexual aesthetics can we understand how sexual aesthetics drive the evolution of sexual beauty.

I have a unique perspective to offer on these issues as I have spent the past forty years studying the sexual behavior of a tiny, bumpy frog in Central America. This work has opened my eyes and mind to both the diversity of sexual behavior in the animal kingdom and a core unifying theory that I have developed called sensory exploitation. The key idea is simple: features of the female's brain that find certain notes of the males' mating call attractive existed long before those attractive notes evolved. Thus, females are the biological puppeteers, making the males sing exactly what their brains desire. Beauty is indeed in the brain of the beholder, and in most cases, that means the female's brain, although I will review numerous cases where males judge female beauty and where there is mutual display and assessment of beauty by both sexes. This simple idea contributed to a paradigm shift in the study of sexual selection, one in which the importance of the sexual brain as a driver of evolution finally was acknowledged.

In this chapter, I will give some background on how scientists have come to understand the evolution of beauty and also explain which sex usually evolves this beauty and why. In the next one, I'll focus on the bumpy frog that has been the focus of much of my scientific brain power, to show how scientists actually go about learning how the brain relates to mating behavior. Chapter 3 delves into how the brain defines beauty by discussing the evolution of sensory systems and the cognitive processing of sensory information. Chapters 4 through 6 describe what is known about visual, acoustic, and olfactory beauty throughout the animal kingdom. Chapter 7 describes some biological underpinnings to the claim that percepts of beauty are sometimes fickle. And in chapter 8, I describe how some percepts of beauty lie masked and unknown until just the right individual appears to elicit attraction. This logic is extended to provide an evolutionary understanding of how various human enterprises, from the fashion industry to pornography, have been able to exploit these hidden preferences. In the epilogue, I close the book with some comments about the biological basis of beauty.

In our search for answers about beauty, we will explore nature and journey to where scientists have studied some of the world's most stunningly beautiful animals. We will probe the basic premises of why sexual beauty had to evolve and delve into new findings from neuroscience that provide insights into how the brain perceives beauty. The analogies between animals and humans might cause us to rethink our own sexual aesthetics. As with much of biology, the best place to start thinking about sexual beauty is with Charles Darwin. Where I will depart from Darwin is within an arena that he knew little about: the brain.

* * *

It is hard to overestimate the impact of Charles Darwin's theory of evolution by natural selection on our view of humanity's place in the universe. It is one of the crowning intellectual achievements of humankind, ranking right up there with Copernicus's theory of celestial motion, Newton's laws of physics, and Einstein's theory of relativity. His book, On the Origin of Species, sold out in a few days; subsequent editions continued to sell out for decades; and it is still one of the most widely cited books in the world.

The most amazing thing about natural selection is its brilliant simplicity, which can be unpacked into three ideas or principles. The first, which comes from Thomas Malthus's Essay on the Principle of Population, is that the rate of reproduction outstrips the available resources to support it — not all offspring survive to reproduce. Consider a pair of house flies that sneak into your dwelling through a small tear in the window screen. This couple is capable of producing five hundred offspring during their short lifetime of one month. If all of their offspring and their future progeny survived to reproduce, six months later you would be inundated by about two trillion flies with a combined weight of more than 2,500 tons, whose body mass would cover more than one thousand square miles, an area close to the size of Luxembourg. Luckily, this doesn't happen, as most of these flies die, and only a handful survive.

The second principle is that differential survival is not always random. Some survivors are just lucky — for example, those who happen not to be around as your fly swatter comes bearing down. But others survive because they are "better"; they have adaptations that allow them to avoid your swat and live to reproduce. Perhaps they are more sensitive to the wind displacements caused by the fly swatter, or they have faster flight muscles that allow escape before they get splat. But they are survivors, and they get to stay on the island, or at least in your house.

The third principle is that if variation in survival traits has a genetic component, these traits will be differentially passed down to the next generation. If the surviving flies have genes for faster flight muscles, for example, so will their offspring. These offspring will constitute a new generation of flies that fly faster, live longer, and reproduce more. This is how natural selection causes the evolution of survival traits. Time to fix that tear in your window screen.

When Darwin, along with Alfred Wallace, formulated the theory of natural selection, he never suggested it explained everything — he never thought that every aspect of every individual was an adaptation for survival. He was aware of the power of culture, in animals as well as humans. Darwin also understood random variation, which occurs when alternative forms of the same trait can become fixed in small populations. But one thing he did not understand, at least not immediately, was the peacock's tail. It caused him such consternation, he wrote to the botanist Asa Gray, that it made him sick. We know that Darwin was often sick, and a hypochondriac to boot, but such malaise in response to something so magnificent seems a bit extreme. The peacock's tail is the mascot for scientific studies of animal beauty, but for Darwin it was a stark reminder of what his theory did not explain, and it motivated him to find a new theory to complement that of natural selection. He called it sexual selection.

* * *

The peacock is a majestic and beautiful beast. He initiates courtship with a female by erecting his feathers to form a fan that spreads out more than 180 degrees. He has two hundred feathers up to four feet long that are adorned with eyelike spots and have an iridescent sheen that causes them to sparkle brilliantly in the sunlight. Once they are erect, he shakes, rattles, and rolls his feathers, causing them to hum like an engine and the eyespots to vibrate hypnotically. All of this beauty evolved in the service of sex. Peahens get to choose their mates, and peacocks evolved their beauty to better compete in the sexual marketplace, where only the beautiful get chosen to pass their genes forward.

A peacock displaying in all his splendor is a majestic sight to us and to peahens alike. But have you ever seen a peacock run or fly? It's pathetic! Dragging his tail behind him, he can't outrun a child let alone a fox, and he can barely fly. If Darwin was correct that natural selection causes adaptations for survival by weeding out the weak, where did this monstrosity come from, and why wasn't it culled out long ago? This is why a mere feather was so distressing to one of science's greatest minds. But it was mental, not physical, duress that caused this particular malady. The peacock's tail offered a major challenge to Darwin's theory of natural selection, so he went to work on another theory to explain how it could evolve.

The peacock's tail was not the only challenge to Darwin's calculus of survival evolution; it was just the tip of the iceberg. In his secondmost famous book, The Descent of Man and Selection in Relation to Sex, published twelve years after On the Origin of Species, Darwin noted that many animals, not just peacocks, harbored traits that seemed at odds with the process of natural selection. Many of these traits also appear beautiful to us and seem superfluous to the animal's survival. Fireflies light up when they glide across a nocturnal meadow; crickets spend hours chirping during the summer nights; coral reef fishes sport colors that focus our gaze; frog choruses announce the coming of spring; canaries sing arias that have charmed their mates for millennia and humans for centuries; bowerbirds decorate and paint their bowers with such creativity that one researcher invoked a comparison to Matisse; and Irish elk carried around eighty-eight-pound antlers with such high calcium demands that this might have eventually led to their extinction. We are no more restrained with our sexual beauty, as we invest billions of dollars each year to paint, perfume, and trim parts of our bodies that make us more sexually attractive. None of this has anything to do with improved survival.

These nonsurvival traits share other commonalities. Most of them are more developed in males than females; they are usually employed in courtship or in battle for mates; and, as first haunted Darwin, many of these traits are detrimental to survival. Darwin called these secondary sexual characters because they differed between the sexes and were associated with reproduction, although not crucial for it. How they evolved required some additional theorizing.

Artificial selection provides some instructive examples of how these showy sexual characters might evolve. It might be one of the most important human inventions since the control of fire, and Darwin used artificial selection as an analogy to natural selection. In artificial selection, humans are the agents of selection. We decide which traits, as the targets of selection, will evolve to meet our predetermined goals. We often selectively breed organisms for utilitarian purposes, such as disease resistance in crops and greater meat yield in cattle. But we also breed animals to please our aesthetic senses. Fish hobbyists breed aquarium fishes with spectacular colors and even implant foreign genes to make some fish glow in the dark, and we are all familiar with breeds of domestic dogs that humans have engineered because they are cute rather than functional.

Based on his intuitions derived from artificial selection, Darwin reasoned that if female animals also had their own aesthetics, their own standards of beauty, they too could exert selection to enhance their species' beauty. If female canaries were attracted to more variable male song, males with more variable song would produce more offspring, and canary song would evolve to be highly variable over time. If female peacocks found longer feathers to be sexually beautiful, they would choose to mate with males that have longer feathers, and consequently those males would have more offspring. Longer tails would come to flourish in future generations, even if these tails increased the male's predation risk. A short-feathered peacock that cannot convince females to mate will not pass his genes along to any offspring, even if he is fast enough to outrun any fox and lives to a ripe old age. Darwin's realizations about these issues allowed him to develop the theory of sexual selection using the same logic he employed for natural selection.