Duck Sex, Aesthetic Evolution, and the Origin of Beauty

Duck Sex, Aesthetic Evolution, and the Origin of Beauty

Richard Prum [9.3.14]

The way nature is—the nature of flowers, the nature of birdsong and bird plumages—implies that subjective experiences are fundamentally important in biology. That the world looks the way it does and is the way it is because of their vital importance as sources of selection in organic diversity, and as a result we need to structure evolutionary biology to recognize the aesthetic, recognize the subjective experience. 


...ducks are one of the few birds that still have a penis. It's a very weird structure. It has an explosive erection, its erection mechanisms are lymphatic instead of vascular, it's stored outside-in inside the cloaca and comes flying out, and they can get very lengthy—up to 40 centimeters, which is over a foot long on a duck that is itself not even a foot long. It's an extraordinary piece of biology. What's going on in these ducks?

In lots of ducks there's forced copulation. It's the equivalent of rape in ducks. In species where there is a lot of forced copulation, females have evolved or co-evolved complex vaginal morphologies that frustrate the intromission or frustrate entry of the penis during forced copulation. For example, the penis of ducks is counter-clockwise coiled and often has ridges or even teeth-like structures on the outside. In this case, in these species, the female has evolved a vagina that has dead end cul-de-sacs, so that if the penis goes down the wrong direction it’ll get bottled up and doesn’t perceive to be closer to the oviduct, or further up the oviduct and closer to ova. And then above the cul-de-sacs, the duck vagina has clockwise coils, so there's literally anti-screw devices that prevent intromission during forced copulation.

(1 hour)

RICHARD PRUM is an evolutionary ornithologist at Yale University, where he is the Curator of Ornithology and Head Curator of Vertebrate Zoology in the Yale Peabody Museum of Natural History. Richard Prum's Edge Bio Page


Over the last few years I've realized that a large portion of the work that I've been doing on bird color, on birdsong, on the evolution of display behavior, is really about one fundamental and important topic, and that's beauty—the role of beauty in nature and how it evolves. The question I'm asking myself a lot now is: what is beauty and how does it evolve? What are the consequences of beauty and its existence in nature?

There's a long history of people thinking about ornament in nature—those aspects of the body or the behavior of organisms that are attractive, which function in perception of other organisms. Usually we think about this in terms of sexual selection or mate choice, but there's a bunch of other contexts in which it can occur, like flowers attracting pollinators and fruits attracting frugivores, or even the opposite—a rattlesnake or a poisonous butterfly scaring away predators. These are all aspects of the body that function not in the regular way but in perception. 

For example, if we think about a plant and the parts of the plant, trying to explain why they are the way they are, if we examine the roots we could come up with a complete description of the roots and their function and their form in terms of their physical function in the soil. They're grabbing into the substrate, they're absorbing water and minerals, they're helping the plant anchor itself. They might even be interacting with fungus and bacteria in the soil. We come up with a complete description of the plants and we have a theory for this, and that theory is natural selection. However, if we think about the flower, many parts of the flower, including its color, the shape of its petals, its fragrance, function through the perceptions of other animals. That is, the bee or the hummingbird comes along and regards the flower, asks itself, "Do I want to forage at that flower now or today?" and then either decides to do so or not. As a result of that, we have a different functional substrate functioning in the brain, functioning in the perception of that other organism.

To come up with a complete description of the function of a flower, we need a whole new kind of data. Not just a description of the physical world, but something else inside, if you will, the mind of this other organism, this cognition. What I'm coming to conclude is that this is a big watershed in evolutionary biology, and that there's a distinct process that occurs when we have evolution occurring through a cognitive or mental substrate. That is, when it's about attracting another individual.

I would refer to this area as aesthetic evolution, and the main topic in aesthetic evolution is the origin of beauty. Of course these are two words that are not often involved in the sciences. In fact, science is a bit afraid of beauty, afraid of the aesthetic. This has to do with the fact that these terms refer to subjective experiences. They refer to something that's sort of unknowable or immeasurable going on inside the cognitive capacities of other organisms. Of course we have difficulty understanding what's going on in somebody else’s mind when they eat rhubarb pie, or smell a flower, or like or don’t like a certain kind of music. Scientists are justifiably afraid of talking about subjective experience, and for the most part we've ceded this entire area to other fields like the humanities. The way nature is—the nature of flowers, the nature of birdsong and bird plumages—implies that subjective experiences are fundamentally important in biology. The world looks the way it does and is the way it is because of their vital importance as sources of selection in organic diversity, and as a result we need to structure evolutionary biology to recognize the aesthetic, recognize the subjective experience.

We will never be able to nail it down exactly as we do many scientific questions. We don’t know what's going on in my brain or your brain with the experience of red, or what it's like to listen to a Mozart symphony and why some people might like certain things and others not, but in biology we have a real interesting opportunity. For example, there are 10,000 or so species of birds in the world, and every single species of bird has a slightly different song and a different courtship display and a different way of attracting a mate and communicating socially. Those have all evolved as a result of subjective experiences: "Do I like this mate or not?" Making a sensory perception, a cognitive evaluation and then a choice. These elements: sensory perception, evaluation and choice, give rise to this aesthetic evolutionary phenomenon.

Quantifying or describing the mental state of an individual, whether it's an individual bird listening to a birdsong or me, is very, very challenging. One of the things that we can do in biology is to study the way in which subjective experiences evolve. We may not know what's happening in the brain of a particular bird species, but by studying the fact that it has diverged in its preferences from other warblers or other gulls or other woodpeckers indicates that we can study the evolution of subjective experience within comparative biology.

It's a little bit like the history of physics when they had a hard problem. You couldn't actually identify the velocity of the electron and its position and its direction and motion all at the same time. What did they do? They had a hard problem, but they didn’t say, Okay, we're going to shelve that problem for some other discipline to deal with. They created new tools—quantum mechanical mechanisms and quantum mechanical concepts—that would allow them to study the hard question of the position and velocity of the electron probabilistically.

In the same way, we can't know what's going on in the brain of any individual organism when they make a subjective evaluation, but we can study how those preferences evolve. We can, if you will, look at the history of diversification preferences. This is a new way to get into this area of the evolution of subjective experience in a way that people have been afraid of, and that's why evolutionary biology has a special role for understanding this aspect of nature, which I would call the aesthetic.

A lot of scientists would probably still be allergic to the words "beauty" and "aesthetic" in science. They think that doesn’t belong. Okay, so maybe you’ve got some concepts. We can progress with them without using those loaded words. But those loaded words, or what people think of as loaded words, are actually effective. They're communicating exactly what it is we want to get at, which is that powerful feeling of, "Huh, I like that," which motivates organisms across the board. Some people think, "Well, how can a bee have a subjective experience? How can they experience beauty? Clearly it's a very simple system responding in a mechanistic way to stimuli, like flowers." If that were the case, if flowers were just specifically designed to push the buttons of bees, make them come and forage because they're so irresistible, then all flowers would converge on that same button, they’d be in the same form, they’d be pushing those bees’ buttons and making him or her forage on that flower. But the fact is that flowers are diverse, they're all different. They're all evolving to be memorably attractive, seductive. They're all appealing to that bee who says, "Huh, do I want to forage on that today?"

Of course to the bees some of those flowers are like nachos, they're cheap and irresistible, but others are special, like carrot cake or whatever. You can go a long way looking for that thing and then enjoy it when you get it. That's what the bees are doing and that's why flowers are diverse, because of the existence and the power of subjective experience as an agent, as an agency in the evolution of organisms.

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After Darwin described the mechanism of evolution by natural selection in the Origin of Species, he had a big problem, and that was the explanation of ornament in nature—those features of the body of animals and plants that function not in furthering the struggle for survival, but in communication with other individuals, and often in the context of mating or ecological interactions. He got a lot of criticism for this, and so he was worried. He wrote to Asa Gray, a great American botanist, in 1861 and said, "The sight of a peacock’s tail, whenever I look at it, makes me sick." Darwin was a sickly guy, and he took a lot of this very seriously. He took it to heart and worried and studied and a little over a decade later, in 1871, he wrote a second book, The Descent of Man, in which he described evolution by sexual selection.

Sexual selection was distinct from natural selection in that it had to do with differential reproductive success. Not survival up until the moment of mating, but differential access to mates as a result of two possible mechanisms: One was male-male competition or competition within the sex, the other was female choice or mate choice of the one sex for members of the opposite sex. Darwin elaborated and predicted how male-male competition should give rise to armaments like antlers and large body size like elephant seals, and that nature should give rise to ornaments like birdsong, beautiful bird plumage and many other ornamental features. Darwin used explicitly aesthetic language to describe his theory. He described the mating preferences of birds as standards of beauty. He described female birds as having an aesthetic faculty. He described birds as the most aesthetic of all organisms, excepting of course man, and he was greatly criticized at the time.

In fact, his theory implied that female aesthetic judgments were a major force in evolution, and that was countered immediately by misogynistic responses who described female choice as "vicious feminine caprice." In those days vicious meant full of vice. In other words, it was even immoral, this theory. In particular, Darwin was criticized for proposing that there was some other theory that might explain evolution other than natural selection, that the power of natural selection was its capacity to explain everything and to be a universal explanation to the origin of biodiversity.

His primary critic and his strongest and most persistent critic was the co-discoverer of natural selection, Alfred Russel Wallace. In the last decade or so of Darwin’s life, Wallace and Darwin were duking it out over the meaning of sexual selection. Wallace was extremely negative about the prospect of beauty and aesthetic having any role in nature, and he criticized the theory in many ways, but he couldn't criticize it entirely. When he admitted that it could occur, he said "Only under special conditions." And those special conditions would be when ornament actually was correlated with qualities that were demonstrably better in terms of natural selection. That is, longer life or better resources or better health. That is, when the trait had evolved some kind of meaning that the female would benefit from choosing.

Today we think of Wallace as the guy who killed sexual selection theory, but actually what Wallace did was describe for the very first time the most popular model of sexual selection today, which is that ornament functions by providing a rich body of information about mate quality that mates need to know, and the basis of which is in this regard, that mate choice is basically about improving conditions of the offspring.

As a scientist I don’t really care that much about this piece of history. I mean, really our job is to come up with and write theories that we have today. I'm interested in what Darwin and Wallace thought and their debates, but it's not critical to science. And yet Darwin still has such an important intellectual status in the world today. This Darwin/Wallace debate is an interesting frame to think about the debate we should still be having.

I'm eager to revive the Darwin/Wallace debate in current biology—comparing Darwin’s broader aesthetic perspective that recognizes that sensory delight, attraction, subjective experience are really the agents of selection in these cases, and Wallace’s honest advertisement of the quality indication model in which the evolution of preference is controlled by a higher power, and that higher power being adaptive natural selection. This is the debate that's happening in literature today and one that I'm eager to inspire. In essence, what I hope to do is to restore the Darwinian view, the legitimately Darwinian view.

In fact, the ideas of honest advertisement and quality indication were variantly anti-Darwinian back in the 1870s, and they still are. Modern neo-Darwinians are really neo-Wallaceans; they aren't Darwinian in the slightest, in the sense that they have laundered out of Darwin’s legacy this history of a regard for aesthetics as an independent force in evolutionary biology, one that is potentially unhinged from natural selection.

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There is this popular reductionist view of neuroaesthetics, which proposes, for example, that through a combination of brain imagery and understanding neuro-function that we’ll understand how the structure of the brain dictates what things will be attractive and not. This leads to a number of reductionist theories of aesthetics. For example, symmetry and indicators of symmetry are particularly important. What any review of art itself in human arts or aesthetic features in organisms will show is that there ain’t no rules, and that rules are made to be broken, and that there is something irreducibly emergent about the way in which subjective experience evolves. And that has to do with what happens when you remove the controlling force of natural selection and allow subjective experience to be an independent player.

The theory on this was actually first developed by Ronald Fisher, who was an evolutionary biologist in the early 20th century and the inventor of statistics and the t-test. Most people and statisticians don’t even know that he was an evolutionary biologist. He came up with an idea: Imagine some females like birds that have red tails and others like birds with blue tails. Then you have males that have both blue and red tails. Well, not surprisingly, females who like red tails are going to find males who have red tails and females who like blue tails are going to find males who have blue tails. What happens is that as a result of selecting on male traits, mating preferences will become genetically correlated with the traits that they prefer. That is, variation in desire and variation in the objects of desire will become correlated or enmeshed, entrained evolutionarily.

What that means is that when individuals, through the action of their preferences, select on traits, they're also indirectly selecting on their own preference. That means that preference is a self-organizing engine of evolution. That is, once you have popularity, then popularity itself can drive the evolution of ornament. What that means is that beauty and the desire for it and preferences coevolve with one another, they are changing one another. The peacock’s tail as it evolves is transforming the female’s brain and her capacity to understand what beauty is, and her preferences are also transforming the tail; they evolve along an entrained path together. Different species are all evolving in different directions, and that's why nature looks the way it does.

The sexual selection mechanism that I'm interested in or that I'm a big fan of really goes from Darwin to Fisher into, more recently, mathematical genetic models by Russ Lande and Mark Kirkpatrick and the intellectual lineage of that group. Of course the opposite have gone from Wallace to a reinvention by Zahavi to lots of modern notions about how ornament should evolve to be honest advertisements. We have this arbitrary mechanism where natural selection is not really involved, and we have an honest mechanism where natural selection is the controlling force. These theories have been around for a while and of course there's been lots of conflict.

My take has been to observe that the adaptationists now rule by essentially rejecting falsification. It's almost a faith-based enterprise in the sense that what people do is they go to nature, they examine a trait, whether it's a patch of plumage or a color of a feather or a birdsong, and they examine everything they can to try to show that it's somehow correlated with some indicator of quality or some measure of direct benefits or good genes. And when they fail to do so, they conclude, "Oh, we're still right. We just haven't worked hard enough to show how it could be true." And when they find that it is true, they say, "Ah-ha, our theory is confirmed." As a result, what we have in the literature is like a weird bonsai tree. It's composed only of the examples that fit the theory. All of those failures to conform to the adaptive theory are evidence completely consistent with the arbitrary model.

They’ve protected themselves from this, and of course this goes back to a quote by Alan Grafen who said, "To believe in the Fisher/Lande mechanism without abundant proof would be methodologically wicked." Not many ideas even in evolutionary biology have been described as wicked, but arbitrary sexual selection is one of them. There's a lot riding on this, and my gambit recently is to propose that the Fisher model—the arbitrary model, the Lande/Kirkpatrick model—is essentially the null hypothesis. It's the prediction of the consequence of genetic variation in traits and preferences in the absence of natural selection on preferences. And so it's what we should expect a large part of the time.

In essence, the null model or the null mechanism is a tough sell, because basically this is the "shit happens" idea. Well, the latest version of this, of course, is that "beauty happens," and that's my new mantra. Right? But in essence it's a hard sell because a lot of people in science, and particularly in evolutionary biology, got into the field because of the buzz they got by explaining things in terms of adaptation. They're eager to confirm that model, and they see the other model as basically intellectually unsatisfying or potentially wicked even.

It's a tough sell, but like the neutralist selectionist debate that went on in genetic evolution or community assembly and community ecology, you can't really do this kind of science in the absence of a null hypothesis. There is a perfectly legitimate and absolutely worthwhile null mechanism for the evolution of the diversity of singles and aesthetic experiences, and that is the arbitrary Lande/Kirkpatrick model.

I'm proposing this. I hear a lot of silence. A lot of times people will read the paper and say, "Well, I liked what you said up to here but then I had this problem." Of course I can resolve those problems quickly, but yet there isn't this big movement to adopt null models in sexual selection. What's going to have to happen? A lot of it is about differential recruitment—bringing new people into the field who are fascinated by the prospect of studying aesthetic evolution, and that's why I'm here talking to you today.

The adaptationist approach is the one that views ornament as an embodied piece of information, quality information. The arbitrary model is the one in which traits and preferences coevolve with one another purely in an aesthetic fashion and without anything other than the benefits of popularity. The adaptationist position is a lot like the efficient market hypothesis in economics. That is that the value of a commodity— how worthwhile this mate might be or the value of your house—is actually explicitly measureable and will always approach a real value because all the players are honest and rational.

The aesthetic approach or the arbitrary model is a lot like the irrationally exuberant market bubbles. And of course going all the way up to the moment of the crash of the housing market and the consequence economic disaster that happened across the globe in 2007 and 2008 you had efficient market theorists saying that bubbles were impossible. They couldn't exist and even describing them was a silly exercise. These guys are like the ardent adaptationists who would describe the Fisher/Lande hypothesis as methodologically wicked. We have a real parity.

In economics, a lot of people that got into these views were the kind of people who read too much Ayn Rand as children, and they go out into the world to find the environment that supports the kinds of thoughts they have. I would maintain that a lot of people in evolutionary biology have come into evolutionary biology because they were attracted to the concept of adaptation. They were influenced to go into the field so that they could have this buzz of explaining the complex in terms of a law-like overriding idea, and since aesthetics can coevolve in lots of different directions in different species, it evades that, and that's why Wallace got so exercised about Darwin. That's why Alan Grafen described the Fisher/Lande mechanism as methodologically wicked. It is a real existential threat to the global law-like power of natural selection to explain biodiversity.

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I'm an evolutionary biologist. I've done evolutionary biology for my entire career almost exclusively, and yet I have been realizing in recent years that for the most part I find adaptation to be kind of boring. I mean, I know it's ubiquitous and I know it's important and all, yet as an idea, as an intellectual concept for me it's mostly over.

What's really interesting is the fact that the contingency of history and biodiversity give rise to all sorts of things that are much more complicated, much more quirky and much more fascinating than the law-like property of adaptation. This has affected lots of my work where I've been doing phylogenetics, evolution and development, the physics of color production and all these areas where contingency and history have a controlling force. What do you call all that together? I don’t really know. It's an evolutionary structuralism where the contingency of history is an important principle in how evolution proceeds.

One of the important consequences of an aesthetic view in evolutionary biology has to do with the 20th century history of evolution and that period of time when Wallace was successful in redefining all sexual selection as merely a form of natural selection, so there was no theory of mate choice, no aesthetic theory available. This is basically the period between 1880 and 1970.

One of the interesting features during this period when evolutionary biology had no concept of mate choice and all mating was under the control of natural selection, that's also the period of time in which essentially all of evolutionary biology was dominated by eugenic theory. What people don’t like to think about is that essentially every evolutionary biologist in the early 20th century was either an ardent eugenicist or a happy fellow traveler. This is exactly the period of which many of the concepts that we still use in evolutionary biology were codified and defined. The core mathematical theory of population genetics was created. Those influences don’t just go away when we say, "Oh, we're no longer eugenic."

If you stick with the hard line adaptationist view of sexual selection in which mate choice is always for those features of your mate that indicate quality, then essentially all mate choice is about natural selection. It's all about getting ahead. In contrast, if you have an aesthetic theory where sometimes things, merely because they're popular, evolve to be more present, you have essentially an opportunity for decadence to evolve, for not just costly honest advertisements, but things that are genuinely costly.

In essence, by adopting a null hypothesis, a null model of mate choice, or evolution by mate choice, in which arbitrary, aesthetic traits can evolve, you permanently inoculate evolutionary biology from this eugenic past. That's critically important, because it's not gone away just because we’d like it to. We have to build a science that prevents us from doing eugenic science again, and that's when you think about genomics and you think about evolutionary psychology and the lack of a null model or the possibility of an aesthetic null in any of that research program, it's a real and present problem. And that's something that could be transformative for evolutionary biology.

Eugenics was the science of human racial superiority, that certain races had evolved as a consequence of natural selection to be superior to others. It led to a concern both for genetic superiority—eugenic means, you know, "well born," true genes, and that's essentially good genes is one of the honest advertisement theories. Almost the same terminology. Eugenics was also concerned with class and money and the environment. These are what we now refer to as direct benefits. Both of the concerns of eugenics are still actively involved in adaptationist theories about mate choice.

Right now the field of sexual selection and the evolution of mate choice is really dominated by the adaptationist school—the Wallacean position—that all traits and preferences evolve because they're correlated with features that are actually legitimately explicitly better. The arbitrary position has not gotten a lot of play in the last few years, so I'm really trying to create a new way of looking at the field, essentially to destabilize the field by proposing that null models ought to be used and force a new scientific standard on the field so that this confirmationist science, the idea that the only thing that we get published are the things that everybody is comfortable already with those ideas and change them a little bit.

This is very much like the neutralist selectionist debate in population genetics, which occurred back in the ‘60s and ‘70s, and that's the kind of debate I'd like to start, that the history there intellectually demonstrates that you can't do evolutionary science without a null model, and that means there's only one way this is going to go, and that is legitimately accepting a broader aesthetic definition of how mate choice could work, restricted in some circumstances to the adaptationist position, and that's where I'd like to see it head. It's only going to happen through differential recruitment—bringing new people into the field that are attracted to evolutionary biology, specifically because it can do this thing that evolutionary biology cannot do right now.

One of the interesting consequences of the adaptationist view of sexual selection—the Wallacean view—is that we don’t really need an account of why females prefer what they do, we don’t need to focus our attention on the female as an evolutionary agent. The reason is because we have a larger, broader, powerful theory about adaptation that describes what the female is doing. We don’t actually have to construct a theory where we recognize, if you will, aesthetic agency—the capacity of females to influence the evolution of their species.

If you eliminate natural selection or admit that sometimes it's present and sometimes it's not, then we have to ask the question: what are females doing? Why do they choose the preferences they do? And this has given rise in my own work to a series of fascinating research programs in the area of sexual conflict, in, that is, what happens when mate choice and mate competition conflict with one another? A perfect example of this is the case of waterfowl or ducks, and in ducks the males do these elaborate displays. They have the bright green head, "quack, quack, quack," and make way for ducklings, all the little movements that they do. The females are choosing on the basis of those displays, and as a result all different duck species have different plumages and different colors to their body.

Meanwhile, there's another force going on. It turns out that there's a lot of male-male competition, and indeed, this goes back to some deep reproductive biology of the ducks, which is that ducks are one of the few birds that still have a penis. It's a very weird structure. It has an explosive erection, its erection mechanisms are lymphatic instead of vascular, it's stored outside-in inside the cloaca and comes flying out, and they can get very lengthy—up to 40 centimeters, which is over a foot long on a duck that is itself not even a foot long. It's an extraordinary piece of biology. What's going on in these ducks?

In lots of ducks there's forced copulation. It's the equivalent of rape in ducks. In species where there is a lot of forced copulation, females have evolved or co-evolved complex vaginal morphologies that frustrate the intromission or frustrate entry of the penis during forced copulation. For example, the penis of ducks is counter-clockwise coiled and often has ridges or even teeth-like structures on the outside. In this case, in these species, the female has evolved a vagina that has dead end cul-de-sacs, so that if the penis goes down the wrong direction it’ll get bottled up and doesn’t perceive to be closer to the oviduct, or further up the oviduct and closer to ova. And then above the cul-de-sacs, the duck vagina has clockwise coils, so there's literally anti-screw devices that prevent intromission during forced copulation.

What's happened here is that females have evolved the capacity to prevent fertilization due to forced copulation most of the time. This is an indication of an evolution of a female advantage through sexual conflict. How does this happen, and what does this have to do with beauty? Well, the way in which it happens is imagine that if a female obtains the mate that she desires. He's got the bright green head, he's got the "quack, quack, quack" that she loves. Her male offspring are going to inherit the genes for those attractive traits that she likes, and her male offspring will therefore benefit by being preferred by other females of the species who evolved the same preferences.

If she's forcibly fertilized by rape, then her offspring will inherit either a random trait because it didn’t pass the test of her preference, or they will inherit traits that have been specifically rejected by other females, and therefore her male offspring will not be as sexually attractive to other females, and that's a genetic cost to her. That's an indirect genetic cost to her fitness. As a consequence, she’ll suffer a cost to sexual coercion. Those individuals that have vaginal morphologies that allow them to achieve what they desire will benefit because other females will reward them by liking and preferring their offspring. This is about how the evolved normativity—the coevolved concept, if you will—of what is sexy, what females prefer, provides leverage that females can use to evolve, to expand their sexual autonomy, to expand their control, their agency in the face of sexual violence.

In the case of the ducks, one of the problems with this mechanism is that it's purely defensive, so the female evolves a more complicated vagina and the male evolves a bigger penis. She gets even more counterclockwise or clockwise coils, and he’ll evolve a penis that has thorny tooth-like structures on it. It's an arm’s race. And that's not good. That's a lot of wasted investment.

There is, however, another alternative, and that's when female choice can act aesthetically to actually remodel or aesthetically transform male behavior in a fundamental way. A great example is the bowerbirds. The bowerbirds are frugivorous fruit eating tropical birds from Australia and New Guinea and nearby islands, and what happens is the male builds a construction—a bower. Often it consists of two walls of sticks with a passageway in the middle, and he gathers all these materials, sometimes bones or berries or fruits or flowers that are brilliantly colored or sometimes a pile of snail shells, and the female visits the bower and chooses her mate based on the bower architecture and on the materials that he provides.

In this case with the bowerbirds, the male builds a seduction theater at the behest of the female. It's evolving because females prefer it. They want this aesthetic architecture in order to advance their mate choices. What's interesting, of course, is that these structures are aesthetic, but they have this special property, which is that if the female is sitting inside the walls of the bower and the male displays in the front and is showing off his cool stuff, before he can copulate with her he has to go back around the back of the bower, and that gives her a chance to pop out the front. She is essentially protected from date rape.

She can explore and see him in a close distance and all of his stuff, and yet she's protected from being jumped or sexually harassed by the male. And why? Because she has preferred those structures that provide her with a safe refuge in which to fulfill her aesthetic desires. In this case we have in bowerbirds the evolution of aesthetic architecture which prevent forced copulation in the females, and that's another way in which females can use the evolved normative concept of what is beautiful to advance their autonomy.

Through thinking about duck sex and aesthetic evolution, I started to develop a scientific concept of sexual autonomy—the way in which a coevolved concept of what's attractive provides leverage for the advancement of the freedom of choice, the freedom of mate choice. I've worked on birds all my career with some little digressions on butterflies and beetles, but basically I'm an ornithologist. That has led me to really entertain the possibility of aesthetic evolution in response to sexual conflict in human evolution. One of the things that's notable about humans is the transformation of male violence. We still have a species where 98 or 99 percent of the violence is still the result of male behavior, and yet we're notably less violent than our immediate closest relative, things like chimpanzees and gorillas. One of the particular ways in which we're less violent is the moderation of sexual conflict in humans.

To understand where we got where we are, let's imagine your typical old world monkey or gorilla or chimpanzee. The situation for females is pretty grim. There's some male that's in political and social control of your group or of you and he controls most of your sexual life. What happens then is that on occasion when there's social unrest, that male will be deposed and a new male will come in. One of the first things that these new males do is they go out and kill all the babies, kill all of the dependent young. Why? Because lactation or breastfeeding prevents ovulation, prevents reproduction. By killing all the offspring of the previous male, he is advancing his reproductive opportunity. All the females will go into estrus and he will have even a sooner opportunity to advance his own fitness. I's an incredibly selfish male behavior that evolves by male-male competition, and it's a huge negative impact on females.

Back in the '80s, Sarah Blaffer Hrdy and others established that one of the responses that females have to this sexual conflict is to mate multiply with other males in hopes of buying an insurance policy that should that guy become the dominant male, he’ll be less likely to kill her child because he might be its father. But of course like ducks, this just gives rise to an arm’s race. If the female starts having sex with other males, then of course the dominant male is going to be much more likely to respond with force to reinforce his social control. You’ve got an arm’s race going on. Females are mating multiply but it's not because they have desire that they're fulfilling, they're just trying to make the best of a bad situation. They're trying to prevent the killings of their offspring.

What's changed about people? Well, your average gorilla or chimpanzee is really almost an infanticidal maniac waiting for his moment. Humans are pretty bad. We've enslaved each other, we have wars where we wipe each other out, but you know, one of the crimes you don’t read about in the newspaper is males killing children for their own reproductive advantage.

I'm interested in the possibility that aesthetic mate choice in humans—female choice—could have played a critical role in the remodeling of male-male competition, essentially by establishing that those features of males that are associated directly with violent competition are unsexy, or more positively, that those features that are associated with advancing female autonomy evolved to be a new from of sexy. That is the kind of dynamic interaction you get between sexual conflict and aesthetic mate choice that we see in birds like bowerbirds and lekking birds and throughout the bird world.

What would these traits be? Well, one of the interesting things is that even though human beings evolved to be much larger than their chimp-like ancestors in body size, they actually have gotten less different in size. Males and females are more similar in size than are chimpanzees. This is exactly against the laws of allometry, which indicate that as you get bigger any differences between the sexes should get broader. That means there's been active selection to reduce the difference in body size between males and females, and that's very likely to have evolved through female mate choice.

Another example is no further than the human smile. All you got to do is look at our smile. We have canine teeth that are sexually monomorphic. In all of our old world primate relatives, including our immediate most close relatives—the gorillas and chimpanzees—the males have deadly weapons in their mouths, which human males lack. The question is, under what conditions are males going to give up their weapons? The answer is really difficult. You’ve got to get them below the belt. It's interesting that of course the Greeks thought of this first in the play Lysistrata (performed in Athens in 411 BC ), and in that Lysistrata organizes the women of Greece and Sparta to create a sex strike. They won't have any sex until the men call off the war against Peloponnesia. Eventually after lots of comedy the males relent and the war is over and everybody goes back to sleeping.

What's perceived, interestingly and appropriately, is that females, organized together, can transform male-male social relationships through mate choice. That is, the importance of bromance before romance. There's something about male cooperation which is particularly attractive to women, and that has had a transforming effect. Of course this is really an important issue. Everything we know that's distinctive about human biology is predicated upon the lengthening of the childhood, child dependency and parental investment, whether it's the brain size, the development of a language capacity, culture and the capacity to learn culture, material culture, technology. All of this required having longer growing up times and a longer time to get smarter and smarter individuals.

Solving the infanticide problem was a big deal. It would be very, very difficult to evolve to invest more in every offspring if potentially a third or a quarter of all offspring are murdered as a result of social violence. And so perhaps one of the key features in the evolution of humanity is the solving of sexual conflict and infanticide problem, and that's why aesthetic evolution and it's interaction with sexual conflict has a fascinating role to play in understanding human nature and the evolution of human biology.

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I started bird watching as a child about ten years old, when I got my first pair of glasses and suddenly the earth came into focus around me and within six months I was a bird watcher. I started with the listening and obsessive listing. I was living in a small town in southern Vermont at that point, and I trampled over hill and dale and all around to see as many birds as I could, and I got hooked on biodiversity. One of the things, as a kid, when you start learning birds and learning birdsongs, you're establishing mental circuits—a way of your brain working in the world that captures this kind of knowledge in an efficient way. It becomes how you think. When I got to college I knew I was going to be involved in ornithology, and I actually imagined myself becoming like a park ranger or running a refuge. I thought that's what it was. I had a good education, but I didn’t know what science was as a life.

Then I discovered that evolutionary biology was the field of science that was about what I was really interested in, which was biodiversity and the origin of all the different birds that I had been learning. I soon got influenced and interested in phylogenetics, the reconstruction of the phylogeny bird, which was the revolutionary event that was happening right at that time. Ultimately I tried to combine my experience with bird watching with my interest in phylogenetics, and I ended up studying the evolution of courtship display in a family of South American birds called manakins, spending a lot of time in the jungle describing the courtship dances of birds that prior to that time were only known for museum drawers, that were not really known in life, and that was delightful.

Part of that work was listening and learning birdsong, and even from a young age I was always able to do that. Starting in grad school I had a sudden virus, idiopathic hearing loss, probably viral, attack my right ear. It took out everything above 1500 hertz. That's about the middle high range on the right hand side of a piano. Overnight. About five or ten years later I started to develop what's called Meniere’s Disease in the opposite ear, which is a problem of control of the endolymph, the fluid inside the ear, and ultimately lost all that hearing.

In the middle of my thirties, having made a career out of studying birds in the field and studying their behavior, I suddenly couldn't hear them any longer. Right now I'm pretty much ornithologically deaf. I can hear a crow, I can hear the bottom half of a robin, but most of the birdsongs of the world I can no longer hear. I suppose I could work on penguins, but that's not the kind of fieldwork I used to do, which was working in the jungle acoustically. In the middle of my career I had to develop a new connection to my life’s work, and that was a big challenge, but that led to a fantastic series of research programs on feathers, on the evolution of feathers, on color, which I can still fortunately see really well, and a whole new kind of research emerged out of that.

At the core of aesthetic evolution is the idea that organisms are aesthetic agents in their own evolution. In other words, birds are beautiful because they're beautiful to themselves. And that scientific conclusion actually has the power to transform our relationship to nature as people who can walk around in nature and regard flowers and listen to birdsong and watch birds and appreciate them in a new way. Aesthetic evolution as a scientific concept has the power to really transform how we experience nature itself, and I know that my own bird watching has been transformed by this. When I'm looking at an indigo bunting, which is a beautiful blue bird, or a scarlet tanager, which is brilliantly red with black ring patches and black tail, then imagining how they came to be through this co-evolutionary dance between traits of the male and the preferences of the female, transform what that's like.

When you're listening to a wood thrush’s complex fluty song and realizing the aesthetic process that's given rise to that, it has a transformative effect. I'm hoping that this view of nature gets out to the public and changes the way in which we look at nature and gets people out more often to learn birdsong themselves and pick up that field guide, identify those birds at the feeder or that are migrating through in the spring. And even though my own brain includes probably hundreds if not thousands of neurons dedicated to learning and knowing birdsongs that I can no longer hear, this exercise of going out into nature and observing it as a human being by understanding the science and the aesthetic lives of the organisms themselves is a really special experience, and I hope that this work will encourage people to do that.