The Evolution of Beauty: How Darwin's Forgotten Theory of Mate Choice Shapes the Animal World and Us. By Richard O. Prum. Doubleday, 2017.

I’m always hoping I’ll come across stories that enhance my appreciation of living creatures. I started Prum’s book hoping to find there such a story. What I found was more complicated.

I don’t care whether a story is true--I anyway wouldn’t know how to tell—I’m satisfied if it leaves me feeling I understand nature better. I can usually tell that in advance from what kind of story it is: “just so,” or “as if.” “Just so” stories don’t help you appreciate anything, they tell you it’s “just so.” An example of that is the modern synthesis of genetic mutation and natural selection. Of anything in nature I want to know why or how it simply says, “it’s just so.” That may be true but it doesn’t add anything to my understanding. I began reading Prum’s book on the lookout for what kind of story he’d be telling. If it was a “just so” story I’d read no further.

What I hoped to find instead was an “as if” story. That’s a story that adds meaning to some aspect of nature, ideally to nature in general. Richard Dawkins provided us with a story like that in his book “The Selfish Gene.” He didn’t mean genes really are selfish, he meant that, from what he knew about evolution, it was “as if” genes are selfish. Take that story to heart, he assured us, and you’ll feel you understand nature better, too. 

Prum’s introduction charmed me. His writing was direct, personal, full of incident, full of feeling. And he did indeed promise me a new story. “I have always been more fascinated by those aspects of evolutionary process that defy simplistic adaptive explanations,” and "aesthetic evolution has great explanatory power, and... rescues us from the tedious and limiting adaptionist insistance on the ubiquitous power of natural selection," finally "the evolutionary dynamics of mate choice are essential to understanding ourselves." Terrific! I was going to encounter some other story than the “just so” of the modern synthesis, a story we could apply to more fully understand ourselves.

Prum’s field of sexual selection usually offers us slim pickings of “as if” stories able to contribute to our understanding. Most evolutionists insist on giving animal choice no place at all in evolution, he reports. He mimics them: “What can we possibly know about the subjective experience of desire in animals? Subjective experience is, almost by definition, unmeasurable and unquantifiable.” He goes on, “Most scientists have therefore been allergic to the idea of making a scientific study of subjective experiences, or even to admitting that they exist.” They regard sexual displays and preferences merely as parts of the environment a creature must become adapted to. For them, Prum mourns, “beauty is merely the handmaiden of natural selection.”

That’s not so for him.

Although I am rather hesitant to admit it, I think that the process of adaptation by natural selection is sort of boring. Of course, as an evolutionary biologist I am well aware that it is a fundamental and ubiquitous force in nature. I don’t deny its immense importance. But the process of adaptation by natural selection is not synonymous with evolution itself. A lot of evolutionary process and evolutionary history cannot be explained by natural selection alone.

His own field work tells against it. Of bower birds he says:

But how do we know that bower design and ornamentation perform an exclusively aesthetic function? Well, we know that the bower serves no physical purpose other than as a location where courtship takes place.

Not only that:

Evolution can even be “decadent,” in the sense of its resulting in sexual ornaments that not only fail to signal anything about objective mate quality but actually lower the survival and fecundity of the signaler and the chooser. In short, in pursuit of their subjective preferences, individuals can make mating choices that are maladaptive resulting in a worse fit between the organism and its environment…. Natural selection is not the only source of design in nature.

Instead he inclines towards a story of Darwin’s, who he quotes as follows:

Courage, pugnacity, perseverance, strength and size of body, weapons of all kinds, musical organs, both vocal and instrumental, bright colors, stripes and marks, ornamental appendages, have all gained… through the influence of love and jealousy, through the appreciation of the beautiful… and the exertion of choice.

The responsible agent in the story Prum wants to tell, like that in Darwin’s, will involve factors--appreciation of the beautiful and freedom of choice--within the subjective experience of individual creatures.

For me, however, the concept of subjective experience is absolutely critical to understanding evolution. I will argue that we need an evolutionary theory that encompasses the subjective experiences of animals in order to develop an accurate scientific account of the natural world. We ignore them at our intellectual peril, because the subjective experiences of animals have critical and decisive consequences for their evolution.

So Prum is intent on establishing a beachhead behind which to gather support for “an evolutionary theory that encompasses the subjective experiences of animals.”

Talk about fools rushing in! While lauding Darwin in extravagant terms for his boldness in making individual female choice one of the drivers of evolution, Prum appears intent on focusing the world’s attention onto what I see as a glaring contradiction in Darwin’s work. Here’s how I expressed it in my book “re-thinking…”:

According to Darwin, peacocks grew enormous tails because peahens like them that way.  If merely liking something could make a creature evolve it then all of evolution could be driven by creatures “liking” things. Then who needed natural selection!

This idea, that creatures can evolve whatever they want merely by wanting it, makes of evolution nothing more than a giant Law of Attraction—creatures will get whatever they wish for hard enough. Yet that does seem to me the principle behind Darwin’s mechanism of sexual selection—by wanting it, peahens can get peacocks to evolve just the kind of tails they’d like. Why didn’t Darwin go on from there to assume that all of evolution could be driven like that, by living creatures experiencing wants in the course of their interactions with the environment? Instead he retreated timidly back to account for all of evolution through a strict reductionist/adaptationist mechanism excepting only the one instance he couldn’t make that mechanism account for, sexually-induced ornament in birds. But by doing so he left the door open for others to say, if creatures wanting some evolutionary change could make it happen in one instance, why not in all? That’s exactly the door that other evolutionists want to keep firmly closed. That’s exactly the door that Prum seems intent on flinging wide open. In the following paragraph he implies that ornaments and sexual preferences for those ornaments differ from all other subjective experiences only because in their case how subjective experiences trigger physical evolution is particularly easy to trace:

We cannot measure or know what these [subjective] experiences are like in any detail, but we can sneak up on them, and as with the electron we can learn fundamental things about them indirectly. For example, as we will see, we can investigate how subjective experiences evolve by tracing the evolution of ornaments and the sexual preferences for them among closely related organisms.

To summarize my very long introduction, Prum intends through his study of sexual selection in birds to come up with a story about how they evolve that will help us understand how evolution works in nature in general, and ultimately how it works in us. What I looked forward to finding out from the rest of his book was how much of evolution he was prepared to convert over from the adaptationist “just so” story to a “subjective experiences” story.

And just who did he think was having these subjective experiences? Perhaps because it’s so common among us, it’s easy to imagine males giving in to nagging from their mates about looking good, and dressing more colorfully. In ducks, for example, females can see how males look, and keep after them until they’ve shaped up. Vision provides a ready feedback loop within the individual duck by which she can detect discrepancies between what she would like to see, and what she actually sees. And that goes for all of the senses. That presumably is what led Darwin to set this kind of evolutionary change apart from evolution by natural selection and call it “sexual selection,” and for Prum to prefer the more specific term “aesthetic selection.” That is, selection can be driven by an esthetic sense within subjective experiences in individual living creatures, as we humans detect having an esthetic sense operating within our own subjective experience.

Prum then goes on to describe the seasonal eruption of violence as drakes coerce females into having sex. In association with this contest between male coercion and female choice strange things happen. Drakes' penises grow to an absurd length and extend themselves within the females' vaginas through a clockwise twisting movement, like an elaborate lock picker's tool. The females, in defense of choice, develop a similarly convoluted vagina, with blind endings and a characteristic counter-clockwise twist, to stall the male.

But is the story of “aesthetic selection” plausible when applied in a case like this? While it’s easy to see how these strategies fulfil the wants of both sexes, where is the sensual feedback by which they could be monitored? Even if the female could imagine turning her vagina into an obstacle course for the male’s penis, how could she be directing a process she can’t monitor in the same way she could visually monitor how well her drakes are conforming to her vision of how they could look?

Still, this process of vaginal reconstruction does look exactly like what you’d suppose is a response to subjective female choice. And that really is what Prum believes. For him, how the female duck experiences “forced copulations” is no different from what human female’s experiences during rape.

“Forced copulations” is the term that ornithologists and evolutionary biologists now use to refer to rape among birds and other animals… Human rape is an act with such great symbolic and social impact that the term didn’t seem appropriate in the context of non-human animals…. Although I do not suggest that we return to the wholesale use of the word “rape” in animal biology, I think that the phrase “forced copulation” does an intellectual disservice to our understanding of sexual violence in non-human animals. Certainly in the case of female ducks, it is scientifically critical to recognize that sexual coercion and violence are very much against their wills too.

Not any longer against their esthetic sense. Against their wills! I propose we call this new principle “evolution by volition,” or “evo voli.”

But even a story involving the volition of individual creatures can be stretched only so far. Prum goes on to give another example, the Club-winged Manakin, unique for the male having altogether-reconfigured ulnas, four times wider and three times larger in volume than those of related species. "In fact, there is nothing else like it in any other bird in the world." Birds’ ulnas have been honed to an invariable sleek mechanical perfection over 135 million years of adaptation to the demands of flight, yet uniquely in the male of this species it has become reshaped in an extraordinarily complicated manner to generate sounds as part of the male's courtship dance. "It is the acoustic collaboration among the multiple feathers attached to the male's ulnas that gives the sound its distinctive harmonic structure and decidedly musical, ringing, violin-like quality." Surely the idea of reshaping a part of your body vital to flight so extravagantly merely to serve sexual display could not have arisen in the subjective experience of any one animal. In my judgment, any story accounting for such evolutionary changes through subjective experience has to locate whatever mind is making those imaginative leaps elsewhere than in individual living creatures.     

Have I lost you? Let’s recap. Whose subjective experience is involved in sexual selection? In the case of the duck directing how her drakes dress we can imagine it being her, we can imagine it taking place in her mind, since she can monitor the process visually as it’s going on. That’s an esthetic selection story. But in the case of the reconstruction of her vagina during mating season, it’s hard to imagine such a thought entering her mind, and even if it did it’s hard to see how it could take place without her being equipped with senses through which she could monitor the process. So who is exerting choice on her behalf? Perhaps it is a representative of the females of her species about which we might create a story involving some ancient female goddess. But even that won’t suffice in the case of the bird with the singing ulnas. The process of shaping his ulna occurs so early in development that it affects the females also, who therefore are burdened with the same impediments as the male but without any corresponding benefit. It seems unlikely that even a female representative of the females of her species would inflict such a pointless burden on her, would so punish her for her lustful delight in her mates’ performance. So in this case, is the subjective experience occuring in the mind of the species as a whole, in expression of its desire to contribute this enhanced performance to the wonders of nature, even at the cost of lessened fitness in both of the species’ sexes?

For me, Prum’s researches open up a huge can of worms. He has analyzed the courtship dances of tropical birds into their component parts and been able to trace the origins of individual components back to ancestor species still living a thousand miles away. Some appear entirely original, and the product of creative subjectivity. Yet it seems impossible to locate the subjective experiences through which he expects to account for the evolution of such items in the minds of individual living creatures. So, must we default back to the prevailing “just so” story, the modern synthesis? No, Prum's fieldwork makes that highly implausible too. Anyway, I’m sure Prum wouldn’t want to see us forced back to that resort.

Through his rashness Prum seems to me to have indeed reduced to a pile of tiny chips all the principles we have available to account for the remarkable creatures he studies. Instead his fieldwork hints at shadowy intelligences lurking in the undergrowth or the canopy directing the evolution of some of the most remarkable tools and ornaments with which living creatures come equipped. Okay, that’s the inference, but where’s the story? Prum admits he doesn’t have one. Perhaps to the story of sexual selection he found in Darwin he should have added that identified by Siddhartha Mukherjee in his "The Gene": "The crucial driver in evolution, Darwin understood, was not nature's sense of purpose, but her sense of humor." Lacking such a story, Prum ends his book with no more revelations about how we evolved than some details of our genitalia.