Note: This is not as much a book review as it is an exploration of my current stance on a central debate in the field of evolutionary biology. I have used the popular example of a peacock's tail but it can be replaced with any male aesthetic trait in a species with significant sexual dimorphism. As for the book - Prum is sufficiently nuanced with his treatment of sexual selection theory, viewing it first in a ornithological context and then carefully extending it to other phylogenies, including humans. Recommended.
Why is the peacock's tail so beautiful?
Darwin had originally proposed two fundamental forces behind evolution - natural selection and sexual selection. He used sexual selection and aesthetic mate choice by females to explain the peacock's tail and other aesthetic traits found across the natural world. Aesthetic traits in males coevolve with female preferences for those traits in a runaway process to create something like a peacock's tail. Over several iterations (as R.A. Fisher would mathematically prove about a century later), female aesthetic taste leads to careful fine-tuning of male aesthetic traits and...beauty happens. Similar to how the price of a tulip kept increasing due to market preferences during the Tulip Bubble of the 1600s, the peacock's tail, lion's mane, and elk's antlers have become what they have due to generations of females acting on their arbitrary aesthetic preferences. Fisherian aesthetic selection is the genetic equivalent of a market bubble driven by irrational exuberance. The irrationality of the aesthetic selection process is evident in how it is often at odds with natural selection. Beauty competes with survival (survival in the face of both environmental threats and male-male competition). The natural world of birds and animals we ultimately observe is the game-theoretically stable state of beauty vs. survival, both constantly interacting with and influencing each other.
So according to Darwin, the peacock's tail has been shaped by generations of peahens and their subjective tastes (I'm reminded of Oscar Wilde's The Critic as Artist as I write this). Unfortunately, a theory with subjectivity, animal agency, and more importantly female agency at its center had no place in 19th century Britain.
The lesser-known co-discoverer of evolutionary theory, Alfred Wallace, was a staunch utilitarian and believed that to invoke 'female choice' was bordering on mysticism. He believed instead that beauty has to have a function. Wallace proposed that male beauty serves as an indicator of good health and fitness. The peacock with its iridescent blue plumage and gorgeous tail is signaling its fitness and the absence of disease to females. Due to Wallace's fierce efforts to proselytize the idea, beauty-as-utility became the standard explanation. Sexual selection now only existed as a sub-set of natural selection, both ultimately maximizing purely adaptive functions.
Amotz Zahavi later introduced the handicap principle or the idea that that the peacock tail (to continue using the example) is an honest signal of fitness because it inflicts an undeniable cost on the male who possesses it. The fact that I have survived for so long despite my extremely conspicuous and heavy tail is a testament to my fitness and good genes. If a signal is costly, it must be honest. Zahavian signaling lent credence to Wallace's beauty-as-utility idea and this neo-Wallacean adaptionism has since taken over the field of evolutionary biology.
To me, the neo-Wallacean view was very enticing when I first encountered it. On the surface, it paints a very rationalist picture of evolution through natural selection. In this view, sexual selection falls under natural selection as just another process through which organisms are selected for fitness. Everything must serve an objective, adaptive function. Indeed, I found immense comfort in this idea for over three years during which I was surprisingly only exposed to the adaptionist view of Darwinism. Darwin's core idea of sexual selection (which he describes in The Descent of Man) is conspicuous by its absence from today's Darwinism. It speaks to how dogmas can completely take over a science. It is particularly concerning given that empirical evidence in support of the beauty-as-utility theory seems to be virtually non-existent.
Perhaps one of the reasons why I found comfort in the beauty-as-utility explanation is because of its simplicity. It flattens the intellectual complexity of the world around us into a singular, definitive explanation. While the explanation might be easy to intuit, I have now come to believe that it is likely a parochial and incomplete view of life. It overfits reality into a rationalist framework that is unsupported by real-world evidence. The dogmatic persistence and the quasi-religious fervor around the neo-Wallacean theory in fact reminds me of the field of economics prior to the behavioral revolution of the early 2000s.
At the heart of economics and finance was the assumption that all humans were rational agents making rational decisions that would maximize their utility. Humans are objective, decisions are rational, and markets are efficient. It took Kahneman, Tversky, Shiller, et al. and about two decades of work for that core assumption to be put to bed. Eric Weinstein talks about economics as an 'as-if physics' of natural and sexual selection. I have spoken to economists who shy away from this explanation (the idealist in me says it's due to humility and not willful ignorance) but I find it to be an extremely useful framing. It is no surprise to me then that economics, the physics of natural and sexual selection, was made richer by the introduction of irrationality, subjectivity, and randomness, which seem to be an inherent part of the natural world. Evolutionary science, which is essentially the philosophy of natural and sexual selection, needs to catch up.
Here's a small example of a logical problem with the neo-Wallacean beauty-as-utility theory. The peacock's tail is obviously costly to the peacock who possess it, at least marginally reducing the probability of his survival. But that is only half the story. Peahens suffer an indirect cost through their male offspring who will carry the burden of a tail. This implies that the adaptive benefit that peahens receive from picking males with the most beautiful tail must outweigh the cost inflicted on their male offspring. If that is the case, then over time in a population, one should expect to see diminishing returns from female vigilance as harmful genes will eventually be selected out of the population. One should subsequently expect to see female vigilance go down over time to compensate for the indirect cost that comes with picking males with the best tails. This would create an oscillating pattern in the population with female vigilance increasing while the benefit outweighs indirect costs and then once an equilibrium is attained, female vigilance should drop. We do not observe this pattern in nature. Moreover, several studies conducted on peacock tails and fitness have failed to find any meaningful correlations. Perhaps peahens select peacocks with beautiful tails because they just really like beautiful tails.
The beauty happens hypothesis driven by female aesthetic mate choice is the most parsimonious explanation for the evidence we see in the world around us. The onus should be on the adaptionists to prove whether beauty has utility. Darwin ends the Origin of Species with the phrase - 'There is grandeur in this view of life...'. I believe that aesthetic selection with its focus on subjective preferences of discerning creatures across phylogenies is essential to maintaining the grandeur in Darwin's theory.
So aesthetic selection explains how female peahens have over generations shaped the male peacock's tail based on what they find beautiful. The question I'm left with now is...why do we find the peacock's tail beautiful?
Addendum: I consciously decided to not include any discussion on how aesthetic selection plays out in humans because it wasn't necessary for the purposes of this review. Prum has some interesting speculative hypotheses in the second half of the book. Recommended.