Central to the author's argument is his distinction between natural selection and sexual selection. Miller uses natural selection to denote "changes in the gene pool of a species due to differences in the ability of individuals to survive and reproduce." By contrast, sexual selection is "evolutionary change due to heritable differences in the ability to attract sexual partners, repel sexual rivals, or do anything else that promotes reproduction." While recognizing this is not the way biologists typically use these terms, he points out that Darwin himself used the terms this way, and that conflating them led to errors in the first 150 years of evolutionary science which we are only beginning to dig our way out of.
According to Miller, evolutionary psychologists have made the mistake of viewing the mind only in terms of what it contributes to our survival, treating it like a "swiss army knife" (Pinker) that evolved to deal with a harsh environment. There are several problems with this view, according to the author, amongst them: If large brains and complex minds are so essential to survival, then why did they arise so late in evolution? Why do so few species have them? Claws, wings, and eyes have evolved separately in many species; yet we're the only species that tells jokes and writes sonatas. Why is there such a long lag between the brain's expansion and its survival payoffs? We seem to have reaped the vast majority of them in only the last few thousand years.
We spend a gross number of our calories every day supporting a giant organ with no immediate survival benefits. Yet while natural selection is rather poor at explaining all the brain's abilities, sexual selection is very good at it. Like the peacock's tail, it's a large, wasteful display. And like the courting behaviors of many animals, our abilities to converse, socialize, get along, treat people with respect, charm, flatter, and know what is appropriate are all good fitness indicators. Sure, we reproduce with people who are nasty and uncouth, and we spread those genes through the population, but it's not like we go out looking to do that. People with normally functioning brains are generally socialized, and we prefer that.
I don't know if I'm wholly convinced by his argument. I read a few reviews of the book, and they repeated some concerns I have with the project. What's gotten my attention in this book is that he proposes a new way to understand evolution generally over the last half billion years.
If many innovations originate through sexual selection, we would expect most micro-innovations that distinguish one species from another to be sexual ornaments. This contradicts some traditional views of how species split apart, but, surprisingly, this is pretty much what biologists see. The vast majority of species-defining innovations seem inconsequential for survival. Francis Bacon, father of the scientific method, disparaged the seemingly pointless variety of plants and animals, calling them "the mere Sport of Nature." Darwin was equally perplexed, often wondering why there was so much variety but so little real novelty. If innovations spread through populations because of their survival benefits, why do so few innovations show the survival improvements associated with major innovations and adaptive radiation?We tend to think of evolution as a series of mechanical "pushes" without any "pulls". Mutations arise each generation because of random copying errors at the molecular level. Most mutations are deleterious to the organism, and if they were allowed to proliferate, species would quickly go extinct. But the environment imposes pressure on organisms. Certain mutations make the organism unable to survive in the environment long enough to reproduce and pass its genes on. Rarely, a mutation will confer some extra survival benefit on an individual, and that new gene may proliferate through the population, creating many individuals who have this gene. When individuals with the new genes are no longer able to reproduce with individuals without them or with different genes, there is a new species.
In place of this purely mechanical view of the history of life where mutations arise by accident, and the environment either favors or rejects them, Miller is suggesting a story in which choice plays a much larger role in the direction of evolution. Novelties arise and survive in species, not for the purposes of survival, but for the purposes of attracting mates.
Sexually selected novelties of this sort could be called "courtship innovations." Most will be nothing more than a slightly novel design for a penis, a minor variation in mating coloration, or a different style of courtship dance. But from these humble origins, a small proportion of courtship innovations and their side-effects may turn out to have some survival benefits in addition to their courtship benefits. They may then become favored by natural as well as sexual selection. Of these survival adaptations, a small proportion may prove significant enough to allow a species to invade many new environmental niches. They produce adaptive radiations, proving themselves over time as major innovations. The ecological success of major innovations may hide the fact that many of them originated as courtship innovations.And then he goes on to tell a story in which wings may have originated, not for the purposes of flying and evading predators, but as sexual displays for dinosaurs. There is a similar story to tell about the evolution of large brains in hominids.
If this is true, it explains just as much as natural selection does and more. It explains why there is so much novelty in nature, and it explains why this novelty first arises with the invention of sexual difference. For the majority of its time on Earth, life has consisted in single-celled organisms no larger than a millimeter across. We're still outnumbered by them. There are at least 10 times as many bacterial cells in your body as human cells.
But there probably aren't as many species of bacteria as there are of more complex creatures. Considering how few in number more complex creatures are relative to single-celled organisms, it's amazing how much difference we exhibit. Most of the macro-level differences are color of fins, facial hair, feathers, or other sexual displays that confer no obvious survival benefit. Indeed, there appears to be a sublime abundance of types of life above and beyond what mere necessity would predict but which we would expect if sexual selection takes the lead over from natural selection.
The "pushes" (natural selection) may have the final say, but only if the "pull" (sexual choice) egregiously contradicts the demands of the environment. Between what life whimsically craves and what the environment unconsciously rebukes, there appears to be a lot of wiggle room.
And of course sexual selection involves choice. It's minimal with a pair of earthworms, but it becomes quite complex when you get up to insects. Is there something that it's like for a female beetle to be excited by the colorful display of a male beetle? We'll never know, though that display, which is wasteful and dangerous because it attracts predators, plays a function in beetle courtship.
As one moves to more complex forms of life, the choices are also more complex. It's doubtful a male bird of paradise is just exciting a female. I don't think it's excessively anthropomorphic to say he's trying to impress her. There may be no difference between those two things from a purely physical point of view. It's all just neurons firing. But the courtship ritual is more complex and has greater texture of meaning, and the female has to take more things into consideration, so her act of choosing is more complex.
I wrote earlier about Teilhard's law of complexity/consciousness, according to which "mind" is present in all matter, but it increases proportional to the complexity of the arrangement of matter. I think what Miller is arguing might add some depth to that idea. The invention of sexual difference allows choice (a proto-subjective state) to arise for the first time, and it allows for the evolution of greater complexity (and hence more complex and varied distinctions between "inside" and "outside"). That's why life really takes off half a billion years ago.
Did this revolution—call it the original Sexual Revolution—have to take place? Would any planet with life on it have to eventually invent sexual difference? I don't know. However, it's intriguing to think that, given the Sexual Revolution, complex minds had eventually to evolve.
I have to think about this and develop it more, but I'll end with this quote from Miller:
We can see that, once sexually reproducing animals evolved the capacity for mate choice, every animal species would then evolve some sort of fitness indicator; and that some indicators might be costly, exaggerated body parts, and others would be costly, ritualized courtship behaviors. But we could not have predicted that courtship behavior would reach an especially high degree of sophistication exactly 535 million years after the Cambrian explosion (when multicellular animals proliferated) in our particular species of bipedal ape. Nor could we have predicted that the courtship behavior would take the precise form of interactive conversations using arbitrary acoustic signals (words) arranged in three-second bursts (sentences) according to recursive syntactic rules. Perhaps it could have happened in an octopus, a dinosaur, or a dolphin. Perhaps it was likely that it would happen sometime, in some species of large-brained social animal. Rewind the tape of evolution, and the human mind would probably not have evolved, because sexual selection would have taken a different contingent route in our lineage of primates. But I suspect that in any replay of evolution on Earth, sexual selection would sooner or later have discovered that intelligent minds similar to ours make good courtship ornaments and good fitness indicators.Emphasis mine.