Why (brain) size really matters

Charles Darwin made not one, but two great contributions to evolutionary theory. The first is the one that everyone thinks they know: the mechanism of "natural selection", leading to what Herbert Spencer called "survival of the fittest". The other is "sexual selection by mate choice", formally proposed in 1871, which says that creatures who reproduce sexually must evolve features to attract mates, for they will not leave offspring unless they do. The two driving forces are largely in conflict, as illustrated by the peacock's tail: wonderful for pulling hens, but potentially disastrous for evading tigers.

But although biologists (and the world at large) embraced natural selection (albeit often in garbled form and with various shades of political overlay), they largely ignored sexual selection for the next 100 years. The business of attracting mates just seemed too frivolous: too effete to compete with the vicissitudes of blood-and-guts survival, so ruthlessly and obviously subject to natural selection.

Sexual selection re-emerged only when a few biologists in the 1980s finally realised the force of what Darwin had said: no mates, no offspring. There is nothing frivolous about mate attraction, even if the features it encourages - feathers and antlers - may be pure caprice. In The Mating Mind, Geoffrey Miller, one of the brightest sparks in modern evolutionary theory, shows how sexual selection might resolve one of the most taxing puzzles of biology: why our own kind of animal, Homo sapiens, is so extraordinarily clever.

The traditional explanation (apart from that of the Book of Genesis) is rooted in natural selection. Big brains and the intelligence that goes with them are obviously useful, the traditionalists say, and are bound to enhance survival. Humans are ground-living apes whose arms and hands are no longer needed for locomotion and so have been freed for making tools.

Ever-more dextrous hands encouraged the selection of bigger brains, and vice versa. By such "co-evolution", the human brain has doubled in size this past two million years, from 700ml to around 1450ml - an unprecedented increase, and miraculous in such a twinkling of biological time.

But there is a snag with this scenario. Dour survival pressure might indeed produce nimble fingers and the ability to count to a dozen or so (if only to keep track of mammoths and rival predators) but modern humans can do much more. Some can do calculus and quantum mechanics. Similarly, we don't just scratch directions on the rocks. A few of us can paint like Titian.

Nor do we simply draw up hunting rosters. We write sonnets. We are not merely agile. We dance like Nureyev, and spin like Comaneci. In short, our palpable abilities far outstrip the requirements of survival on the Pleistocene plains of Africa - so how could they have been shaped by natural selection?

Defenders argue that our present skills are side-effects: evolving the ability to count to 12 we also, somehow, developed the essentials of algebra. Miller's sexual-selection thesis stands in absolute contrast. He proposes that men in particular evolved a phantasmagoria of skills - from high-flown philosophy to break-dancing and fine art - just as peacocks evolved their tails: to show women what fine fellows they are. Of course, such features far exceed the requirements of mere survival. That is their point. They are meant to advertise underlying strengths, for only superior individuals can afford such extravagance. Women evolved the same skills because the genes that women select in their men are passed on to their daughters, too.

The theory of sexual selection gives rise to many key ideas of modern evolutionary thinking. What features do people find sexually attractive? The particular chemistry remains mysterious but wit, humour, and kindness are demonstrably among the acknowledged components of "charm". Why should such qualities appeal? It isn't enough to say "because wit is fun". Why do we find it fun? Why aren't we appalled by frivolity, as a Puritan might affect to be (although only by exercising self-restraint)?

Because wit is an index of intelligence - which indeed is worth having in a mate. Natural selection on its own could not take intelligence beyond the ability to stalk a mammoth; but the need to demonstrate intelligence to potential mates certainly could, for then the demonstrator must cut an extra dash to outshine all his rivals.

Natural selection produces predictable qualities - strength, speed, resistance to infection, hard hooves in deer and antelope, big teeth in all carnivores, whether dogs, cats, or T. rex. Sexual selection, by contrast, can produce almost any quality, each peculiar to its population. The peacock's tail seems ludicrous, self-destructive. Indeed it is, because it is intended to be gratuitous, the better to advertise underlying strength.

We admire the survival qualities in other species because we would like them for ourselves - the leopard's agility, the stamina of the wolf - but we disdain their particular sexual wiles. Chimps are our closest relatives, but any human being who thrilled to the red swollen rumps of the ovulating females would be perverted indeed.

Above all, sexual selection is creative. While natural selection merely chisels away at the genetic mutations that produce variation, "sexual selection through mate choice can be much more intelligent". Each partner practices a kind of artificial selection on potential partners, like a dog-breeder preparing for Cruft's.

Individuals who make bad choices - mistakenly choosing partners who are stupid or ridden with parasites - leave blighted offspring. Their lineages die out. Those who select features that connote true ability do well. Thus features like wit and brilliant feathers that advertise underlying strengths are enhanced with each generation. And so, commensurately, is the partner's predilection for such qualities. Thus a feedback effect results of the kind that could indeed double the human brain in a mere two million years.

The Mating Mind is an exercise in evolutionary psychology, and EP should be seen as an Enlightenment pursuit with Darwinian insights, which aims to tease out the roots of human nature. Critics of EP with their tired little portmanteau of slogans - "just-so stories" and "biological determinism" - have missed the point, and should be ashamed of themselves. Miller is the real thing, and his wonderfully readable book should be read by everyone with a taste for serious ideas.

Colin Tudge's new book, 'The Variety of Life', is published by Oxford