For simple traits that depend on just a few genes, selection is pretty good at eliminating mutations. Each mutation is likely to cause such dramatic change that natural selection rapidly eliminates it But for very complex traits, like human brains, that grow through the interaction of many genes, mutations are harder for selection to eliminate. There are more genes vulnerable to mutation in the first place, and selection's effects get diluted across more genes. This decreases selection's power to eliminate mutations on any one gene. With mutation stronger and selection weaker, complex traits are less likely to be perched on the peak of perfection.
Genetic variation is more likely to be manifest in complex traits. This makes complex traits like the human brain better fitness indicators.
Imagine all the DNA in our 23 pairs of chromosomes laid end to end in a single strip. The DNA from a single human cell would be about six feet long, and contain about 80,000 genes. Imagine that the genes involved in growing a particular trait are lit up in bright green, and that each gene has a tiny chance of having a mutation that turns the green fight red. For a very simple trait like skin color, there might be only half a dozen lights sprinkled along the six-foot length of DNA. It is very unlikely that any of them would be red. For a moderately complex trait like the shape of the human face, there might be several hundred fights. It is likely that a few of them might be red. For a very complex organ like the human brain, there might be tens of thousands of fights. Our DNA would fight up like a Christmas tree. Although the proportion of red lights would still be very low, the absolute number would be much higher. The brain would give much better information about mutation load and fitness, because it gives mate choice a wider window on a larger sample of our DNA. (The larger the sample of genes, the more accurate the estimate of mutation load.) This is what biologists mean by the "mutational target size" of a trait: the proportion of the genome that is involved in a trait's development determines the proportion of all mutations that are visible in the trait.
At the moment, nobody knows exactly how many of our genes are involved in growing our brains. Geneticists sometimes estimate that about half of our genes are involved in brain development, and about a third might be active only in the brain. If this guess is about right (and we shall know within a decade or two whether it is), then the mutational target size of the human brain is about half the human genome. The brain probably has a larger mutational target size than any other organ. Of all the new mutations that mess up something during human development, half of them mess up something in the human brain.
If mutations maintain most of the variation in fitness that we see, then the organs with the largest mutational target sizes will make the best fitness indicators. The human brain should make a very good fitness indicator indeed. Its vulnerability to mutation is precisely why sexual choice mechanisms should evolve to pay attention to its performance.
In the rest of this book, I shall take the heritability of fitness for granted. The expectation that fitness should not be heritable was based on theoretical arguments developed in the 1930s. Those arguments are contradicted by the evidence. Wild populations show large amounts of genetic variation. Biologists routinely find individual differences in reproductive success in the wild, differences which are often genetically heritable. Fitness remains heritable in most species for most of the time. It seems likely that a lot of this continuing heritability is due to the continual rain of mutations. Some biologists even wonder how selection can possibly be strong enough to eliminate all these new mutations, and keep the species from falling apart. Fitness-eroding mutations are ubiquitous, and usually stick around for a fairly long time. There is always a tension between mutation and selection. And there are always fluctuations in fitness across time and space which keeps fitness heritable. These are just the facts of life. Mate choice evolves to deal with them.
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