The Blind Watchmaker (35 page)

It is an obvious fact that, when we measure almost anything about animals, although most members of a species are fairly close to the average, some individuals are a little above average, while others are below average. We can be sure that there was a range of tail lengths in the ancestral widow bird, some being longer and some being shorter than the average of 3 inches. It is safe to assume that tail length would have been governed by a large number of genes, each one of small effect, their effects adding up, together with the effects of diet and other environmental variables, to make the actual tail length of an individual. Large numbers of genes whose effects add up are called polygenes. Most measures of ourselves, for instance our height and weight, are affected by large numbers of polygenes. The mathematical model of sexual selection that I am following most closely, that of Russell Lande, is a model of polygenes.

Now we must turn our attention to females, and how they choose their mates. It may seem rather sexist to assume that it is the females that would choose their mates, rather than the other way round. Actually, there are good theoretical reasons for expecting it to be this way round (see
The Selfish Gene
), and as a matter of fact it normally is in practice. Certainly modern long-tailed widow bird males attract harems of half a dozen or so females. This means that there is a surplus of males in me population who do not reproduce. This, in turn, means that females have no difficulty in finding mates, and are in a position to be choosy. A male has a great deal to gain by being attractive to females. A female has little to gain by being attractive to males, since she is bound to be in demand anyway.

So, having accepted the assumption that females do the choosing, we next take the crucial step that Fisher took in confounding Darwin’s critics. Instead of simply agreeing that females have whims, we regard female preference as a genetically influenced variable just like any other. Female preference is a quantitative variable, and we can assume that it is under the control of polygenes in just the same kind of way as male tail length itself. These polygenes may act on any of a wide variety of parts of the female’s brain, or even on her eyes; on anything that has the effect of altering the female’s preference. Female preference doubtless takes account of many parts of a male, the colour of his shoulder patch, the shape of his beak, and so on; but we happen to be interested, here, in the evolution of male tail length, and hence we are interested in female preferences for male tails of different length. We can therefore measure female preference in exactly the same units as we measure male tail length - inches. Polygenes will see to it that there are some females with a liking for longer than average male tails, others with a liking for shorter than average male tails, and others with a liking for tails of about average length.

Now comes one of the key insights in the whole theory. Although genes for female preference only
express
themselves in female behaviour, nevertheless they are present in the bodies of males too. And by the same token, genes for male tail length are present in the bodies of females, whether or not they express themselves in females. The idea of genes failing to express themselves is not a difficult one. If a man has genes for a long penis, he is just as likely to pass those genes on to his daughter as to his son. His son may express those genes whereas his daughter, of course, will not, because she doesn’t have a penis at all. But if the man eventually gets grandsons, the sons of his daughter may be just as likely to inherit his long penis as the sons of his son. Genes may be carried in a body but not expressed. In the same way. Fisher and Lande assume that genes for female preference are
carried
in male bodies, even though they are only
expressed
in female bodies. And genes for male tails are carried in female bodies, even if they are not expressed in females.

Suppose we had a special microscope, which enabled us to look inside any bird’s cells and inspect its genes. Take a male who happens to have a longer than average tail, and look inside his cells at his genes. Looking first at the genes for tail length itself, it comes as no surprise to discover that he has genes that make a long tail: this is obvious, since he
has
a long tail. But now look at his genes for tail
preference
. Here we have no clue from the outside, since such genes only express themselves in females. We have to look with our microscope. What would we see? We’d see genes for making females prefer long tails. Conversely, if we looked inside a male who actually has a short tail, we should see genes for making females prefer short tails. This is really a key point in the argument. The rationale for it is as follows.

If I am a male with a long tail, my father is more likely than not to have had a long tail too. This is just ordinary heredity. But also, since my father was chosen as a mate by my mother, my mother is more likely than not to have preferred long-tailed males. Therefore, if I have inherited genes for a long tail from my father, I am also likely to have inherited genes for preferring long tails from my mother. By the same reasoning, if you have inherited the genes for a short tail, the chances are that you have also inherited the genes for making females prefer a short tail.

We can follow the same kind of reasoning for females. If I am a female who prefers long-tailed males, the chances are that my mother also preferred long-tailed males. Therefore the chances are that my father had a long tail, since he was chosen by my mother. Therefore if I have inherited genes for preferring long tails, the chances are that I have also inherited genes for having a long tail, whether or not those genes are actually expressed in my female body. And if I have inherited genes for preferring short tails, the chances are that I have also inherited genes for
having
a short tail. The general conclusion is this. Any individual, of either sex, is likely to contain
both
genes for making males
have
a certain quality,
and
genes for making females
prefer
that selfsame quality, whatever that quality might be.

So, the genes for male qualities, and the genes for making females prefer those qualities, will not be randomly shuffled around the population, but will tend to be shuffled around
together
. This ‘togetherness’, which goes under the daunting technical name of linkage disequilibrium, plays curious tricks with the equations of mathematical geneticists. It has strange and wonderful consequences, not the least of which in practice, if Fisher and Lande are right, is the explosive evolution of peacocks’ and widow birds’ tails, and a host of other organs of attraction. These consequences can only be proved mathematically, but it is possible to say in words what they are, and we can try to gain some flavour of the mathematical argument in nonmathematical language. We still need our mental running shoes, although actually climbing boots is a better analogy. Each step in the argument is simple enough, but there is a long series of steps up the mountain of understanding, and if you miss any of the earlier steps you unfortunately can’t take the later ones.

So far we have recognized the possibility of a complete range of female preferences, from females with a taste for long-tailed males through to females with the opposite taste, for short-tailed males. But if we actually did a poll of the females in a particular population, we would probably find that a majority of females shared the same general tastes in males. We can express the
range
of female tastes in the population in the same units - inches - as we express the range of male tail lengths. And we can express the
average
female preference in the same units of inches. It could turn out that the average female preference was exactly the same as the average male tail length, 3 inches in both cases. In this case female choice will not be an evolutionary force tending to change male tail length. Or it could turn out that the average female preference was for a tail rather longer than the average tail that actually exists, say 4 inches rather than 3. Leaving open, for the moment, why there might be such a discrepancy, just accept that there is one and ask the next obvious question. Why, if most females prefer males with 4-inch tails, do the majority of males actually have 3-inch tails? Why doesn’t the average tail length in the population shift to 4 inches under the influence of female sexual selection? How can there be a discrepancy of 1 inch between the average preferred tail length and the actual average tail length?

The answer is that female taste is not the only kind of selection that bears upon male tail length. Tails have an important job to perform in flight, and a tail that is too long or too short will decrease the efficiency of flight. Moreover, a long tail costs more energy to carry around, and more to make it in the first place. Males with 4-inch tails might well pull the female birds, but the price the males would pay is their less-efficient flight, greater energy costs and greater vulnerability to predators. We can express this by saying that there is a
utilitarian optimum
tail length, which is different from the sexually selected optimum: an ideal tail length from the point of view of ordinary useful criteria; a tail length that is ideal from all points of view apart from attracting females.

Should we expect that the actual average tail length of males, 3 inches in our hypothetical example, will be the same as the utilitarian optimum? No, we should expect the utilitarian optimum to be less, say 2 inches. The reason is that the actual average tail length of 3 inches is the result of a compromise between utilitarian selection tending to make tails shorter, and sexual selection tending to make them longer. We may surmise that, if there were no need to attract females, average tail length would shrink towards 2 inches. If there were no need to worry about flying efficiency and energy costs, average tail length would shoot out towards 4 inches. The actual average of 3 inches is a compromise.

We left on one side the question of
why
females might agree in preferring a tail that departed from the utilitarian optimum. At first sight the very idea seems silly. Fashion-conscious females, with a taste for tails that are longer than they should be on good design criteria, are going to have poorly designed, inefficient, clumsily flying sons. Any mutant female who happened to have an unfashionable taste for shorter-tailed males, in particular a mutant female whose taste in tails happened to coincide with the utilitarian optimum, would produce efficient sons, well designed for flying, who would surely outcompete the sons of her more fashion-conscious rivals. Ah, but here is the rub. It is implicit in my metaphor of ‘fashion’. The mutant female’s sons may be efficient flyers, but they are not seen as attractive by the majority of females in the population. They will attract only minority females, fashion-defying females, and minority females, by definition, are harder to find than majority females, for the simple reason that they are thinner on the ground. In a society where only one in six tnales mates at all and the fortunate males have large harems, pandering to the majority tastes of females will have enormous benefits, benefits that are well capable of outweighing the utilitarian costs in energy and’ flight efficiency.

But even so, the reader may complain, the whole argument is based upon an arbitrary assumption. Given that most females prefer nonutilitarian long tails, the reader will admit, everything else follows. But
why
did this majority female taste come about in the first place? Why didn’t the majority of females prefer tails that are
smaller
than the utilitarian optimum, or exactly the same length as the utilitarian optimum? Why shouldn’t fashion coincide with utility? The answer is that any of these things might have happened, and in many species it probably did. My hypothetical case of females preferring long tails was, indeed arbitrary. But
whatever
the majority female taste had happened to be, and no matter how arbitrary, there would have been a tendency for that majority to be maintained by selection or even, under some conditions, actually increased exaggerated. It is at this point in the argument that the lack of mathematical justification in my account becomes really noticeable. I could invite the reader simply to accept that the mathematical reasoning of Lande proves the point, and leave it at that. This might be the wisest course for me to pursue, but I shall have one try at explaining part of the idea in words.

The key to the argument lies in the point we established earlier about ‘linkage disequilibrium’, the ‘togetherness’ of genes for tails of a given length - any length - and corresponding genes for preferring tails of that selfsame length. We can think about the ‘togetherness factor’ as a measurable number. If the togetherness factor is very high, this means that knowledge about an individual’s genes for tail length enables us to predict, with great accuracy, his
her genes for preference, and vice versa. Conversely, if the togetherness factor is low, this means that knowledge about an individual’s genes in one of the two departments - preference or tail length - gives us only a slight hint about his
her genes in the other department.

The kind of thing that affects the magnitude of the togetherness factor is the strength of the females’ preference - how tolerant they are of what they see as imperfect males; how much of the variation in male tail length is governed by genes as opposed to environmental factors; and so on. If, as a result of all these effects, the togetherness factor - the tightness of binding of genes for tail length and genes for tail-length preference - is very strong, we can deduce the following consequence. Every time a male is chosen because of his long tail, not only are genes for long tails being chosen. At the same time, because of the ‘togetherness’ coupling, genes for
preferring
long tails are also being chosen. What this means is that genes that make females choose male tails of a particular length are, in effect,
choosing copies of themselves
. This is the essential ingredient of a self-reinforcing process: it has its own self-sustaining momentum. Evolution having started in a particular direction, this can, in itself, tend to make it persist in the same direction.