commonplace book redux

In frogs, for instance, neither sex has a penis. Perhaps, then, the words male and female have no general meaning. They are, after all, only words, and if we do not find them helpful for describing frogs, we are quite at liberty to abandon them. We could arbitrarily divide frogs into Sex I and Sex 2 if we wished. However, there is one fundamental feature of the sexes which can be used to label males as males, and females as females, throughout animals and plants. This is that the sex cells or ‘gametes’ of males are much smaller and more numerous than the gametes of females. This is true whether we are dealing with animals or plants. One group of individuals has large sex cells, and it is convenient to use the word female for them. The other group, which it is convenient to call male, has small sex cells. The difference is especially pronounced in reptiles and in birds, where a single egg cell is big enough and nutritious enough to feed a developing baby for several weeks. Even in humans, where the egg is microscopic, it is still many times larger than the sperm. As we shall see, it is possible to interpret all the other differences between the sexes as stemming from this one basic difference.

In certain primitive organisms, for instance some fungi, maleness and femaleness do not occur, although sexual reproduction of a kind does. In the system known as isogamy the individuals are not distinguishable into two sexes. Anybody can mate with anybody else. There are not two different sorts of gametes—sperms and eggs—but all sex cells are the same, called isogametes. New individuals are formed by the fusion of two isogametes, each produced by meiotic division. If we have three isogametes, A, B, and C, A could fuse with B or C, B could fuse with A or C. The same is never true of normal sexual systems. If A is a sperm and it can fuse with B or C, then B and C must be eggs and B cannot fuse with C.

When two isogametes fuse, both contribute equal numbers of genes to the new individual, and they also contribute equal amounts of food reserves. Sperms and eggs too contribute equal numbers of genes, but eggs contribute far more in the way of food reserves: indeed, sperms make no contribution at all and are simply concerned with transporting their genes as fast as possible to an egg. At the moment of conception, therefore, the father has invested less than his fair share (i.e. 50 per cent) of resources in the offspring. Since each sperm is so tiny, a male can afford to make many millions of them every day. This means he is potentially able to beget a very large number of children in a very short period of time, using different females. This is only possible because each new embryo is endowed with adequate food by the mother in each case. This therefore places a limit on the number of children a female can have, but the number of children a male can have is virtually unlimited. Female exploitation begins here.

Parker and others showed how this asymmetry might have evolved from an originally isogamous state of affairs. In the days when all sex cells were interchangeable and of roughly the same size, there would have been some that just happened to be slightly bigger than others. In some respects a big isogamete would have an advantage over an average-sized one, because it would get its embryo off to a good start by giving it a large initial food supply. There might therefore have been an evolutionary trend towards larger gametes. But there was a catch. The evolution of isogametes that were larger than was strictly necessary would have opened the door to selfish exploitation. Individuals who produced smaller than average gametes could cash in, provided they could ensure that their small gametes fused with extra-big ones. This could be achieved by making the small ones more mobile, and able to seek out large ones actively. The advantage to an individual of producing small, rapidly moving gametes would be that he could afford to make a larger number of gametes, and therefore could potentially have more children. Natural selection favoured the production of sex cells that were small and that actively sought out big ones to fuse with. So we can think of two divergent sexual ‘strategies’ evolving. There was the large-investment or ‘honest’ strategy. This automatically opened the way for a small-investment exploitative strategy. Once the divergence between the two strategies had started, it would have continued in runaway fashion. Medium-sized intermediates would have been penalized, because they did not enjoy the advantages of either of the two more extreme strategies. The exploiters would have evolved smaller and smaller size, and faster mobility. The honest ones would have evolved larger and larger size, to compensate for the ever-smaller investment contributed by the exploiters, and they became immobile because they would always be actively chased by the exploiters anyway. Each honest one would ‘prefer’ to fuse with another honest one. But the selection pressure to lock out exploiters would have been weaker than the pressure on exploiters to duck under the barrier: the exploiters had more to lose, and they therefore won the evolutionary battle. The honest ones became eggs, and the exploiters became sperms.

. . . the number of children a male can have is virtually unlimited. Female exploitation begins here.

It now seems misleading to emphasize the disparity between sperm and egg size as the basis of sex roles. Even if one sperm is small and cheap, it is far from cheap to make millions of sperms and successfully inject them into a female against all the competition. I now prefer the following approach to explaining the fundamental asymmetry between males and females.

Suppose we start with two sexes that have none of the particular attributes of males and females. Call them by the neutral names A and B. All we need specify is that every mating has to be between an A and a B. Now, any animal, whether an A or a B, faces a trade-off. Time and effort devoted to fighting with rivals cannot be spent on rearing existing offspring, and vice versa. Any animal can be expected to balance its effort between these rival claims. The point I am about to come to is that the A’s may settle at a different balance from the B’s and that, once they do, there is likely to be an escalating disparity between them.

To see this, suppose that the two sexes, the A’s and the B’s, differ from one another, right from the start, in whether they can most influence their success by investing in children or by investing in lighting (I’ll use ‘fighting’ to stand for all kinds of direct competition within one sex). Initially the difference between the sexes can be very slight, since my point will be that there is an inherent tendency for it to grow. Say the A’s start out with fighting making a greater contribution to their reproductive success than parental behaviour does; the B’s, on the other hand, start out with parental behaviour contributing slightly more than fighting to variation in their reproductive success. This means, for example, that although an A of course benefits from parental care, the difference between a successful carer and an unsuccessful carer among the A’s is smaller than the difference between a successful fighter and an unsuccessful fighter among the A’s. Among the B’s, just the reverse is true. So, for a given amount of effort, an A can do itself good by fighting, whereas a B is more likely to do itself good by shifting its effort away from fighting and towards parental care.

In subsequent generations, therefore, the A’s will fight a bit more than their parents, the B’s will fight a bit less and care a bit more than their parents. Now the difference between the best A and the worst A with respect to fighting will be even greater, the difference between the best A and the worst A with respect to caring will be even less. Therefore an A has even more to gain by putting its effort into fighting, even less to gain by putting its effort into caring. Exactly the opposite will be true of the B’s as the generations go by. The key idea here is that a small initial difference between the sexes can be self-enhancing: selection can start with an initial, slight difference and make it grow larger and larger, until the A’s become what we now call males, the B’s what we now call females. The initial difference can be small enough to arise at random. After all, the starting conditions of the two sexes are unlikely to be exactly identical.

As you will notice, this is rather like the theory, originating with Parker, Baker, and Smith and discussed on page 142, of the early separation of primitive gametes into sperms and eggs. The argument just given is more general. The separation into sperms and eggs is only one aspect of a more basic separation of sexual roles. Instead of treating the sperm-egg separation as primary, and tracing all the characteristic attributes of males and females back to it, we now have an argument that explains the sperm-egg separation and other aspects all in the same way. We have to assume only that there are two sexes who have to mate with each other; we need know nothing more about those sexes. Starting from this minimal assumption, we positively expect that, however equal the two sexes may be at the start, they will diverge into two sexes specializing in opposite and complementary reproductive techniques. The separation between sperms and eggs is a symptom of this more general separation, not the cause of it.

Richard Dawkins, The Selfish Gene, 30th Anniversary Edition, 2006

Footnotes (1989 edition) are doubly indented.