The Selfish Gene (26 page)

Kamikaze behaviour and other forms of altruism and cooperation by workers are not astonishing once we accept the fact that they are sterile. The body of a normal animal is manipulated to ensure the survival of its genes both through bearing offspring and through caring for other individuals containing the same genes. Suicide in the interests of caring for other individuals is incompatible with future bearing of one's own offspring. Suicidal self-sacrifice therefore seldom evolves. But a worker bee never bears offspring of its own. All its efforts are directed to preserving its genes by caring for relatives other than its own offspring. The death of a single sterile worker bee is no more serious to its genes than is the shedding of a leaf in autumn to the genes of a tree.

There is a temptation to wax mystical about the social insects, but there is really no need for this. It is worth looking in some detail at how the selfish gene theory deals with them, and in particular at how it explains the evolutionary origin of that extraordinary phenomenon of worker sterility from which so much seems to follow.

A social insect colony is a huge family, usually all descended from the same mother. The workers, who seldom or never reproduce themselves, are often divided into a number of distinct castes, including small workers, large workers, soldiers, and highly specialized castes like the honey-pots. Reproductive females are called queens. Reproductive males are sometimes called drones or kings. In the more advanced societies, the reproductives never work at anything except procreation, but at this one task they are extremely good. They rely on the workers for their food and protection, and the workers are also responsible for looking after the brood. In some ant and termite species the queen has swollen into a gigantic egg factory, scarcely recognizable as an insect at all, hundreds of times the size of a worker and quite incapable of moving. She is constantly tended by workers who groom her, feed her, and transport her ceaseless flow of eggs to the communal nurseries. If such a monstrous queen ever has to move from the royal cell she rides in state on the backs of squadrons of toiling workers.

In Chapter 7 I introduced the distinction between bearing and caring. I said that mixed strategies, combining bearing and caring, would normally evolve. In Chapter 5 we saw that mixed evolutionarily stable strategies could be of two general types. Either each individual in the population could behave in a mixed way: thus individuals usually achieve a judicious mixture of bearing and caring; or, the population may be divided into two different types of individual: this was how we first pictured the balance between hawks and doves. Now it is theoretically possible for an evolutionarily stable balance between bearing and caring to be achieved in the latter kind of way: the population could be divided into bearers and carers. But this can only be evolutionarily stable if the carers are close kin to the individuals for whom they care, at least as close as they would be to their own offspring if they had any. Although it is theoretically possible for evolution to proceed in this direction, it seems to be only in the social insects that it has actually happened.

Social insect individuals are divided into two main classes, bearers and carers. The bearers are the reproductive males and females. The carers are the workers-infertile males and females in the termites, infertile females in all other social insects. Both types do their job more efficiently because they do not have to cope with the other. But from whose point of view is it efficient? The question which will be hurled at the Darwinian theory is the familiar cry: 'What's in it for the workers?'

Some people have answered 'Nothing.' They feel that the queen is having it all her own way, manipulating the workers by chemical means to her own selfish ends, making them care for her own teeming brood. This is a version of Alexander's 'parental manipulation' theory which we met in Chapter 8. The opposite idea is that the workers 'farm' the reproductives, manipulating them to increase their productivity in propagating replicas of the workers' genes. To be sure, the survival machines that the queen makes are not offspring to the workers, but they are close relatives nevertheless. It was Hamilton who brilliantly realized that, at least in the ants, bees, and wasps, the workers may actually be more closely related to the brood than the queen herself is! This led him, and later Trivers and Hare, on to one of the most spectacular triumphs of the selfish gene theory. The reasoning goes like this.

Insects of the group known as the Hymenoptera, including ants, bees, and wasps, have a very odd system of sex determination. Termites do not belong to this group and they do not share the same peculiarity. A hymenopteran nest typically has only one mature queen. She made one mating flight when young and stored up the sperms for the rest of her long life-ten years or even longer. She rations the sperms out to her eggs over the years, allowing the eggs to be fertilized as they pass out through her tubes. But not all the eggs are fertilized. The unfertilized ones develop into males. A male therefore has no father, and all the cells of his body contain just a single set of chromosomes (all obtained from his mother) instead of a double set (one from the father and one from the mother) as in ourselves. In terms of the analogy of Chapter 3, a male hymenopteran has only one copy of each 'volume' in each of his cells, instead of the usual two.

A female hymenopteran, on the other hand, is normal in that she does have a father, and she has the usual double set of chromosomes in each of her body cells. Whether a female develops into a worker or a queen depends not on her genes but on how she is brought up. That is to say, each female has a complete set of queen-making genes, and a complete set of worker-making genes (or, rather, sets of genes for making each specialized caste of worker, soldier, etc.). Which set of genes is 'turned on' depends on how the female is reared, in particular on the food she receives.

Although there are many complications, this is essentially how things are. We do not know why this extraordinary system of sexual reproduction evolved. No doubt there were good reasons, but for the moment we must just treat it as a curious fact about the Hymenoptera. Whatever the original reason for the oddity, it plays havoc with Chapter 6's neat rules for calculating relatedness. It means that the sperms of a single male, instead of all being different as they are in ourselves, are all exactly the same. A male has only a single set of genes in each of his body cells, not a double set Every sperm must therefore receive the full set of genes rather than a 50 per cent sample, and all sperms from a given male are therefore identical. Let us now try to calculate the relatedness between a mother and son. If a male is known to possess a gene A, what are the chances that his mother shares it? The answer must be 100 per cent, since the male had no father and obtained all his genes from his mother. But now suppose a queen is known to have the gene B. The chance that her son shares the gene is only 50 per cent, since he contains only half her genes. This sounds like a contradiction, but it is not. A male gets all his genes from his mother, but a mother only gives half her genes to her son. The solution to the apparent paradox lies in the fact that a male has only half the usual number of genes. There is no point in puzzling over whether the 'true' index of relatedness is 1/2 or 1. The index is only a man-made measure, and if it leads to difficulties in particular cases, we may have to abandon it and go back to first principles. From the point of view of a gene A in the body of a queen, the chance that the gene is shared by a son is 1/2, just as it is for a daughter. From a queen's point of view therefore, her offspring, of either sex, are as closely related to her as human children are to their mother.

Things start to get intriguing when we come to sisters. Full sisters not only share the same father: the two sperms that conceived them were identical in every gene. The sisters are therefore equivalent to identical twins as far as their paternal genes are concerned. If one female has a gene A, she must have got it from either her father or her mother. If she got it from her mother then there is a 50 per cent chance that her sister shares it. But if she got it from her father, the chances are 100 per cent that her sister shares it. Therefore the relatedness between hymenopteran full sisters is not 1/2 as it would be for normal sexual animals, but 3/4.

It follows that a hymenopteran female is more closely related to her full sisters than she is to her offspring of either sex. As Hamilton realized (though he did not put it in quite the same way) this might well predispose a female to farm her own mother as an efficient sister-making machine. A gene for vicariously making sisters replicates itself more rapidly than a gene for making offspring directly. Hence worker sterility evolved. It is presumably no accident that true sociality, with worker sterility, seems to have evolved no fewer than eleven times independently in the Hymenoptera and only once in the whole of the rest of the animal kingdom, namely in the termites.

However, there is a catch. If the workers are successfully to farm their mother as a sister-producing machine, they must somehow curb her natural tendency to give them an equal number of little brothers as well. From the point of view of a worker, the chance of any one brother containing a particular one of her genes is only 1/4. Therefore, if the queen were allowed to produce male and female reproductive offspring in equal proportions, the farm would not show a profit as far as the workers are concerned. They would not be maximizing the propagation of their precious genes.

Trivers
and Hare realized that the workers must try to bias the sex ratio in favour of females. They took the Fisher calculations on optimal sex ratios (which we looked at in the previous chapter) and re-worked them for the special case of the Hymenoptera. It turned out that the stable ratio of investment for a mother is, as usual, 1:1. But the stable ratio for a sister is 3:1 in favour of sisters rather than brothers. If you are a hymenopteran female, the most efficient way for you to propagate your genes is to refrain from breeding yourself, and to make your mother provide you with reproductive sisters and brothers in the ratio 3:1. But if you must have offspring of your own, you can benefit your genes best by having reproductive sons and daughters in equal proportions.

As we have seen, the difference between queens and workers is not a genetic one. As far as her genes are concerned, an embryo female might be destined to become either a worker, who 'wants' a 3 :1 sex ratio, or a queen, who 'wants' a 1:1 ratio. So what does this 'wanting' mean? It means that a gene that finds itself in a queen's body can propagate itself best if that body invests equally in reproductive sons and daughters. But the same gene finding itself in a worker's body can propagate itself best by making the mother of that body have more daughters than sons. There is no real paradox here. A gene must take best advantage of the levers of power that happen to be at its disposal. If it finds itself in a position to influence the development of a body that is destined to turn into a queen, its optimal strategy to exploit that control is one thing. If it finds itself in a position to influence the way a worker's body develops, its optimal strategy to exploit that power is different.

This means there is a conflict of interests down on the farm. The queen is 'trying' to invest equally in males and females. The workers are trying to shift the ratio of reproductives in the direction of three females to every one male. If we are right to picture the workers as the farmers and the queen as their brood mare, presumably the workers will be successful in achieving their 3 :1 ratio. If not, if the queen really lives up to her name and the workers are her slaves and the obedient tenders of the royal nurseries, then we should expect the 1:1 ratio which the queen 'prefers' to prevail. Who wins in this special case of a battle of the generations? This is a matter that can be put to the test and that is what Trivers and Hare did, using a large number of species of ants.

The sex ratio that is of interest is the ratio of male to female reproductives. These are the large winged forms which emerge from the ants' nest in periodic bursts for mating flights, after which the young queens may try to found new colonies. It is these winged forms that have to be counted to obtain an estimate of the sex ratio. Now the male and female reproductives are, in many species, very unequal in size. This complicates things since, as we saw in the previous chapter, the Fisher calculations about optimal sex ratio strictly apply, not to numbers of males and females, but to quantity of investment in males and females. Trivers and Hare made allowance for this by weighing them. They took 20 species of ant and estimated the sex ratio in terms of investment in reproductives. They found a rather convincingly close fit to the 3:1 female to male ratio predicted by the theory that the workers are running the show for their own benefit. It seems then that in the ants studied, the conflict of interests is 'won' by the workers. This is not too surprising since worker bodies, being the guardians of the nurseries, have more power in practical terms than queen bodies. Genes trying to manipulate the world through queen bodies are outmanoeuvred by genes manipulating the world through worker bodies. It is interesting to look around for some special circumstances in which we might expect queens to have more practical power than workers. Trivers and Hare realized that there was just such a circumstance which could be used as a critical test of the theory.

This arises from the fact that there are some species of ant that take slaves. The workers of a slave-making species either do no ordinary work at all or are rather bad at it. What they are good at is going on slaving raids. True warfare in which large rival armies fight to the death is known only in man and in social insects. In many species of ants the specialized caste of workers known as soldiers have formidable fighting jaws, and devote their time to fighting for the colony against other ant armies. Slaving raids are just a particular kind of war effort. The slavers mount an attack on a nest of ants belonging to a different species, attempt to kill the defending workers or soldiers, and carry off the unhatched young. These young ones hatch out in the nest of their captors. They do not 'realize' that they are slaves and they set to work following their built-in nervous programs, doing all the duties that they would normally perform in their own nest. The slave-making workers or soldiers go on further slaving expeditions while the slaves stay at home and get on with the everyday business of running an ants' nest, cleaning, foraging, and caring for the brood.