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, usin
g 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.
The slaves are, of course, blissfully ignorant of the fact that they are unrelated to the queen and to the brood that they are tending. Unwittingly they are rearing new platoons of slave-makers. No doubt natural selection, acting on the genes of the slave species, tends to favour anti-slavery adaptations. However, these are evidently not fully effective because slavery is a wide spread phenomenon.
The consequence of slavery that is interesting from our present point of view is this. The queen of the slave-making species is now in a position to bend the sex ratio in the direction she 'prefers'. This is because her own true-born children, the slavers, no longer hold the practical power in the nurseries. This power is now held by the slaves. The slaves 'think' they are looking after their own siblings and they are presumably doing whatever would be appropriate in their own nests to achieve their desired 3:1 bias in favour of sisters. But the queen of the slave-making species is able to get away with countermeasures and there is no selection operating on the slaves to neutralize these counter-measures, since the slaves are totally unrelated to the brood.
For example, suppose that in any ant species, queens 'attempt' to disguise male eggs by making them smell like female ones. Natural selection will normally favour any tendency by workers to 'see through' the disguise. We may picture an evolutionary battle in which queens continually 'change the code', and workers 'break the code'. The war will be won by whoever manages to get more of her genes into the next generation, via the bodies of the reproductives. This will normally be the workers, as we have seen. But when the queen of a slave-making species changes the code, the slave workers cannot evolve any ability to break the code. This is because any gene in a slave worker 'for breaking the code' is not represented in the body of any reproductive individual, and so is not passed on. The reproductives all belong to the slave-making species, and are kin to the queen but not to the slaves. If the genes of the slaves find their way into any reproductives at all, it will be into the reproductives that emerge from the original nest from which they were kidnapped. The slave workers will, if anything, be busy breaking the wrong code! Therefore, queens of a slave-making species can get away with changing their code freely, without there being any danger that genes for breaking the code will be propagated into the next generation.
The upshot of this involved argument is that we should expect in slave-making species that the ratio of investment in reproductives of the two sexes should approach 1:1 rather than 3:1. For once, the queen will have it all her own way. This is just what Trivers and Hare found, although they only looked at two slave-making species.
I must stress that I have told the story in an idealized way. Real life is not so neat and tidy. For instance, the most familiar social insect species of all, the honey bee, seems to do entirely the 'wrong' thing. There is a large surplus of investment in males over queens- something that does not appear to make sense from either the workers' or the mother queen's point of view. Hamilton has offered a possible solution to this puzzle. He points out that when a queen bee leaves the hive she goes with a large swarm of attendant workers, who help her to start a new colony. These workers are lost to the parent hive, and the cost of making them must be reckoned as part of the cost of reproduction: for every queen who leaves, many extra workers have to be made. Investment in these extra workers should be counted as part of the investment in reproductive females. The extra workers should be weighed in the balance against the males when the sex ratio is computed. So this was not a serious difficulty for the theory after all.
A more awkward spanner in the elegant works of the theory is the fact that, in some species, the young queen on her mating flight mates with several males instead of one. This means that the average relatedness among her daughters is less than 3/4, and may even approach 1/4 in extreme cases. It is tempting, though probably not very logical, to regard this as a cunning blow struck by queens against workers! Incidentally, this might seem to suggest that workers should chaperone a queen on her mating flight, to prevent her from mating more than once. But this would in no way help the workers' own genes-only the genes of the coming generation of workers. There is no trade-union spirit among the workers as a class. All that each one of them 'cares' about is her own genes. A worker might have 'liked' to have chaperoned her own mother, but she lacked the opportunity, not having been conceived in those days. A young queen on her mating flight is the sister of the present generation of workers, not the mother. Therefore they are on her side rather than on the side of the next generation of workers, who are merely their nieces. My head is now spinning, and it is high time to bring this topic to a close.
I have used the analogy of farming for what hymenopteran workers do to their mothers. The farm is a gene farm. The workers use their mother as a more efficient manufacturer of copies of their own genes than they would be themselves. The genes come off the production line in packages called reproductive individuals. This farming analogy should not be confused with a quite different sense in which the social insects may be said to farm. Social insects discovered, as man did long after, that settled cultivation of food can be more efficient than hunting and gathering.
For example, several species of ants in the New World, and, quite independently, termites in Africa, cultivate 'fungus gardens'. The best known are the so-called parasol ants of South America. These are immensely successful. Single colonies with more than two million individuals have been found. Their nests consist of huge spreading underground complexes of
passages and galleries going down to a depth of ten feet or more, made by the excavation of as much as 40 tons of soil. The underground chambers contain the fungus gardens. The ants deliberately sow fungus of a particular species in special compost beds which they prepare by chewing leaves into fragments. Instead of foraging directly for their own food, the workers forage for leaves to make compost. The 'appetite' of a colony of parasol ants for leaves is gargantuan. This makes them a major economic pest, but the leaves are not food for themselves but food for their fungi. The ants eventually harvest and eat the fungi and feed them to their brood. The fungi are more efficient at breaking down leaf material than the ants' own stomachs would be, which is how the ants benefit by the arrangement. It is possible that the fungi benefit too, even though they are cropped: the ants propagate them more efficiently than their own spore dispersal mechanism might achieve. Furthermore, the ants 'weed' the fungus gardens, keeping them clear of alien species of fungi. By removing competition, this may benefit the ants' own domestic fungi. A kind of relationship of mutual altruism could be said to exist between ants and fungi. It is remarkable that a very similar system of fungus farming has evolved independently, among the quite unrelated termites.
Ants have their own domestic animals as well as their crop plants. Aphids-greenfly and similar bugs-are highly specialized for sucking the juice out of plants. They pump the sap up out of the plants' veins more efficiently than they subsequently digest it. The result is that they excrete a liquid that has had only some of its nutritious value extracted. Droplets of sugar-rich 'honeydew' pass out of the back end at a great rate, in some cases more than the insect's own body-weight every hour. The honeydew normally rains down on to the ground-it may well have been the providential food known as 'manna' in the Old Testament. But ants of several species intercept it as soon as it leaves the bug. The ants 'milk' the aphids by stroking their hind-quarters with their feelers and legs. Aphids respond to this, in some cases apparently holding back their droplets until an ant strokes them, and even withdrawing a droplet if an ant is not ready to accept it. It has been suggested that some aphids have evolved a backside that looks and feels like an ant's face, the better to attract ants. What the aphids have to gain from the relationship is apparently protection from their natural enemies. Like our own dairy cattle they lead a sheltered life, and aphid species that are much cultivated by ants have lost their normal defensive mechanisms. In some cases ants care for the aphid eggs inside their own underground nests, feed the young aphids, and finally, when they are grown, gently carry them up to the protected grazing grounds.