1We have considered parental, sexual, and aggressive interactions between survival machines belonging to the same species. There are striking aspects of animal interactions which do not seem to be obviously covered by any of these headings. One of these is the propensity that so many animals have for living in groups. Birds flock, insects swarm, fish and whales school, plains-dwelling mammals herd together or hunt in packs. These aggregations usually consist of members of a single species only, but there are exceptions. Zebras often herd together with gnus, and mixed-species flocks of birds are sometimes seen.

2The suggested benefits that a selfish individual can wrest from living in a group constitute rather a miscellaneous list. I am not going to trot out the catalogue, but will mention just a few suggestions. In the course of this I shall return to the remaining examples of apparently altruistic behaviour that I gave in Chapter 1, and which I promised to explain. This will lead into a consideration of the social insects, without which no account of animal altruism would be complete. Finally in this rather miscellaneous chapter, I shall mention the important idea of reciprocal altruism, the principle of 'You scratch my back, I'll scratch yours'.

3If animals live together in groups their genes must get more benefit out of the association than they put in. A pack of hyenas can catch prey so much larger than a lone hyena can bring down that it pays each selfish individual to hunt in a pack, even though this involves sharing food. It is probably for similar reasons that some spiders cooperate in building a huge communal web. Emperor penguins conserve heat by huddling together. Each one gains by presenting a smaller surface area to the elements than he would on his own. A fish who swims obliquely behind another fish may gain a hydrodynamic advantage from the turbulence produced by the fish in front. This could be partly why fish school. A related trick concerned with air turbulence is known to racing cyclists, and it may account for the V- formation of flying birds. There is probably competition to avoid the disadvantageous position at the head of the flock. Possibly the birds take turns as unwilling leader-a form of the delayed reciprocal- altruism to be discussed at the end of the chapter.

4Many of the suggested benefits of group living have been concerned with avoiding being eaten by predators. An elegant formulation of such a theory was given by W. D. Hamilton, in a paper called Geometry for the selfish herd. Lest this lead to misunderstanding, I must stress that by 'selfish herd' he meant 'herd of selfish individuals'.

5Once again we start with a simple 'model' which, though abstract, helps us to understand the real world. Suppose a species of animal is hunted by a predator that always tends to attack the nearest prey individual.

6From the predator's point of view this is a reasonable strategy, since it tends to cut down energy expenditure. From the prey's point of view it has an interesting consequence. It means that each prey individual will constantly try to avoid being the nearest to a predator. If the prey can detect the predator at a distance, it will simply run away. But if the predator is apt to turn up suddenly without warning, say it lurks concealed in long grass, then each prey individual can still take steps to minimize its chance of being the nearest to a predator. We can picture each prey individual as being surrounded by a 'domain of danger'. This is defined as that area of ground in which any point is nearer to that individual than it is to any other individual. For instance, if the prey individuals march spaced out in a regular geometric formation, the domain of danger round each one (unless he is on the edge) might be roughly hexagonal in shape. If a predator happens to be lurking in the hexagonal domain of danger surrounding individual A, then individual A is likely to be eaten. Individuals on the edge of the herd are especially vulnerable, since their domain of danger is not a relatively small hexagon, but includes a wide area on the open side.

7Now clearly a sensible individual will try to keep his domain of danger as small as possible. In particular, he will try to avoid being on the edge of the herd. If he finds himself on the edge he will take immediate steps to move towards the centre. Unfortunately somebody has to be on the edge, but as far as each individual is concerned it is not going to be him! There will be a ceaseless migration in from the edges of an aggregation towards the centre. If the herd was previously loose and straggling, it will soon become tightly bunched as a result of the inward migration. Even if we start our model with no tendency towards aggregation at all, and the prey animals start by being randomly dispersed, the selfish urge of each individual will be to reduce his domain of danger by trying to position himself in a gap between other individuals. This will quickly lead to the formation of aggregations which will become ever more densely bunched.

8Obviously, in real life the bunching tendency will be limited by opposing pressures: otherwise all individuals would collapse in a writhing heap!

9But still, the model is interesting as it shows us that even very simple assumptions can predict aggregation. Other, more elaborate models have been proposed. The fact that they are more realistic does not detract from the value of the simpler Hamilton model in helping us to think about the problem of animal aggregation.

10The selfish-herd model in itself has no place for cooperative interactions.

11There is no altruism here, only selfish exploitation by each individual of every other individual. But in real life there are cases where individuals seem to take active steps to preserve fellow members of the group from predators. Bird alarm calls spring to mind. These certainly function as alarm signals in that they cause individuals who hear them to take immediate evasive action. There is no suggestion that the caller is 'trying to draw the predator's fire' away from his colleagues. He is simply informing them of the predator's existence-warning them. Nevertheless the act of calling seems, at least at first sight, to be altruistic, because it has the effect of calling the predator's attention to the caller. We can infer this indirectly from a fact which was noticed by P. R. Marler. The physical characteristics of the calls seem to be ideally shaped to be difficult to locate. If an acoustic engineer were asked to design a sound that a predator would find it hard to approach, he would produce something very like the real alarm calls of many small songbirds. Now in nature this shaping of the calls must have been produced by natural selection, and we know what that means. It means that large numbers of individuals have died because their alarm calls were not quite perfect.

12Therefore there seems to be danger attached to giving alarm calls. The selfish gene theory has to come up with a convincing advantage of giving alarm calls which is big enough to counteract this danger.

13In fact this is not very difficult. Bird alarm calls have been held up so many times as 'awkward' for the Darwinian theory that it has become a kind of sport to dream up explanations for them. As a result, we now have so many good explanations that it is hard to remember what all the fuss was about.

14Obviously, if there is a chance that the flock contains some close relatives, a gene for giving an alarm call can prosper in the gene pool because it has a good chance of being in the bodies of some of the individuals saved. This is true, even if the caller pays dearly for his altruism by attracting the predator's attention to himself.

15If you are not satisfied with this kin-selection idea, there are plenty of other theories to choose from.

16There are many ways in which the caller could gain selfish benefit from warning his fellows. Trivers reels off five good ideas, but I find the following two of my own rather more convincing.

17The first I call the cave theory, from the Latin for 'beware', still used (pronounced 'kay-vee') by schoolboys to warn of approaching authority.

18This theory is suitable for camouflaged birds that crouch frozen in the undergrowth when danger threatens. Suppose a flock of such birds is feeding in a field. A hawk flies past in the distance. He has not yet seen the flock and he is not flying directly towards them, but there is a danger that his keen eyes will spot them at any moment and he will race into the attack. Suppose one member of the flock sees the hawk, but the rest have not yet done so. This one sharp-eyed individual could immediately freeze and crouch in the grass. But this would do him little good, because his companions are still walking around conspicuously and noisily. Any one of them could attract the hawk's attention and then the whole flock is in peril. From a purely selfish point of view the best policy for the individual who spots the hawk first is to hiss a quick warning to his companions, and so shut them up and reduce the chance that they will inadvertently summon the hawk into his own vicinity.

19The other theory I want to mention may be called the 'never break ranks' theory. This one is suitable for species of birds that fly off when a predator approaches, perhaps up into a tree. Once again, imagine that one individual in a flock of feeding birds has spotted a predator.

20What is he to do? He could simply fly off himself, without warning his colleagues.

21But now he would be a bird on his own, no longer part of a relatively anonymous flock, but an odd man out. Hawks are actually known to go for odd pigeons out, but even if this were not so there are plenty of theoretical reasons for thinking that breaking ranks might be a suicidal policy. Even if his companions eventually follow him, the individual who first flies up off the ground temporarily increases his domain of danger.

22Whether Hamilton's particular theory is right or wrong, there must be some important advantage in living in flocks, otherwise the birds would not do it. Whatever that advantage may be, the individual who leaves the flock ahead of the others will, at least in part, forfeit that advantage. If he must not break ranks, then, what is the observant bird to do? Perhaps he should just carry on as if nothing had happened and rely on the protection afforded by his membership of the flock. But this too carries grave risks. He is still out in the open, highly vulnerable. He would be much safer up in a tree. The best policy is indeed to fly up into a tree, but to make sure everybody else does too. That way, he will not become an odd man out and he will not forfeit the advantages of being part of a crowd, but he will gain the advantage of flying off into cover. Once again, uttering a warning call is seen to have a purely selfish advantage. E. L.

23Charnov and J. R. Krebs have proposed a similar theory in which they go so far as to use the word 'manipulation' to describe what the calling bird does to the rest of his flock. We have come a long way from pure, disinterested altruism!

24Superficially, these theories may seem incompatible with the statement that the individual who gives the alarm call endangers himself. Really there is no incompatibility. He would endanger himself even more by not calling. Some individuals have died because they gave alarm calls, especially the ones whose calls were easy to locate. Other individuals have died because they did not give alarm calls.

25The cave theory and the

26'never break ranks' theory are just two out of many ways of explaining why.

27What of the stotting Thomson's gazelle, which I mentioned in Chapter 1, and whose apparently suicidal altruism moved Ardrey to state categorically that it could be explained only by group selection? Here the selfish gene theory has a more exacting challenge. Alarm calls in birds do work, but they are clearly designed to be as inconspicuous and discreet as possible. Not so the stotting high- jumps. They are ostentatious to the point of downright provocation. The gazelles look as if they are deliberately inviting the predator's attention, almost as if they are teasing the predator. This observation has led to a delightfully daring theory. The theory was originally foreshadowed by N.

28Smythe but, pushed to its logical conclusion, it bears the unmistakeable signature of A. Zahavi.

29Zahavi's theory can be put like this. The crucial bit of lateral thinking is the idea that stotting, far from being a signal to the other gazelles, is really aimed at the predators. It is noticed by the other gazelles and it affects their behaviour, but this is incidental, for it is primarily selected as a signal to the predator. Translated roughly into English it means: 'Look how high I can jump, I am obviously such a fit and healthy gazelle, you can't catch me, you would be much wiser to try and catch my neighbour who is not jumping so high!' In less anthropomorphic terms, genes for jumping high and ostentatiously are unlikely to be eaten by predators because predators tend to choose prey who look easy to catch.

30In particular, many mammal predators are known to go for the old and the unhealthy. An individual who jumps high is advertising, in an exaggerated way, the fact that he is neither old nor unhealthy.

31According to this theory, the display is far from altruistic. If anything it is selfish, since its object is to persuade the predator to chase somebody else. In a way there is a competition to see who can jump the highest, the loser being the one chosen by the predator.

32The other example that I said I would return to is the case of the kamikaze bees, who sting honey- raiders but commit almost certain suicide in the process. The honey bee is just one example of a highly social insect. Others are wasps, ants, and termites or 'white ants'. I want to discuss social insects generally, not just suicidal bees. The exploits of the social insects are legendary, in particular their astonishing feats of cooperation and apparent altruism. Suicidal stinging missions typify their prodigies of self-abnegation. In the 'honey-pot' ants there is a caste of workers with grotesquely swollen, food-packed abdomens, whose sole function in life is to hang motionless from the ceiling like bloated light-bulbs, being used as food stores by the other workers. In the human sense they do not live as individuals at all; their individuality is subjugated, apparently to the welfare of the community. A society of ants, bees, or termites achieves a kind of individuality at a higher level.

33Food is shared to such an extent that one may speak of a communal stomach.

34Information is shared so efficiently by chemical signals and by the famous 'dance' of the bees that the community behaves almost as if it were a unit with a nervous system and sense organs of its own.

35Foreign intruders are recognized and repelled with something of the selectivity of a body's immune reaction system. The rather high temperature inside a beehive is regulated nearly as precisely as that of the human body, even though an individual bee is not a 'warm blooded' animal. Finally and most importantly, the analogy extends to reproduction. The majority of individuals in a social insect colony are sterile workers. The 'germ line'-the line of immortal gene continuity-flows through the bodies of a minority of individuals, the reproductives. These are the analogues of our own reproductive cells in our testes and ovaries. The sterile workers are the analogy of our liver, muscle, and nerve cells.

36Kamikaze behaviour and other forms of altruism and cooperation by workers are not astonishing once we accept the fact that they are sterile.

37The 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.

38The 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.

39There 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.

40A 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.

41Reproductive females are called queens. Reproductive males are sometimes called drones or kings.

42In 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.

43In 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.

44Social 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.

45Insects 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.

46A 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.

47Although there are many complications, this is essentially how things are.

48We 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.

49Whatever 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.

50But 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.

51Things 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.

52It 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.

53Hence 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.

54However, 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.

55From 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.

56They would not be maximizing the propagation of their precious genes.

57Trivers 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.

58As 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.

59There 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.

60This 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'

61to prevail. Who wins in this special case of a battle of the generations?

62This 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.

63The 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.

64Trivers 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.

65This 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.

66Slaving 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.

67The slaves are, of course, blissfully ignorant of the fact that they are unrelated to the queen and to the brood that they are tending.

68Unwittingly 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.

69The 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.

70This 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.

71For 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'

72the 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.

73The 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.

74I 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.

75A 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.

76A young queen on her mating flight is the sister of the present generation of workers, not the mother.

77Therefore they are on her side rather than on the side of the next generation of workers, who are merely their nieces.

78My head is now spinning, and it is high time to bring this topic to a close.

79I 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.

80For 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.

81The 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.

82Instead of foraging directly for their own food, the workers forage for leaves to make compost.

83The '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.

84Furthermore, 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.

85Ants have their own domestic animals as well as their crop plants.

86Aphids-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.

87Aphids 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.

88A relationship of mutual benefit between members of different species is called mutualism or symbiosis. Members of different species often have much to offer each other because they can bring different 'skills' to the partnership. This kind of fundamental asymmetry can lead to evolutionarily stable strategies of mutual cooperation. Aphids have the right sort of mouthparts for pumping up plant sap, but such sucking mouthparts are no good for self-defence. Ants are no good at sucking sap from plants, but they are good at fighting. Ant genes for cultivating and protecting aphids have been favoured in ant gene-pools. Aphid genes for cooperating with the ants have been favoured in aphid gene-pools.

89Symbiotic relationships of mutual benefit are common among animals and plants. A lichen appears superficially to be an individual plant like any other. But it is really an intimate symbiotic union between a fungus and a green alga. Neither partner could live without the other. If their union had become just a bit more intimate we would no longer have been able to tell that a lichen was a double organism at all. Perhaps then there are other double or multiple organisms which we have not recognized as such. Perhaps even we ourselves?

90Within each one of our cells there are numerous tiny bodies called mitochondria. The mitochondria are chemical factories, responsible for providing most of the energy we need. If we lost our mitochondria we would be dead within seconds. Recently it has been plausibly argued that mitochondria are, in origin, symbiotic bacteria who joined forces with our type of cell very early in evolution. Similar suggestions have been made for other small bodies within our cells. This is one of those revolutionary ideas which it takes time to get used to, but it is an idea whose time has come. I speculate that we shall come to accept the more radical idea that each one of our genes is a symbiotic unit. We are gigantic colonies of symbiotic genes. One cannot really speak of 'evidence' for this idea, but, as I tried to suggest in earlier chapters, it is really inherent in the very way we think about how genes work in sexual species. The other side of this coin is that viruses may be genes who have broken loose from 'colonies' such as ourselves. Viruses consist of pure DNA (or a related self- replicating molecule) surrounded by a protein jacket. They are all parasitic. The suggestion is that they have evolved from 'rebel' genes who escaped, and now travel from body to body directly through the air, rather than via the more conventional vehicles-sperms and eggs. If this is true, we might just as well regard ourselves as colonies of viruses! Some of them cooperate symbiotically, and travel from body to body in sperms and eggs. These are the conventional 'genes'.