You scratch my back, I'll ride on yours
We 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.
The 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'.
If 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. Many 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'.
Once 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. From 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.
Now 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.
Obviously, in real life the bunching tendency will be limited by opposing pressures: otherwise all individuals would collapse in a writhing heap! But 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.
The selfish-herd model in itself has no place for cooperative interactions. There 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. Therefore 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.
In 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. Obviously, 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.
If you are not satisfied with this kin-selection idea, there are plenty of other theories to choose from. There 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.
The first I call the cave theory, from the Latin for 'beware', still used (pronounced 'kay-vee') by schoolboys to warn of approaching authority. This 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 thi
s 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.
The 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. What is he to do? He could simply fly off himself, without warning his colleagues. But 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. Whether 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. Charnov 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!
Superficially, 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. The cave theory and the 'never break ranks' theory are just two out of many ways of explaining why.
What 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. Smythe but, pushed to its logical conclusion, it bears the unmistakeable signature of A. Zahavi.
Zahavi'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. In 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. According 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.
The 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. Food is shared to such an extent that one may speak of a communal stomach. Information 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. Foreign 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.
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?'