Presumably the most important kind of non-arbitrary asymmetry is in size and general fighting ability. Large size is not necessarily always the most important quality needed to win fights, but it is probably one of them. If the larger of two fighters always wins, and if each individual knows for certain whether he is larger or smaller than his opponent, only one strategy makes any sense: 'If your opponent is larger than you, run away. Pick fights with people smaller than you are.' Things are a bit more complicated if the importance of size is less certain. If large size confers only a slight advantage, the strategy I have just mentioned is still stable. But if the risk of injury is serious there may also be a second, 'paradoxical strategy'. This is: 'Pick fights with people larger than you are and run away from people smaller than you are'! It is obvious why this is called paradoxical. It seems completely counter to common sense. The reason it can be stable is this. In a population consisting entirely of paradoxical strategists, nobody ever gets hurt. This is because in every contest one of the participants, the larger, always runs away. A mutant of average size who plays the 'sensible' strategy of picking on smaller opponents is involved in a seriously escalated fight with half the people he meets. This is because, if he meets somebody smaller than him, he attacks; the smaller individual fights back fiercely, because he is playing paradoxical; although the sensible strategist is more likely to win than the paradoxical one, he still runs a substantial risk of losing and of being seriously injured. Since the majority of the population are paradoxical, a sensible strategist is more likely to be injured than any single paradoxical strategist.
Even though a paradoxical strategy can be stable, it is probably only of academic interest. Paradoxical fighters will only have a higher average pay-off if they very heavily out-number sensible ones. It is hard to imagine how this state of affairs could ever arise in the first place. Even if it did, the ratio of sensibles to paradoxicals in the population only has to drift a little way towards the sensible side before reaching the 'zone of attraction' of the other ESS, the sensible one. The zone of attraction is the set of population ratios at which, in this case, sensible strategists have the advantage: once a population reaches this zone, it will be sucked inevitably towards the sensible stable point. It would be exciting to find an example of a paradoxical ESS in nature, but I doubt if we can really hope to do so. (I spoke too soon. After I had written this last sentence, Professor Maynard Smith called my attention to the following description of the behaviour of the Mexican social spider, Oecobius civitas, by J. W. Burgess: 'If a spider is disturbed and driven out of its retreat, it darts across the rock and, in the absence of a vacant crevice to hide in, may seek refuge in the hiding place of another spider of the same species. If the other spider is in residence when the intruder enters, it does not attack but darts out and seeks a new refuge of its own. Thus once the first spider is disturbed the process of sequential displacement from web to web may continue for several seconds, often causing a majority of the spiders in the aggregation to shift from their home refuge to an alien one (Social Spiders, Scientific American, March 1976).
What if individuals retain some memory of the outcome of past fights? This depends on whether the memory is specific or general. Crickets have a general memory of what happened in past fights. A cricket that has recently won a large number of fights becomes more hawkish. A cricket that has recently had a losing streak becomes more dovish. This was neatly shown by R. D. Alexander. He used a model cricket to beat up real crickets. After this treatment the real crickets became more likely to lose fights against other real crickets. Each cricket can be thought of as constantly updating his own estimate of his fighting ability, relative to that of an average individual in his population. If animals such as crickets, who work with a general memory of past fights, are kept together in a closed group for a time, a kind of dominance hierarchy is likely to develop. An observer can rank the individuals in order. Individuals lower in the order tend to give in to individuals higher in the order. There is no need to suppose that the individuals recognize each other. All that happens is that individuals who are accustomed to winning become even more likely to win, while individuals who are accustomed to losing become steadily more likely to lose. Even if the individuals started by winning or losing entirely at random, they would tend to sort themselves out into a rank order. This incidentally has the effect that the number of serious fights in the group gradually dies down.
I have to use the phrase 'kind of dominance hierarchy', because many people reserve the term dominance hierarchy for cases in which individual recognition is involved. In these cases, memory of past fights is specific rather than general. Crickets do not recognize each other as individuals, but hens and monkeys do. If you are a monkey, a monkey who has beaten you in the past is likely to beat you in the future. The best strategy for an individual is to be relatively dovish towards an individual who has previously beaten him. If a batch of hens who have never met before are introduced to each other, there is usually a great deal of fighting. After a time the fighting dies down. Not for the same reason as in the crickets, though. In the case of the hens it is because each individual 'learns her place' relative to each other individual. This is incidentally good for the group as a whole. As an indicator of this it has been noticed that in established groups of hens, where fierce fighting is rare, egg production is higher than in groups of hens whose membership is continually being changed, and in which fights are consequently more frequent. Biologists often speak of the biological advantage or 'function' of dominance hierarchies as being to reduce overt aggression in the group. However, this is the wrong way to put it. A dominance hierarchy perse cannot be said to have a 'function' in the evolutionary sense, since it is a property of a group, not of an individual. The individual behaviour patterns that manifest themselves in the form of dominance hierarchies when viewed at the group level may be said to have functions. It is, however, even better to abandon the word 'function' altogether, and to think about the matter in terms of ESSs in asymmetric contests where there is individual recognition and memory.
We have been thinking of contests between members of the same species. What about inter-specific contests? As we saw earlier, members of different species are less direct competitors than members of the same species. For this reason we should expect fewer disputes between them over resources, and our expectation is borne out. For instance, robins defend territories against other robins, but not against great tits. One can draw a map of the territories of different individual robins in a wood and one can superimpose a map of the territories of individual great tits. The territories of the two species overlap in an entirely indiscriminate way. They might as well be on different planets.
But there are other ways in which the interests of individuals from different species conflict very sharply. For instance a lion wants to eat an antelope's body, but the antelope has very different plans for its body. This is not normally regarded as competition for a resource, but logically it is hard to see why not. The resource in question is meat. The lion genes 'want' the meat as food for their survival machine. The antelope genes want the meat as working muscle and organs for their survival machine. These two uses for the meat are mutually incompatible, therefore there is conflict of interest.
Members of one's own species are made of meat too. Why is cannibalism relatively rare? As we saw in the case of black-headed gulls, adults do sometimes eat the young of their own species. Yet adult carnivores are never to be seen actively pursuing other adults of their own species with a view to eating them. Why not? We are still so used to thinking in terms of the 'good of the species' view of evolution that we often forget to ask perfectly reasonable questions like: 'Why don't lions hunt other lions?' Another good question of a type which is seldom asked is: 'Why do antelopes run away from lions instead of hitting back?'
The reason lions do not hunt lions is that it would not be an ESS for them to do so. A cannibal strategy would be unstable for the same reason as the hawk s
trategy in the earlier example. There is too much danger of retaliation. This is less likely to be true in contests between members of different species, which is why so many prey animals run away instead of retaliating. It probably stems originally from the fact that in an interaction between two animals of different species there is a built-in asymmetry which is greater than that between members of the same species. Whenever there is strong asymmetry in a contest, ESSs are likely to be conditional strategies dependent on the asymmetry. Strategies analogous to 'if smaller, run away; if larger, attack' are very likely to evolve in contests between members of different species because there are so many available asymmetries. Lions and antelopes have reached a kind of stability by evolutionary divergence, which has accentuated the original asymmetry of the contest in an ever-increasing fashion. They have become highly proficient in the arts of, respectively, chasing, and running away. A mutant antelope that adopted a 'stand and fight' strategy against lions would be less successful than rival antelopes disappearing over the horizon.
I have a hunch that we may come to look back on the invention of the ESS concept as one of the most important advances in evolutionary theory since Darwin. It is applicable wherever we find conflict of interest, and that means almost everywhere. Students of animal behaviour have got into the habit of talking about something called 'social organization'. Too often the social organization of a species is treated as an entity in its own right, with its own biological 'advantage'. An example I have already given is that of the 'dominance hierarchy'. I believe it is possible to discern hidden group-selectionist assumptions lying behind a large number of the statements that biologists make about social organization. Maynard Smith's concept of the ESS will enable us, for the first time, to see clearly how a collection of independent selfish entities can come to resemble a single organized whole. I think this will be true not only of social organizations within species, but also of 'ecosystems' and 'communities' consisting of many species. In the long term, I expect the ESS concept to revolutionize the science of ecology.
We can also apply it to a matter that was deferred from Chapter 3, arising from the analogy of oarsmen in a boat (representing genes in a body) needing a good team spirit. Genes are selected, not as 'good' in isolation, but as good at working against the background of the other genes in the gene pool. A good gene must be compatible with, and complementary to, the other genes with whom it has to share a long succession of bodies. A gene for plant-grinding teeth is a good gene in the gene pool of a herbivorous species, but a bad gene in the gene pool of a carnivorous species.
It is possible to imagine a compatible combination of genes as being selected together as a unit. In the case of the butterfly mimicry example of Chapter 3, this seems to be exactly what happened. But the power of the ESS concept is that it can now enable us to see how the same kind of result could be achieved by selection purely at the level of the independent gene. The genes do not have to be linked on the same chromosome.
The rowing analogy is really not up to explaining this idea. The nearest we can come to it is this. Suppose it is important in a really successful crew that the rowers should coordinate their activities by means of speech. Suppose further that, in the pool of oarsmen at the coach's disposal, some speak only English and some speak only German. The English are not consistently better or worse rowers than the Germans. But because of the importance of communication, a mixed crew will tend to win fewer races than either a pure English crew or a pure German crew.
The coach does not realize this. All he does is shuffle his men around, giving credit points to individuals in winning boats, marking down individuals in losing boats. Now if the pool available to him just happens to be dominated by Englishmen it follows that any German who gets into a boat is likely to cause it to lose, because communications break down. Conversely, if the pool happened to be dominated by Germans, an Englishman would tend to cause any boat in which he found himself to lose. What will emerge as the overall best crew will be one of the two stable states-pure English or pure German, but not mixed. Superficially it looks as though the coach is selecting whole language groups as units. This is not what he is doing. He is selecting individual oarsmen for their apparent ability to win races. It so happens that the tendency for an individual to win races depends on which other individuals are present in the pool of candidates. Minority candidates are automatically penalized, not because they are bad rowers, but simply because they are minority candidates. Similarly, the fact that genes are selected for mutual compatibility does not necessarily mean we have to think of groups of genes as being selected as units, as they were in the case of the butterflies. Selection at the low level of the single gene can give the impression of selection at some higher level.
In this example, selection favours simple conformity. More interestingly, genes may be selected because they complement each other. In terms of the analogy, suppose an ideally balanced crew would consist of four right-handers and four left-handers. Once again assume that the coach, unaware of this fact, selects blindly on 'merit'. Now if the pool of candidates happens to be dominated by right-handers, any individual left-hander will tend to be at an advantage: he is likely to cause any boat in which he finds himself to win, and he will therefore appear to be a good oarsman. Conversely, in a pool dominated by left-handers, a right-hander would have an advantage. This is similar to the case of a hawk doing well in a population of doves, and a dove doing well in a population of hawks. The difference is that there we were talking about interactions between individual bodies-selfish machines-whereas here we are talking, by analogy, about interactions between genes within bodies.
The coach's blind selection of 'good' oarsmen will lead in the end to an ideal crew consisting of four left-handers and four righthanders. It will look as though he selected them all together as a complete, balanced unit. I find it more parsimonious to think of him as selecting at a lower level, the level of the independent candidates. The evolutionarily stable state ('strategy' is misleading in this context) of four left-handers and four right-handers will emerge simply as a consequence of low-level selection on the basis of apparent merit.
The gene pool is the long-term environment of the gene. 'Good' genes are blindly selected as those that survive in the gene pool. This is not a theory; it is not even an observed fact: it is a tautology. The interesting question is what makes a gene good. As a first approximation I said that what makes a gene good is the ability to build efficient survival machines-bodies. We must now amend that statement. The gene pool will become an evolutionarily stable set of genes, defined as a gene pool that cannot be invaded by any new gene. Most new genes that arise, either by mutation or reassortment or immigration, are quickly penalized by natural selection: the evolutionarily stable set is restored. Occasionally a new gene does succeed in invading the set: it succeeds in spreading through the gene pool. There is a transitional period of instability, terminating in a new evolutionarily stable set-a little bit of evolution has occurred. By analogy with the aggression strategies, a population might have more than one alternative stable point, and it might occasionally flip from one to another. Progressive evolution may be not so much a steady upward climb as a series of discrete steps from stable plateau to stable plateau. It may look as though the population as a whole is behaving like a single self-regulating unit. But this illusion is produced by selection going on at the level of the single gene. Genes are selected on 'merit'. But merit is judged on the basis of performance against the background of the evolutionarily stable set which is the current gene pool.
By focussing on aggressive interactions between whole individuals, Maynard Smith was able to make things very clear. It is easy to think of stable ratios of hawk bodies and dove bodies, because bodies are large things which we can see. But such interactions between genes sitting in different bodies are only the tip of the iceberg. The vast majority of significant interactions between genes in the evolutionarily stable set-the gene pool-go on within individual
bodies. These interactions are difficult to see, for they take place within cells, notably the cells of developing embryos. Well-integrated bodies exist because they are the product of an evolutionarily stable set of selfish genes.
But I must return to the level of interactions between whole animals which is the main subject of this book. For understanding aggression it was convenient to treat individual animals as independent selfish machines. This model breaks down when the individuals concerned are close relatives-brothers and sisters, cousins, parents and children. This is because relatives share a substantial proportion of their genes. Each selfish gene therefore has its loyalties divided between different bodies. This is explained in the next chapter.
Genesmanship
What is the selfish gene? It is not just one single physical bit of DNA. Just as in the primeval soup, it is all replicas of a particular bit of DNA, distributed throughout the world. If we allow ourselves the licence of talking about genes as if they had conscious aims, always reassuring ourselves that we could translate our sloppy language back into respectable terms if we wanted to, we can ask the question, what is a single selfish gene trying to do? It is trying to get more numerous in the gene pool. Basically it does this by helping to program the bodies in which it finds itself to survive and to reproduce. But now we are emphasizing that 'it' is a distributed agency, existing in many different individuals at once. The key point of this chapter is that a gene might be able to assist replicas of itself that are sitting in other bodies. If so, this would appear as individual altruism but it would be brought about by gene selfishness.
The Selfish Gene Page 12