The Selfish Gene (14 page)

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 strategy 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.

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.

Consider the gene for being an albino in man. In fact several genes exist that can give rise to albinism, but I am talking about just one of them. It is recessive; that is, it has to be present in double dose in order for the person to be an albino. This is true of about 1 in 20,000 of us. But it is also present, in single dose, in about 1 in 70 of us, and these individuals are not albinos. Since it is distributed in many individuals, a gene such as the albino gene could, in theory, assist its own survival in the gene pool by programming its bodies to behave altruistically towards other albino bodies, since these are known to contain the same gene. The albino gene should be quite happy if some of the bodies that it inhabits die, provided that in doing so they help other bodies containing the same gene to survive. If the albino gene could make one of its bodies save the lives of 10 albino bodies, then even the death of the altruist is amply compensated by the increased numbers of albino genes in the gene pool.

Should we then expect albinos to be especially nice to each other? Actually the answer is probably no. In order to see why not, we must temporarily abandon our metaphor of the gene as a conscious agent, because in this context it becomes positively misleading. We must translate back into respectable, if more longwinded terms. Albino genes do not really 'want' to survive or to help other albino genes. But if the albino gene just happened to cause its bodies to behave altruistically towards other albinos, then automatically, willy-nilly, it would tend to become more numerous in the gene pool as a result. But, in order for this to happen, the gene would have to have two independent effects on bodies. Not only must it confer its usual effect of a very pale complexion. It must also confer a tendency to be selectively altruistic towards individuals with a very pale complexion. Such a double-effect gene could, if it existed, be very successful in the population.

Now it is true that genes do have multiple effects, as I emphasized in Chapter 3. It is theoretically possible that a gene could arise which conferred an externally visible 'label', say a pale skin, or a green beard, or anything conspicuous, and also a tendency to be specially nice to bearers of that conspicuous label. It is possible, but not particularly likely. Green beardedness is just as likely to be linked to a tendency to develop ingrowing toenails or any other trait, and a fondness for green beards is just as likely to go together with an inability to smell freesias. It is not very probable that one and the same gene would produce both the right label and the right sort of altruism. Nevertheless, what may be called the Green Beard Altruism Effect is a theoretical possibility.

An arbitrary label like a green beard is just one way in which a gene might 'recognize' copies of itself in other individuals. Are there any other ways? A particularly direct possible way is the following. The possessor of an altruistic gene might be recognized simply by the fact that he does altruistic acts. A gene could prosper in the gene pool if it 'said' the equivalent of: 'Body, if A is drowning as a result of trying to save someone else from drowning, jump in and rescue A.' The reason such a gene could do well is that there is a greater than average chance that A contains the same life-saving altruistic gene. The fact that A is seen to be trying to rescue somebody else is a label, equivalent to a green beard. It is less arbitrary than a green beard, but it still seems rather implausible. Are there any plausible ways in which genes might 'recognize' their copies in other individuals?

The answer is yes. It is easy to show that close relatives-kin-have a greater than average chance of sharing genes. It has long been clear that this must be why altruism by parents towards their young is so common. What R. A. Fisher, J. B. S. Haldane, and especially W. D. Hamilton realized, was that the same applies to other close relations-brothers and sisters, nephews and nieces, close cousins. If an individual dies in order to save ten close relatives, one copy of the kin-altruism gene may be lost, but a larger number of copies of the same gene is saved.

'A larger number' is a bit vague. So is 'close relatives'. We can do better than that, as Hamilton showed. His two papers of 1964 are among the most important contributions to social ethology ever written, and I have never been able to understand why they have been so neglected by ethologists (his name does not even appear in the index of two major text-books of ethology, both published in 1970). Fortunately there are recent signs of a revival of interest in his ideas. Hamilton's papers are rather mathematical, but it is easy to grasp the basic principles intuitively, without rigorous mathematics, though at the cost of some over-simplification. The thing we want to calculate is the probability, or odds, that two individuals, say two sisters, share a particular gene.

For simplicity I shall assume that we are talking about genes that are rare in the gene pool as a whole. Most people share 'the gene for not being an albino', whether they are related to each other or not. The reason this gene is so common is that in nature albinos are less likely to survive than non-albinos because, for example, the sun dazzles them and makes them relatively unlikely to see an approaching predator. We are not concerned with explaining the prevalence in the gene pool of such obviously 'good' genes as the gene for not being an albino. We are interested in explaining the success of genes specifically as a result of their altruism. We can therefore assume that, at least in the early stages of this process of evolution, these genes are rare. Now the important point is that even a gene that is rare in the population as a whole is common within a family. I contain a number of genes that are rare in the population as a whole, and you also contain genes that are rare in the population as a whole. The chance that we both contain the same rare genes is very small indeed. But the chances are good that my sister contains a particular rare gene that I contain, and the chances are equally good that your sister contains a rare gene in common with you. The odds are in this case exactly 50 per cent, and it is easy to explain why.

Suppose you contain one copy of the gene G. You must have received it either from your father or from your mother (for convenience we can neglect various infrequent possibilities-that G is a new mutation, that both your parents had it, or that either of your parents had two copies of it). Suppose it was your father who gave you the gene. Then every one of his ordinary body cells contained one copy of G. Now you will remember that when a man makes a sperm he doles out half his genes to it. There is therefore a 50 per cent chance that the sperm that begot your sister received the gene G. If, on the other hand, you received G from your mother, exactly parallel reasoning shows that half of her eggs must have contained G; once again, the chances are 50 per cent that your sister contains G. This means that if you had 100 brothers and sisters, approximately 50 of them would contain any particular rare gene that you contain. It also means that if you have 100 rare genes, approximately 50 of them are in the body of any one of your brothers or sisters.

You can do the same kind of calculation for any degree of kinship you like. An important relationship is that between parent and child. If you have one copy of gene H, the chance that any particular one of your children has it is 50 per cent, because half your sex cells contain H, and any particular child was made from one of those sex cells. If you have one copy of gene J, the chance that your father also had J is 50 per cent, because you received half your genes from him, and half from your mother. For convenience we use an index of relatedness, which expresses the chance of a gene being shared between two relatives. The relatedness between two brothers is 1/2, since half the genes possessed by one brother will be found in the other. This is an average figure: by the luck of the meiotic draw, it is possible for particular pairs of brothers to share more or fewer genes than this. The relatedness between parent and child is always exactly 1/2.

It is rather tedious going through the calculations from first principles every time, so here is a rough and ready rule for working out the relatedness between any two individuals A and B. You may find it useful in making your will, or in interpreting apparent resemblances in your own family. It works for all simple cases, but breaks down where incestuous mating occurs, and in certain insects, as we shall see.

First identify all the common ancestors of A and B. For instance, the common ancestors of a pair of first cousins are their shared grandfather and grandmother. Once you have found a common ancestor, it is of course logically true that all his ancestors are common to A and B as well. However, we ignore all but the most recent common ancestors. In this sense, first cousins have only two common ancestors. If B is a lineal descendant of A, for instance his great grandson, then A himself is the 'common ancestor' we are looking for.

Having located the common ancestor(s) of A and B, count the generation distance as follows. Starting at A, climb up the family tree until you hit a common ancestor, and then climb down again to B. The total number of steps up the tree and then down again is the generation distance. For instance, if A is B's uncle, the generation distance is 3. The common ancestor is A's father (say) and B's grandfather. Starting at A you have to climb up one generation in order to hit the common ancestor. Then to get down to B you have to descend two generations on the other side. Therefore the generation distance is 1 + 2 = 3.

Having found the generation distance between A and B via a particular common ancestor, calculate that part of their relatedness for which that ancestor is responsible. To do this, multiply 1/2 by itself once for each step of the generation distance. If the generation distance is 3, this means calculate 1/2 x 1/2 x 1/2. If the generation distance via a particular ancestor is equal to g steps, the portion of relatedness due to that ancestor is (1/2) to the power g.

But this is only part of the relatedness between A and B. If they have more than one common ancestor we have to add on the equivalent figure for each ancestor. It is usually the case that the generation distance is the same for all common ancestors of a pair of individuals. Therefore, having worked out the relatedness between A and B due to any one of the ancestors, all you have to do in practice is to multiply by the number of ancestors. First cousins, for instance, have two common ancestors, and the generation distance via each one is 4. Therefore their relatedness is 1/8.

If A is Bs greatgrandchild, the generation distance is 3 and the number of common 'ancestors' is 1 (B himself), so the relatedness is 1/8. Genetically speaking, your first cousin is equivalent to a great grandchild. Similarly, you are just as likely to 'take after' your uncle (relatedness = 1/4) as after your grandfather (relatedness = 1/4).

For relationships as distant as third cousin (1/128), we are getting down near the baseline probability that a particular gene possessed by A will be shared by any random individual taken from the population. A third cousin is not far from being equivalent to any old Tom, Dick, or Harry as far as an altruistic gene is concerned. A second cousin (relatedness = 1/32) is only a little bit special; a first cousin somewhat more so (1/8). Full brothers and sisters, and parents and children are very special (1/2), and identical twins (relatedness = 1) just as special as oneself. Uncles and aunts, nephews and nieces, grandparents and grandchildren, and half brothers and half sisters, are intermediate with a relatedness of 3.

Now we are in a position to talk about genes for kin-altruism much more precisely. A gene for suicidally saving five cousins would not become more numerous in the population, but a gene for saving five brothers or ten first cousins would. The minimum requirement for a suicidal altruistic gene to be successful is that it should save more than two siblings (or children or parents), or more than four half-siblings (or uncles, aunts, nephews, nieces, grandparents, grandchildren), or more than eight first cousins, etc. Such a gene, on average, tends to live on in the bodies of enough individuals saved by the altruist to compensate for the death of the altruist itself.

If an individual could be sure that a particular person was his identical twin, he should be exactly as concerned for his twin's welfare as for his own. Any gene for twin altruism is bound to be carried by both twins, therefore if one dies heroically to save the other the gene lives on. Nine-banded armadillos are born in a litter of identical quadruplets. As far as I know, no feats of heroic self-sacrifice have been reported for young armadillos, but it has been pointed out that some strong altruism is definitely to be expected, and it would be well worth somebody's while going out to South America to have a look.

We can now see that parental care is just a special case of kin altruism. Genetically speaking, an adult should devote just as much care and attention to its orphaned baby brother as it does to one of its own children. Its relatedness to both infants is exactly the same, 1/2. In gene selection terms, a gene for big sister altruistic behaviour should have just as good a chance of spreading through the population as a gene for parental altruism. In practice, this is an over-simplification for various reasons which we shall come to later, and brotherly or sisterly care is nothing like so common in nature as parental care. But the point I am making here is that there is nothing special genetically speaking about the parent/child relationship as against the brother/ sister relationship. The fact that parents actually hand on genes to children, but sisters do not hand on genes to each other is irrelevant, since the sisters both receive identical replicas of the same genes from the same parents.