The Selfish Gene

by Richard Dawkins

  Some survival machines exploit the sexual desires of others. Bee orchids induce bees to copulate with their flowers, because of their strong resemblance to female bees. What the orchid has to gain from this deception is pollination, for a bee who is fooled by two orchids will incidentally carry pollen from one to the other. Fireflies (which are really beetles) attract their mates by flashing lights at them. Each species has its own particular dot-dash flashing pattern, which prevents confusion between species, and consequent harmful hybridization. Just as sailors look out for the flash patterns of particular lighthouses, so fireflies seek the coded flash patterns of their own species. Females of the genus Photuris have 'discovered' that they can lure males of the genus Photinus if they imitate the flashing code of a Photinus female. This they do, and when a Photinus male is fooled by the lie into approaching, he is summarily eaten by the Photuris female. Sirens and Lorelei spring to mind as analogies, but Cornishmen will prefer to think of the wreckers of the old days, who used lanterns to lure ships on to the rocks, and then plundered the cargoes that spilled out of the wrecks.

  Whenever a system of communication evolves, there is always the danger that some will exploit the system for their own ends. Brought up as we have been on the 'good of the species' view of evolution, we naturally think first of liars and deceivers as belonging to different species: predators, prey, parasites, and so on. However, we must expect lies and deceit, and selfish exploitation of communication to arise whenever the interests of the genes of different individuals diverge. This will include individuals of the same species. As we shall see, we must even expect that children will deceive their parents, that husbands will cheat on wives, and that brother will lie to brother.

  Even the belief that animal communication signals originally evolve to foster mutual benefit, and then afterwards become exploited by malevolent parties, is too simple. It may well be that all animal communication contains an element of deception right from the start, because all animal interactions involve at least some conflict of interest. The next chapter introduces a powerful way of thinking about conflicts of interest from an evolutionary point of view.

  Aggression: Stability and the Selfish Machine

  This chapter is mostly about the much-misunderstood topic of aggression. We shall continue to treat the individual as a selfish machine, programmed to do whatever is best for its genes as a whole. This is the language of convenience. At the end of the chapter we return to the language of single genes.

  To a survival machine, another survival machine (which is not its own child or another close relative) is part of its environment, like a rock or a river or a lump of food. It is something that gets in the way, or something that can be exploited. It differs from a rock or a river in one important respect: it is inclined to hit back. This is because it too is a machine that holds its immortal genes in trust for the future, and it too will stop at nothing to preserve them. Natural selection favours genes that control their survival machines in such a way that they make the best use of their environment. This includes making the best use of other survival machines, both of the same and of different species.

  In some cases survival machines seem to impinge rather little on each others' lives. For instance moles and blackbirds do not eat each other, mate with each other, or compete with each other for living space. Even so, we must not treat them as completely insulated. They may compete for something, perhaps earthworms. This does not mean you will ever see a mole and a blackbird engaged in a tug of war over a worm; indeed a blackbird may never set eyes on a mole in its life. But if you wiped out the population of moles, the effect on blackbirds might be dramatic, although I could not hazard a guess as to what the details might be, nor by what tortuously indirect routes the influence might travel.

  Survival machines of different species influence each other in a variety of ways. They may be predators or prey, parasites or hosts, competitors for some scarce resource. They may be exploited in special ways, as for instance when bees are used as pollen carriers by flowers.

  Survival machines of the same species tend to impinge on each others' lives more directly. This is for many reasons. One is that half the population of one's own species may be potential mates, and potentially hard-working and exploitable parents to one's children. Another reason is that members of the same species, being very similar to each other, being machines for preserving genes in the same kind of place, with the same kind of way of life, are particularly direct competitors for all the resources necessary for life. To a blackbird, a mole may be a competitor, but it is not nearly so important a competitor as another blackbird. Moles and blackbirds may compete for worms, but blackbirds and blackbirds compete with each other for worms and for everything else. If they are members of the same sex, they may also compete for mating partners. For reasons that we shall see, it is usually the males who compete with each other for females. This means that a male might benefit his own genes if he does something detrimental to another male with whom he is competing.

  The logical policy for a survival machine might therefore seem to be to murder its rivals, and then, preferably, to eat them. Although murder and cannibalism do occur in nature, they are not as common as a naive interpretation of the selfish gene theory might predict. Indeed Konrad Lorenz, in On Aggression, stresses the restrained and gentlemanly nature of animal fighting. For him the notable thing about animal fights is that they are formal tournaments, played according to rules like those of boxing or fencing. Animals fight with gloved fists and blunted foils. Threat and bluff take the place of deadly earnest. Gestures of surrender are recognized by victors, who then refrain from dealing the killing blow or bite that our naive theory might predict.

  This interpretation of animal aggression as being restrained and formal can be disputed. In particular, it is certainly wrong to condemn poor old Homo sapiens as the only species to kill his own kind, the only inheritor of the mark of Cain, and similar melodramatic charges. Whether a naturalist stresses the violence or the restraint of animal aggression depends partly on the kinds of animals he is used to watching, and partly on his evolutionary preconceptions-Lorenz is, after all, a 'good of the species' man. Even if it has been exaggerated, the gloved fist view of animal fights seems to have at least some truth. Superficially this looks like a form of altruism. The selfish gene theory must face up to the difficult task of explaining it. Why is it that animals do not go all out to kill rival members of their species at every possible opportunity?

  The general answer to this is that there are costs as well as benefits resulting from outright pugnacity, and not only the obvious costs in time and energy. For instance, suppose that B and C are both my rivals, and I happen to meet B. It might seem sensible for me as a selfish individual to try to kill him. But wait. C is also my rival, and C is also B's rival. By killing B, I am potentially doing a good turn to C by removing one of his rivals. I might have done better to let B live, because he might then have competed or fought with C, thereby benefiting me indirectly. The moral of this simple hypothetical example is that there is no obvious merit in indiscriminately trying to kill rivals. In a large and complex system of rivalries, removing one rival from the scene does not necessarily do any good: other rivals may be more likely to benefit from his death than oneself. This is the kind of hard lesson that has been learned by pest-control officers. You have a serious agricultural pest, you discover a good way to exterminate it and you gleefully do so, only to find that another pest benefits from the extermination even more than human agriculture does, and you end up worse off than you were before.

  On the other hand, it might seem a good plan to kill, or at least fight with, certain particular rivals in a discriminating way. If B is an elephant seal in possession of a large harem full of females, and if I, another elephant seal, can acquire his harem by killing him, I might be well advised to attempt to do so. But there are costs and risks even in selectivity pugnacity. It is to B's advantage to fight back, to defend his valuable prope
rty. If I start a fight, I am just as likely to end up dead as he is. Perhaps even more so. He holds a valuable resource, that is why I want to fight him. But why does he hold it? Perhaps he won it in combat. He has probably beaten off other challengers before me. He is probably a good fighter. Even if I win the fight and gain the harem, I may be so badly mauled in the process that I cannot enjoy the benefits. Also, fighting uses up time and energy. These might be better conserved for the time being. If I concentrate on feeding and on keeping out of trouble for a time, I shall grow bigger and stronger. I'll fight him for the harem in the end, but I may have a better chance of winning eventually if I wait, rather than rush in now.

  This subjective soliloquy is just a way of pointing out that the decision whether or not to fight should ideally be preceded by a complex, if unconscious, 'cost-benefit' calculation. The potential benefits are not all stacked up on the side of fighting, although undoubtedly some of them are. Similarly, during a fight, each tactical decision over whether to escalate the fight or cool it has costs and benefits which could, in principle, be analysed. This has long been realized by ethologists in a vague sort of way, but it has taken J. Maynard Smith, not normally regarded as an ethologist, to express the idea forcefully and clearly. In collaboration with G. R. Price and G. A. Parker, he uses the branch of mathematics known as Game Theory. Their elegant ideas can be expressed in words without mathematical symbols, albeit at some cost in rigour.

  The essential concept Maynard Smith introduces is that of the evolutionarily stable strategy, an idea that he traces back to W. D. Hamilton and R. H. MacArthur. A 'strategy' is a pre-programmed behavioural policy. An example of a strategy is: 'Attack opponent; if he flees pursue him; if he retaliates run away.' It is important to realize that we are not thinking of the strategy as being consciously worked out by the individual. Remember that we are picturing the animal as a robot survival machine with a pre-programmed computer controlling the muscles. To write the strategy out as a set of simple instructions in English is just a convenient way for us to think about it. By some unspecified mechanism, the animal behaves as if he were following these instructions.

  An evolutionarily stable strategy or ESS is defined as a strategy which, if most members of a population adopt it, cannot be bettered by an alternative strategy. It is a subtle and important idea. Another way of putting it is to say that the best strategy for an individual depends on what the majority of the population are doing. Since the rest of the population consists of individuals, each one trying to maximize his own success, the only strategy that persists will be one which, once evolved, cannot be bettered by any deviant individual. Following a major environmental change there may be a brief period of evolutionary instability, perhaps even oscillation in the population. But once an ESS is achieved it will stay: selection will penalize deviation from it.

  To apply this idea to aggression, consider one of Maynard Smith's simplest hypothetical cases. Suppose that there are only two sorts of fighting strategy in a population of a particular species, named hawk and dove. (The names refer to conventional human usage and have no connection with the habits of the birds from whom the names are derived: doves are in fact rather aggressive birds.) Any individual of our hypothetical population is classified as a hawk or a dove. Hawks always fight as hard and as unrestrainedly as they can, retreating only when seriously injured. Doves merely threaten in a dignified conventional way, never hurting anybody. If a hawk fights a dove the dove quickly runs away, and so does not get hurt. If a hawk fights a hawk they go on until one of them is seriously injured or dead. If a dove meets a dove nobody gets hurt; they go on posturing at each other for a long time until one of them tires or decides not to bother any more, and therefore backs down. For the time being, we assume that there is no way in which an individual can tell, in advance, whether a particular rival is a hawk or a dove. He only discovers this by fighting him, and he has no memory of past fights with particular individuals to guide him.

  Now as a purely arbitrary convention we allot contestants 'points'. Say 50 points for a win, 0 for losing, -100 for being seriously injured, and -10 for wasting time over a long contest. These points can be thought of as being directly convertible into the currency of gene survival. An individual who scores high points, who has a high average 'pay-off, is an individual who leaves many genes behind him in the gene pool. Within broad limits the actual numerical values do not matter for the analysis, but they help us to think about the problem.

  The important thing is that we are not interested in whether hawks will tend to beat doves when they fight them. We already know the answer to that: hawks will always win. We want to know whether either hawk or dove is an evolutionarily stable strategy. If one of them is an ESS and the other is not, we must expect that the one which is the ESS will evolve. It is theoretically possible for there to be two ESSs. This would be true if, whatever the majority strategy of the population happened to be, whether hawk or dove, the best strategy for any given individual was to follow suit. In this case the population would tend to stick at whichever one of its two stable states it happened to reach first. However, as we shall now see, neither of these two strategies, hawk or dove, would in fact be evolutionarily stable on its own, and we should therefore not expect either of them to evolve. To show this we must calculate average pay-offs.

  Suppose we have a population consisting entirely of doves.

  Whenever they fight, nobody gets hurt. The contests consist of prolonged ritual tournaments, staring matches perhaps, which end only when one rival backs down. The winner then scores 50 points for gaining the resource in dispute, but he pays a penalty of -10 for wasting time over a long staring match, so scores 40 in all. The loser also is penalized -10 points for wasting time. On average, any one individual dove can expect to win half his contests and lose half. Therefore his average pay-off per contest is the average of +40 and -10, which is +15. Therefore, every individual dove in a population of doves seems to be doing quite nicely.

  But now suppose a mutant hawk arises in the population. Since he is the only hawk around, every fight he has is against a dove. Hawks always beat doves, so he scores +50 every fight, and this is his average pay-off. He enjoys an enormous advantage over the doves, whose net pay-off is only +15. Hawk genes will rapidly spread through the population as a result. But now each hawk can no longer count on every rival he meets being a dove. To take an extreme example, if the hawk gene spread so successfully that the entire population came to consist of hawks, all fights would now be hawk fights. Things are now very different. When hawk meets hawk, one of them is seriously injured, scoring -100, while the winner scores +50. Each hawk in a population of hawks can expect to win half his fights and lose half his fights. His average expected pay-off per fight is therefore half-way between +50 and -100, which is -25. Now consider a single dove in a population of hawks. To be sure, he loses all his fights, but on the other hand he never gets hurt. His average pay-off is 0 in a population of hawks, whereas the average pay-off for a hawk in a population of hawks is -25. Dove genes will therefore tend to spread through the population.

  The way I have told the story it looks as if there will be a continuous oscillation in the population. Hawk genes will sweep to ascendancy; then, as a consequence of the hawk majority, dove genes will gain an advantage and increase in numbers until once again hawk genes start to prosper, and so on. However, it need not be an oscillation like this. There is a stable ratio of hawks to doves. For the particular arbitrary points system we are using, the stable ratio, if you work it out, turns out to be 5/12 doves to 7/12 hawks. When this stable ratio is reached, the average pay-off for hawks is exactly equal to the average pay-off for doves. Therefore selection does not favour either one of them over the other. If the number of hawks in the population started to drift upwards so that the ratio was no longer 7/12 doves would start to gain an extra advantage, and the ratio would swing back to the stable state. Just as we shall find the stable sex ratio to be 50:50, so the stable ha
wk to dove ratio in this hypothetical example is 7:5. In either case, if there are oscillations about the stable point, they need not be very large ones.

  Superficially, this sounds a little like group selection, but it is really nothing of the kind. It sounds like group selection because it enables us to think of a population as having a stable equilibrium to which it tends to return when disturbed. But the ESS is a much more subtle concept than group selection. It has nothing to do with some groups being more successful than others. This can be nicely illustrated using the arbitrary points system of our hypothetical example. The average pay-off to an individual in a stable population consisting of 7/12 hawks and 5/12 doves, turns out to be 6 1/4. This is true whether the individual is a hawk or a dove. Now 6 1/4 is much less than the average pay-off for a dove in a population of doves (15). If only everybody would agree to be a dove, every single individual would benefit. By simple group selection, any group in which all individuals mutually agree to be doves would be far more successful than a rival group sitting at the ESS ratio. (As a matter of fact, a conspiracy of nothing but doves is not quite the most successful possible group. In a group consisting of 1/6 hawks and 5/6 doves, the average pay-off per contest is 16 2/3. This is the most successful possible conspiracy, but for present purposes we can ignore it. A simpler all-dove conspiracy, with its average pay-off for each individual of 15, is far better for every single individual than the ESS would be.) Group selection theory would therefore predict a tendency to evolve towards an all-dove conspiracy, since a group that contained a 7/12 proportion of hawks would be less successful. But the trouble with conspiracies, even those that are to everybody's advantage in the long run, is that they are open to abuse. It is true that everybody does better in an all-dove group than he would in an ESS group. But unfortunately, in conspiracies of doves, a single hawk does so extremely well that nothing could stop the evolution of hawks. The conspiracy is therefore bound to be broken by treachery from within. An ESS is stable, not because it is particularly good for the individuals participating in it, but simply because it is immune to treachery from within.