How can reciprocal altruism evolve

Living reference work entry First Online: 10 December How to cite. Synonyms Cooperative investments ; Cooperative returns ; Reciprocal rewards ; Reciprocity ; Sanctions ; Social partner choice. This process is experimental and the keywords may be updated as the learning algorithm improves. This is a preview of subscription content, log in to check access. Arnocky, S.

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The costs and benefits are measured in terms of reproductive fitness , or expected number of offspring. So by behaving altruistically, an organism reduces the number of offspring it is likely to produce itself, but boosts the number that other organisms are likely to produce. This biological notion of altruism is not identical to the everyday concept. But in the biological sense there is no such requirement.

Indeed, some of the most interesting examples of biological altruism are found among creatures that are presumably not capable of conscious thought at all, e. For the biologist, it is the consequences of an action for reproductive fitness that determine whether the action counts as altruistic, not the intentions, if any, with which the action is performed.

Altruistic behaviour is common throughout the animal kingdom, particularly in species with complex social structures. For example, vampire bats regularly regurgitate blood and donate it to other members of their group who have failed to feed that night, ensuring they do not starve. Vervet monkeys give alarm calls to warn fellow monkeys of the presence of predators, even though in doing so they attract attention to themselves, increasing their personal chance of being attacked.

In social insect colonies ants, wasps, bees and termites , sterile workers devote their whole lives to caring for the queen, constructing and protecting the nest, foraging for food, and tending the larvae. Such behaviour is maximally altruistic: sterile workers obviously do not leave any offspring of their own—so have personal fitness of zero—but their actions greatly assist the reproductive efforts of the queen. From a Darwinian viewpoint, the existence of altruism in nature is at first sight puzzling, as Darwin himself realized.

Natural selection leads us to expect animals to behave in ways that increase their own chances of survival and reproduction, not those of others. To see this, imagine that some members of a group of Vervet monkeys give alarm calls when they see predators, but others do not.

Other things being equal, the latter will have an advantage. By selfishly refusing to give an alarm call, a monkey can reduce the chance that it will itself be attacked, while at the same time benefiting from the alarm calls of others.

So we should expect natural selection to favour those monkeys that do not give alarm calls over those that do. But this raises an immediate puzzle. How did the alarm-calling behaviour evolve in the first place, and why has it not been eliminated by natural selection? How can the existence of altruism be reconciled with basic Darwinian principles?

The problem of altruism is intimately connected with questions about the level at which natural selection acts. If selection acts exclusively at the individual level, favouring some individual organisms over others, then it seems that altruism cannot evolve, for behaving altruistically is disadvantageous for the individual organism itself, by definition.

However, it is possible that altruism may be advantageous at the group level. A group containing lots of altruists, each ready to subordinate their own selfish interests for the greater good of the group, may well have a survival advantage over a group composed mainly or exclusively of selfish organisms.

A process of between-group selection may thus allow the altruistic behaviour to evolve. Within each group, altruists will be at a selective disadvantage relative to their selfish colleagues, but the fitness of the group as a whole will be enhanced by the presence of altruists. Groups composed only or mainly of selfish organisms go extinct, leaving behind groups containing altruists. In the example of the Vervet monkeys, a group containing a high proportion of alarm-calling monkeys will have a survival advantage over a group containing a lower proportion.

So conceivably, the alarm-calling behaviour may evolve by between-group selection, even though within each group, selection favours monkeys that do not give alarm calls.

The idea that group selection might explain the evolution of altruism was first broached by Darwin himself. In The Descent of Man , Darwin discussed the origin of altruistic and self-sacrificial behaviour among humans. Darwin's suggestion is that the altruistic behaviour in question may have evolved by a process of between-group selection.

The concept of group selection has a chequered and controversial history in evolutionary biology. The founders of modern neo-Darwinism—R. Fisher, J. Haldane and S. Wright—were all aware that group selection could in principle permit altruistic behaviours to evolve, but they doubted the importance of this evolutionary mechanism.

Nonetheless, many mid-twentieth century ecologists and some ethologists, notably Konrad Lorenz, routinely assumed that natural selection would produce outcomes beneficial for the whole group or species, often without even realizing that individual-level selection guarantees no such thing.

Williams and J. Maynard Smith These authors argued that group selection was an inherently weak evolutionary force, hence unlikely to promote interesting altruistic behaviours. This conclusion was supported by a number of mathematical models, which apparently showed that group selection would only have significant effects for a limited range of parameter values. As a result, the notion of group selection fell into widespread disrepute in orthodox evolutionary circles; see Sober and Wilson , Segestrale , Okasha , Leigh and Sober for details of the history of this debate.

These free-riders will have an obvious fitness advantage: they benefit from the altruism of others, but do not incur any of the costs. So even if a group is composed exclusively of altruists, all behaving nicely towards each other, it only takes a single selfish mutant to bring an end to this happy idyll.

By virtue of its relative fitness advantage within the group, the selfish mutant will out-reproduce the altruists, hence selfishness will eventually swamp altruism. Since the generation time of individual organisms is likely to be much shorter than that of groups, the probability that a selfish mutant will arise and spread is very high, according to this line of argument.

If group selection is not the correct explanation for how the altruistic behaviours found in nature evolved, then what is? This theory, discussed in detail below, apparently showed how altruistic behaviour could evolve without the need for group-level selection, and quickly gained prominence among biologists interested in the evolution of social behaviour; the empirical success of kin selection theory contributed to the demise of the group selection concept.

However, the precise relation between kin and group selection is a source of ongoing controversy see for example the recent exchange in Nature between Nowak, Tarnita and Wilson and Abbot et.

Sober and Wilson The basic idea of kin selection is simple. Imagine a gene which causes its bearer to behave altruistically towards other organisms, e. Organisms without the gene are selfish—they keep all their food for themselves, and sometimes get handouts from the altruists.

Clearly the altruists will be at a fitness disadvantage, so we should expect the altruistic gene to be eliminated from the population. However, suppose that altruists are discriminating in who they share food with. They do not share with just anybody, but only with their relatives. This immediately changes things.

For relatives are genetically similar—they share genes with one another. So when an organism carrying the altruistic gene shares his food, there is a certain probability that the recipients of the food will also carry copies of that gene. How probable depends on how closely related they are.

This means that the altruistic gene can in principle spread by natural selection. The gene causes an organism to behave in a way which reduces its own fitness but boosts the fitness of its relatives—who have a greater than average chance of carrying the gene themselves.

So the overall effect of the behaviour may be to increase the number of copies of the altruistic gene found in the next generation, and thus the incidence of the altruistic behaviour itself.

Though this argument was hinted at by Haldane in the s, and to a lesser extent by Darwin in his discussion of sterile insect castes in The Origin of Species , it was first made explicit by William Hamilton in a pair of seminal papers.

Hamilton demonstrated rigorously that an altruistic gene will be favoured by natural selection when a certain condition, known as Hamilton's rule , is satisfied. The costs and benefits are measured in terms of reproductive fitness. Two genes are identical by descent if they are copies of a single gene in a shared ancestor.

The higher the value of r, the greater the probability that the recipient of the altruistic behaviour will also possess the gene for altruism. So what Hamilton's rule tells us is that a gene for altruism can spread by natural selection, so long as the cost incurred by the altruist is offset by a sufficient amount of benefit to sufficiently closed related relatives.

The proof of Hamilton's rule relies on certain non-trivial assumptions; see Frank , Grafen , , Queller a, b, Boyd and McIlreath and Birch forthcoming for details.

Kin selection theory predicts that animals are more likely to behave altruistically towards their relatives than towards unrelated members of their species. Moreover, it predicts that the degree of altruism will be greater, the closer the relationship.

In the years since Hamilton's theory was devised, these predictions have been amply confirmed by empirical work. Similarly, studies of Japanese macaques have shown that altruistic actions, such as defending others from attack, tend to be preferentially directed towards close kin.

So a female may well be able to get more genes into the next generation by helping the queen reproduce, hence increasing the number of sisters she will have, rather than by having offspring of her own. Kin selection theory therefore provides a neat explanation of how sterility in the social insects may have evolved by Darwinian means.

Note, however, that the precise significance of haplodiploidy for the evolution of worker sterility is a controversial question; see Maynard Smith and Szathmary ch. The gene's eye-view is certainly the easiest way of understanding kin selection, and was employed by Hamilton himself in his papers.

Altruism seems anomalous from the individual organism's point of view, but from the gene's point of view it makes good sense. A gene wants to maximize the number of copies of itself that are found in the next generation; one way of doing that is to cause its host organism to behave altruistically towards other bearers of the gene, so long as the costs and benefits satisfy the Hamilton inequality.

But interestingly, Hamilton showed that kin selection can also be understood from the organism's point of view. Though an altruistic behaviour which spreads by kin selection reduces the organism's personal fitness by definition , it increases what Hamilton called the organism's inclusive fitness. An organism's inclusive fitness is defined as its personal fitness, plus the sum of its weighted effects on the fitness of every other organism in the population, the weights determined by the coefficient of relationship r.

Given this definition, natural selection will act to maximise the inclusive fitness of individuals in the population Grafen Instead of thinking in terms of selfish genes trying to maximize their future representation in the gene-pool, we can think in terms of organisms trying to maximize their inclusive fitness.

Contrary to what is sometimes thought, kin selection does not require that animals must have the ability to discriminate relatives from non-relatives, less still to calculate coefficients of relationship. Many animals can in fact recognize their kin, often by smell, but kin selection can operate in the absence of such an ability. Hamilton's inequality can be satisfied so long as an animal behaves altruistically towards other animals that are in fact its relatives.

The animal might achieve this by having the ability to tell relatives from non-relatives, but this is not the only possibility. An alternative is to use some proximal indicator of kinship. For example, if an animal behaves altruistically towards those in its immediate vicinity, then the recipients of the altruism are likely to be relatives, given that relatives tend to live near each other. No ability to recognize kin is presupposed. Cuckoos exploit precisely this fact, free-riding on the innate tendency of birds to care for the young in their nests.

Though some sociobiologists have made incautious remarks to this effect, evolutionary theories of behaviour, including kin selection, are not committed to it. So long as the behaviours in question have a genetical component , i. Kin selection theory does not deny the truism that all traits are affected by both genes and environment.

Nor does it deny that many interesting animal behaviours are transmitted through non-genetical means, such as imitation and social learning Avital and Jablonka The importance of kinship for the evolution of altruism is very widely accepted today, on both theoretical and empirical grounds. However, kinship is really only a way of ensuring that altruists and recipients both carry copies of the altruistic gene, which is the fundamental requirement. If altruism is to evolve, it must be the case that the recipients of altruistic actions have a greater than average probability of being altruists themselves.

Kin-directed altruism is the most obvious way of satisfying this condition, but there are other possibilities too Hamilton , Sober and Wilson , Bowles and Gintis , Gardner and West For example, if the gene that causes altruism also causes animals to favour a particular feeding ground for whatever reason , then the required correlation between donor and recipient may be generated.

It is this correlation, however brought about, that is necessary for altruism to evolve. This point was noted by Hamilton himself in the s: he stressed that the coefficient of relationship of his papers should really be replaced with a more general correlation coefficient, which reflects the probability that altruist and recipient share genes, whether because of kinship or not Hamilton , , This point is theoretically important, and has not always been recognized; but in practice, kinship remains the most important source of statistical associations between altruists and recipients Maynard Smith , Okasha , West et al.

Consider a large population of organisms who engage in a social interaction in pairs; the interaction affects their biological fitness. Organisms are of two types: selfish S and altruistic A. The latter engage in pro-social behaviour, thus benefiting their partner but at a cost to themselves; the former do not. So in a mixed S,A pair, the selfish organism does better—he benefits from his partner's altruism without incurring any cost.

However, A,A pairs do better than S,S pairs—for the former work as a co-operative unit, while the latter do not. The interaction thus has the form of a one-shot Prisoner's dilemma, familiar from game theory.

The question we are interested in is: which type will be favoured by selection? To make the analysis tractable, we make two simplifying assumptions: that reproduction is asexual, and that type is perfectly inherited, i. Modulo these assumptions, the evolutionary dynamics can be determined very easily, simply by seeing whether the S or the A type has higher fitness, in the overall population.

The fitness of the S type, W S , is the weighted average of the payoff to an S when partnered with an S and the payoff to an S when partnered with an A , where the weights are determined by the probability of having the partner in question.

The conditional probabilities in the above expression should be read as the probability of having a selfish altruistic partner, given that one is selfish oneself.

From these expressions for the fitnesses of the two types of organism, we can immediately deduce that the altruistic type will only be favoured by selection if there is a statistical correlation between partners, i. For suppose there is no such correlation—as would be the case if the pairs were formed by random sampling from the population.

Then, the probability of having a selfish partner would be the same for both S and A types, i. From these probabilistic equalities, it follows immediately that W S is greater than W A , as can be seen from the expressions for W S and W A above; so the selfish type will be favoured by natural selection, and will increase in frequency every generation until all the altruists are eliminated from the population. Therefore, in the absence of correlation between partners, selfishness must win out cf.

Skyrms This confirms the point noted in section 2—that altruism can only evolve if there is a statistical tendency for the beneficiaries of altruistic actions to be altruists themselves. The easiest way to see this is to suppose that the correlation is perfect, i. This simple model also highlights the point made previously, that donor-recipient correlation, rather than genetic relatedness, is the key to the evolution of altruism.

What is needed for altruism to evolve, in the model above, is for the probability of having a partner of the same type as oneself to be sufficiently larger than the probability of having a partner of opposite type; this ensures that the recipients of altruism have a greater than random chance of being fellow altruists, i.

Whether this correlation arises because partners tend to be relatives, or because altruists are able to seek out other altruists and choose them as partners, or for some other reason, makes no difference to the evolutionary dynamics, at least in this simple example. Altruism is a well understood topic in evolutionary biology; the theoretical ideas explained above have been extensively analysed, empirically confirmed, and are widely accepted.

Nonetheless, there are a number of conceptual ambiguities surrounding altruism and related concepts in the literature; some of these are purely semantic, others are more substantive. Three such ambiguities are briefly discussed below; for further discussion, see West et al. According to the standard definition, a social behaviour counts as altruistic if it reduces the fitness of the organism performing the behaviour, but boosts the fitness of others.

This was the definition used by Hamilton , and by many subsequent authors. However, there is less consensus on how to describe behaviours that boost the fitness of others but also boost the fitness of the organism performing the behaviour.

As West et al. To avoid this confusion, West et al. Whatever term is used, the important point is that behaviours that benefit both self and others can evolve much more easily than altruistic behaviours, and thus require no special mechanisms such as kinship. The reason is clear: organisms performing such behaviours thereby increase their personal fitness, so are at a selective advantage vis-a-vis those not performing the behaviour.

The fact that the behaviour has a beneficial effect on the fitness of others is a mere side-effect, or byproduct, and is not part of the explanation for why the behaviour evolves.

For example, Sachs et al. Also indicative of the difference between altruistic behaviour and behaviour that benefit both self and others is the fact that in the latter case, though not the former, the beneficiary may be a member of a different species, without altering the evolutionary dynamics of the behaviour.

By contrast, in the case of altruism, it makes an enormous difference whether the beneficiary and the donor are con-specifics or not; for if not, then kin selection can play no role, and it is quite unclear how the altruistic behaviour can evolve.

Unsurprisingly, virtually all the bona fide examples of biological altruism in the living world involve donors and recipients that are con-specifics. A quite different ambiguity concerns the distinction between weak and strong altruism, in the terminology of D. Wilson , , This distinction is about whether the altruistic action entails an absolute or relative fitness reduction for the donor.

To count as strongly altruistic, a behaviour must reduce the absolute fitness i. Strong altruism is the standard notion of altruism in the literature, and was assumed above. To count as weakly altruistic, an action need only reduce the relative fitness of the donor, i. Thus for example, an action which causes an organism to leave an additional 10 offspring, but causes each organism s with which it interacts to leave an additional 20 offspring, is weakly but not strongly altruistic.

Should weakly altruistic behaviours be classified as altruistic or selfish? This question is not merely semantic; for the real issue is whether the conditions under which weak altruism can evolve are relevantly similar to the conditions under which strong altruism can evolve, or not.

To appreciate this argument, consider a game-theoretic scenario similar to the one-shot Prisoner's dilemma of section 4, in which organisms engage in a pair-wise interaction that affects their fitness. Organisms are of two types, weakly altruistic W and non-altruistic N. W -types perform an action that boosts their own fitness by 10 units and the fitness of their partner by 20 units; N -types do not perform the action.

The payoff matrix is thus:. The payoff matrix highlights the fact that weak altruism is individually advantageous, and thus the oddity of thinking of it it as altruistic rather than selfish. To see this, assume for a moment that the game is being played by two rational agents, as in classical game theory.

Clearly, the rational strategy for each individual is W , for W dominates N. Each individual gets a higher payoff from playing W than N , irrespective of what its opponent does —30 rather than 20 if the opponent plays W , 10 rather than 0 if the opponent plays N.

This captures a clear sense in which weak altruism is individually advantageous. In the context of evolutionary game theory, where the game is being played by pairs of organisms with hard-wired strategies, the counterpart of the fact that W dominates N is the fact that W can spread in the population even if pairs are formed at random cf.

Wilson To see this, consider the expressions for the overall population-wide fitnesses of W and N :. Therefore, weak altruism can evolve in the absence of donor-recipient correlation; as we saw, this is not true of strong altruism.

So weak and strong altruism evolve by different evolutionary mechanisms, hence should not be co-classified, according to this argument.