Primate reciprocity and its cognitive requirements

Humans can engage in relatively indiscriminate altruistic behaviors such as donating money to charities, giving blood, and volunteering to review scientific papers. They also live in societies characterized by examples of cooperation of unmatched complexity, such as organized armies, the cooperative building of infrastructures such as roads and railways, and tax‐paying, among others. (We exclude, of course, the “anonymous” societies of some social insects in which the animals themselves are not aware of the cooperative roles they play.) The emphasis on these unique aspects of our behavior 1 has sometimes distracted scientists from paying attention to the more common aspects of our daily lives, which share characteristics with those of our fellow primates. We invite friends for dinner, console others after a loss, intervene in ongoing fights, and even groom others. 2 - 4 These small acts of altruism, which constitute a large part of our daily social life, tend to resemble those of nonhuman primates.     

Give unto others: genetically unrelated cotton-top tamarin monkeys preferentially give food to those who altruistically give food back

Altruistic food giving among genetically unrelated individuals is rare in nature. The few examples that exist suggest that when animals give food to unrelated others, they may do so on the basis of mutualistic or reciprocally altruistic relationships. We present the results of four experiments designed to tease apart the factors mediating food giving among genetically unrelated cotton-top tamarins (Saguinus oedipus), a cooperatively breeding New World primate. In experiment 1 we show that individuals give significantly more food to a trained conspecific who unilaterally gives food than to a conspecific who unilaterally never gives food. The apparent contingency of the tamarins' food-giving behaviour motivated the design of experiments 2-4. Results from all three experiments show that altruistic food giving is mediated by prior acts of altruistic food giving by a conspecific. Specifically, tamarins do not give food to unrelated others when the food received in the past represents the by-product of another's selfish actions (experiments 2 and 3) or when a human experimenter gives them food (experiment 4) as did the unilateral altruist in experiment 1. By contrast, if one tamarin gives another food without obtaining any immediate benefit, then the recipient is more likely to give food in return. Overall, results show that tamarins altruistically give food to genetically unrelated conspecifics, discriminate between altruistic and selfish actions, and give more food to those who give food back. Tamarins therefore have the psychological capacity for reciprocally mediated altruism.     

Linking brain structure and activation in temporoparietal junction to explain the neurobiology of human altruism

Human altruism shaped our evolutionary history and pervades social and political life. There are, however, enormous individual differences in altruism. Some people are almost completely selfish, while others display strong altruism, and the factors behind this heterogeneity are only poorly understood. We examine the neuroanatomical basis of these differences with voxel-based morphometry and show that gray matter (GM) volume in the right temporoparietal junction (TPJ) is strongly associated with both individuals' altruism and the individual-specific conditions under which this brain region is recruited during altruistic decision making. Thus, individual differences in GM volume in TPJ not only translate into individual differences in the general propensity to behave altruistically, but they also create a link between brain structure and brain function by indicating the conditions under which individuals are likely to recruit this region when they face a conflict between altruistic and selfish acts.     

Altruism among relatives and non-relatives

Hamilton's [Hamilton, W.D., 1964. The genetical evolution of social behavior, I, II. J. Theor. Biol. 7, 1-52] kin-selection theory predicts that altruism will be greater with greater genetic overlap (degree of kinship) between giver and receiver. Kin may be identified in terms of social distance-the closer you feel to someone else, (a) the greater your genetic overlap with them should be, and (b) the more altruistic you should be toward them. The present experiment determined the amount of their own (hypothetical) monetary reward undergraduates were willing to forgo in order to give $75 to other people at various social distances. We found that (a) genetic relationship and (b) altruism varied inversely with social distance; the closer you feel to someone else, the closer their relation to you is likely to be, and the more altruistic you are likely to be toward them. However, even at the same social distance, participants were willing to forgo significantly more money for the benefit of relatives than for the benefit of non-relatives. These results are consistent with kin-selection theory and imply that altruism is determined by factors in addition to social distance.     

Altruism in networks: the effect of connections

Why are individuals altruistic to their friends? Theory suggests that individual, relationship and network factors will all influence the levels of altruism; but to date, the effects of social network structure have received relatively little attention. The present study uses a novel correlational design to test the prediction that an individual will be more altruistic to friends who are well-connected to the individual''s other friends. The result shows that, as predicted, even when controlling for a range of individual and relationship factors, the network factor (number of connections) makes a significant contribution to altruism, thus showing that individuals are more likely to be altruistic to better-connected members of their social networks. The implications of incorporating network structure into studies of altruism are discussed.     

Kin selection,social grooming and the removal of ectoparasites: A theoretical investigation

This paper considers how individuals should apportion their altruism among their relatives, with particular reference to social grooming in primates. It is concluded that there are no good reasons to expect an altruist to deploy its altruism among other individuals in proportion to its coefficients of relatedness to them. Various factors may cause an individual to be altruistic not just to its closest relative. One factor which is probably of widespread importance is when altruism reaches a point of diminishing returns, so that an increase in aid given is not accompanied by a proportional increase in benefit received. Quantitative predictions are made for social grooming with special reference to its possible function of ectoparasite removal.     

From reciprocity to unconditional altruism through signalling benefits

Cooperation among genetically unrelated individuals is commonly explained by the potential for future reciprocity or by the risk of being punished by group members. However, unconditional altruism is more difficult to explain. We demonstrate that unconditional altruism can evolve as a costly signal of individual quality (i.e. a handicap) as a consequence of reciprocal altruism. This is because the emergent correlation between altruism and individual quality in reciprocity games can facilitate the use of altruism as a quality indicator in a much wider context, outside the reciprocity game, thus affecting its further evolution through signalling benefits. Our model, based on multitype evolutionary game theory shows that, when the additive signalling benefit of donating help exceeds the cost for only some individuals (of high-quality state) but not for others (of low-quality state), the population possesses an evolutionarily stable strategy (ESS) profile wherein high-quality individuals cooperate unconditionally while low-quality individuals defect or play tit-for-tat (TfT). Hence, as predicted by Zahavi's handicap model, signalling benefits of altruistic acts can establish a stable generosity by high-quality individuals that no longer depends on the probability of future reciprocation or punishment.     

Origins of altruism diversity I: the diverse ecological roles of altruistic strategies and their evolutionary responses to local competition

Nature abounds with a rich variety of altruistic strategies, including public resource enhancement, resource provisioning, communal foraging, alarm calling, and nest defense. Yet, despite their vastly different ecological roles, current theory typically treats diverse altruistic traits as being favored under the same general conditions. Here, we introduce greater ecological realism into social evolution theory and find evidence of at least four distinct modes of altruism. Contrary to existing theory, we find that altruistic traits contributing to "resource-enhancement" (e.g., siderophore production, provisioning, agriculture) and "resource-efficiency" (e.g., pack hunting, communication) are most strongly favored when there is strong local competition. These resource-based modes of helping are "K-strategies" that increase a social group's growth yield, and should characterize species with scarce resources and/or high local crowding caused by low mortality, high fecundity, and/or mortality occurring late in the process of resource-acquisition. The opposite conditions, namely weak local competition (abundant resource, low crowding), favor survival (e.g., nest defense) and fecundity (e.g., nurse workers) altruism, which are "r-strategies" that increase a social group's growth rate. We find that survival altruism is uniquely favored by a novel evolutionary force that we call "sunk cost selection." Sunk cost selection favors helping that prevents resources from being wasted on individuals destined to die before reproduction. Our results contribute to explaining the observed natural diversity of altruistic strategies, reveal the necessary connection between the evolution and the ecology of sociality, and correct the widespread but inaccurate view that local competition uniformly impedes the evolution of altruism.     

Not only states but traits — Humans can identify permanent altruistic dispositions in 20 s

Humans behave altruistically in one-shot interactions under total anonymity. In search of explanations for such behavior, it has been argued that at least some individuals have a general tendency to behave altruistically independent of profitability. In fact, a stable altruistic trait would be adaptive if it were recognizable. Then, altruists could choose each other in order to retain benefits through mutual cooperation. Previous research has shown that individuals can predict the degree of altruistic behavior of strangers by reading signs of emotions evoked in significant social decisions. However, the identification of benevolent emotional states is no guarantee of the existence of permanent altruistic traits, though permanent traits are the preferable criterion for selection of good interaction partners. In this study, we tested whether individuals are able to identify altruistic traits. Judges watched 20-s silent video clips of unacquainted target persons and were asked to estimate the behavior of these target persons in a money-sharing task. As the videotapes of the target persons had been recorded in a setting unrelated to altruistic behavior, the judges could not base their estimates on situational cues related to the money-sharing task but instead had to draw on stable signals of altruism. Estimates were significantly better than chance, indicating that individuals can identify permanent altruistic traits in others. As this mechanism raises opportunities for selective interactions between altruists, our findings are discussed with respect to their relevance for explaining the evolution of altruism through assortment.     

Relatedness and altruism in Polistes wasps

Genetic relatedness is expected to play a crucial role in theevolution of altruistic behaviors such as worker behavior inthe social insects. If individuals sacrifice their own reproduction,then the genes for this sacrifice will be lost unless theseindividuals aid the reproduction of others who share the genes.This leads to the prediction that altruism should be most commonin species with high relatedness among potential beneficiaries.Here we report an attempt to test for such an association. Weestimated both the incidence of altruism and the relatednessto potential beneficiaries in foundresses of seven species ofpaper wasps. The predicted positive correlation was not found,and we conclude that factors other than relatedness are moreimportant in determining interspecific differences in the incidenceof altruism.     

Reproductive skew can provide a net advantage in both conditional and unconditional social interactions

We revisit a model for the evolution of costly social behaviour in the presence of reproductive skew. The model population is structured into groups, and reproductive skew is captured by assuming individuals adopt one of two social roles (dominant/subordinate). Unlike previous work, we adopt an ultimate perspective by tracking a mutant allele over the entire course of an invasion. Our main analysis applies the theory of branching processes, but a parallel analysis using the inclusive-fitness approach is also provided. Our first two results are modifications of known inequalities describing selective advantages for behaviours expressed conditional upon social status. We find that altruistic subordinate individuals are favoured more readily than previously thought; spiteful dominant individuals, however, are favoured less readily. Secondly, we identify the condition under which unconditional altruism (performed by both dominant and subordinate) will be adaptive. Our third main result shows that increasing the strength of selection can also change the range of parameters over which costly social behaviours are favoured. We find that stronger selection makes it relatively easier for subordinate altruism to emerge, but more difficult for dominant spite and unconditional altruism to occur. We discuss the possible implications of our results for human social evolution.     

Reciprocal altruism in birds: A critical review

Many proposed examples of reciprocal altruism are either misidentified or involve questionable assumptions concerning the costs and benefits accruing to the interactors. Waltz's (Am. Nat. 118: 588–592, 1981) definition of reciprocal altruism as an interaction in which “one individual aids another in anticipation that the recipient will return the favor benefiting the actor in the future” is not sufficiently restrictive: there must also be a direct fitness cost to the individual performing the original beneficent act that is less than the fitness benefit received when the act is reciprocated (again at a cost) by the second individual.Several recurring problems in identifying potential examples of reciprocal altruism are discussed, including the assumption that restraint is an act of altruism and the misclassification of “generational mutualisms,” in which individuals helping to raise young are “repaid” one generation later by the offspring they assisted in raising. No definite case of reciprocal altruism is currently known in birds, but examples in which this phenomenon may be involved include helping behavior in a few cooperative breeders and communal feeding in several taxa including gulls, jays, and juncos.     

Is sociality driven by the costs of dispersal or the benefits of philopatry? A role for kin-discrimination mechanisms

The role of ecological constraints in promoting sociality is currently much debated. Using a direct-fitness approach, we show this role to depend on the kin-discrimination mechanisms underlying social interactions. Altruism cannot evolve under spatially based discrimination, unless ecological constraints prevent complete dispersal. Increasing constraints enhances both the proportion of philopatric (and thereby altruistic) individuals and the level of altruistic investments conceded in pairwise interactions. Familiarity-based discrimination, by contrast, allows philopatry and altruism to evolve at significant levels even in the absence of ecological constraints. Increasing constraints further enhances the proportion of philopatric (and thereby altruistic) individuals but not the level of altruism conceded. Ecological constraints are thus more likely to affect social evolution in species in which restricted cognitive abilities, large group size, and/or limited period of associative learning force investments to be made on the basis of spatial cues.     

Kin selection in human populations: theory reconsidered

Past considerations of kin selection have assumed a dyadic fitness exchange relationship between altruist and recipient. This approach does not account for all alleles affected by altruistic behavior. This can be corrected by focusing on matings rather than on individuals. I present a model that tries to account for fitness changes resulting from altruistic acts, not only for the altruist and recipient but also for their spouses, in an evolving population. Results from this model indicate that Hamilton's rule fails to predict when the altruism allele will increase in frequency and, more important, suggest that kin selection can, at most, account for low levels of a gene for altruism but only if fairly extreme conditions are met.     

Is prospective altruist-detection an evolved solution to the adaptive problem of subtle cheating in cooperative ventures? Supportive evidence using the Wason selection task

Reciprocal altruism in humans may be made possible in part by the existence of information processing mechanisms for the detection of overt cheating. However, cheating may not always be readily detectable due to the division of labor. Subtle cheating poses a serious problem for the evolution of altruism. This article argues that subtle cheating may have exerted selective pressures on early hominids to be sensitive to information regarding the genuineness of an altruistic act. In two experiments, subjects were required to complete Wason selection tasks designed to allow for the detection of altruism. Performance on the altruist-detection tasks was compared to performance on control Wason selection tasks (Experiment 1) and to performance on control and cheater detection tasks (Experiment 2). Participants were significantly better at solving cheater-detection and altruist-detection versions compared to control versions of the problems, and there was no significant difference between altruist-detection and cheater-detection. Results are discussed in relation to recent conceptual models for the evolution of altruism. Specifically, it is argued that non-kin altruism may be an evolutionarily stable strategy if altruists can detect one another and form mutually beneficial social support networks.     

Models for alarm call behaviour

The evolution of alarm call behaviour under individual selection is studied. Four mathematical models of increasing complexity are proposed and analysed. Theoretical conditions for the evolution of “selfish”, “mutualistic”, “altruistic” or “spiteful” alarm calls are established. The models indicate that the hypotheses of benefits of retaining group members or avoiding group detection are not sufficient to explain the evolution of alarm call behaviour, but serve as a complementary factor to facilitate its evolution in most cases. It is hypothesized that the evolution of alarm calls between non-kin should evolve probably when calls are mutualistic, mildly altruistic and there are beneficial group size effects against predation.     

Monetary exchanges with nieces and nephews: a comparison of Samoan men,women, and fa'afafine

Androphilia refers to sexual attraction and arousal to adult males, whereas gynephilia refers to sexual attraction and arousal to adult females. The kin selection hypothesis for male androphilia suggests that androphilic males have been selected to act as “helpers-in-the-nest,” caring for nieces and nephews and, by extension, increasing their indirect fitness. Previous research has demonstrated that Samoan male androphiles (known locally as fa'afafine) exhibit significantly higher altruistic tendencies toward nieces and nephews compared to Samoan women and gynephilic men. Elevated avuncular tendencies must translate into real-world avuncular behavior if they are to have any impact on the fitness of nieces and nephews and the uncles themselves. The present study examined whether Samoan fa'afafine exhibit higher altruistic behavior toward nieces and nephews compared to women and gynephilic men. We used money given to, and received from, oldest and youngest siblings' sons and daughters as a behavioral assay of kin altruism. Compared to women and gynephilic men, fa'afafine gave significantly more money to their youngest siblings' daughters. No group differences were observed for money received from nieces and/or nephews. There were no correlations between number of children parented and monetary exchanges with the niece and nephew categories examined, suggesting that childlessness cannot account for why fa'afafine give more money to their youngest siblings' daughters. These findings are consistent with the kin selection hypothesis for male androphilia.     

Models of the evolution of altruism

There are two ways of calculating the spread of a gene for altruism. One, originally proposed by Hamilton, is to allow for the effects of the gene on the survival and reproduction of collateral relatives of the individual carrying it (i.e., “inclusive fitness”); this leads to the condition k > 1/r for the spread of the gene, where k is a benefit/cost ratio. The other is to count only the direct offspring of a carrier, but to allow for the altruistic acts performed toward the carrier by its relatives (“neighbour modulated fitness” or “personal fitness”). A recent personal fitness model (L. L. Cavalli Sforza and M. W. Feldman, 1978, Theor. Pop. Biol.14, 268–280) analyses parent-offspring and sib-sib altruism and concludes that k > 1/r is applicable only when fitness components are combined additively. The present paper analyses some simple models in which the phenotypic effects are carefully specified. It is concluded that it is sometimes, but not always, appropriate to combine fitness components additively. The relative roles of inclusive and personal fitness models are compared. The former have the virtue of being easier to think about in causal terms; and the latter of incorporating the evolution of altruism into the corpus of population genetics as an example of frequency-dependent selection.