Primate Nepotism: What is the Explanatory Value of Kin Selection?

Kin selection theory (KS) is widely invoked to account for the preferential treatment of kin—nepotism—in primate societies. Because this idea is so pervasive the role of KS is often unquestioned and optional mechanisms are often ignored. I first examine the potential role of some other nepotism-generating mechanisms by concentrating on the effect of the proximity correlate of matrilineal kinship. This correlate of kinship may bias the development of mutually selfish interactions among relatives—kin-biased mutualism—and that of reciprocally altruistic interactions—kin-biased reciprocal altruism—two mechanisms that have been given little weight compared to KS and whose impact on the evolution of nepotism is therefore unknown. However, these two options to KS cannot account for the existence of unilaterally altruistic interactions among kin, which provide, therefore, the best type of evidence to test KS. But such evidence is difficult to obtain because many behaviors considered altruistic may in fact be selfish, and because kin altruism is seldom unilateral; it is most often bilateral, as expected by reciprocal altruism theory. For these reasons, one should be extremely cautious before equating nepotism exclusively with KS. Next, I examine the predictions of KS regarding the deployment of altruism according to degree of kinship by considering, in addition to the variables of Hamilton's equation, the duration of behaviors, the size of kin classes and their differential availability. In general, altruism is expected to be allocated at a fairly constant rate among kin categories and to drop markedly past the degree of relatedness beyond which altruism is no more profitable. Very little data allow one to test conclusively this prediction, as well as some other significant predictions. Overall, there is ample evidence for the role of KS in shaping mother-offspring interactions in various areas. But the evidence for kin-selected altruism beyond the mother-offspring bond (r < 0.5), though qualitatively solid, is much less abundant. Kin altruism drops markedly beyond r = 0.25 (half-siblings and grandmother-grandoffspring dyads).     

Kin recognition and the evolution of altruism

In 1964, Hamilton formalized the idea of kin selection to explain the evolution of altruistic behaviours. Since then, numerous examples from a diverse array of taxa have shown that seemingly altruistic actions towards close relatives are a common phenomenon. Although many species use kin recognition to direct altruistic behaviours preferentially towards relatives, this important aspect of social biology is less well understood theoretically. I extend Hamilton's classic work by defining the conditions for the evolution of kin-directed altruism when recognizers are permitted to make acceptance (type I) and rejection (type II) errors in the identification of social partners with respect to kinship. The effect of errors in recognition on the evolution of kin-directed altruism depends on whether the population initially consists of unconditional altruists or non-altruists (i.e. alternative forms of non-recognizers). Factors affecting the level of these error rates themselves, their evolution and their long-term stability are discussed.     

Competitive altruism: from reciprocity to the handicap principle

Current work on cooperation is focused on the theory of reciprocal altruism. However, reciprocity is just one way of getting a return on an investment in altruism and is difficult to apply to many examples. Reciprocity theory addresses how animals respond dynamically to others so as to cooperate without being exploited. I discuss how introducing differences in individual generosity together with partner choice into models of reciprocity can lead to an escalation in altruistic behaviour. Individuals may compete for the most altruistic partners and non-altruists may become ostracized. I refer to this phenomenon as competitive altruism and propose that it can represent a move away from the dynamic responsiveness of reciprocity. Altruism may be rewarded in kind, but rewards may be indirectly accrued or may not involve the return of altruism at all, for example if altruists tend to be chosen as mates. This variety makes the idea of competitive altruism relevant to behaviours which cannot be explained by reciprocity. I consider whether altruism might act as a signal of quality, as proposed by the handicap principle. I suggest that altruistic acts could make particularly effective signals because of the inherent benefits to receivers. I consider how reciprocity and competitive altruism are related and how they may be distinguished.     

Tag-based indirect reciprocity by incomplete social information

Evolution of altruistic behaviour in interacting individuals is accounted for by, for example, kin selection, direct reciprocity, spatially limited interaction and indirect reciprocity. Real social agents, particularly humans, often take actions based on similarity between themselves and others. Although tag-based indirect reciprocity in which altruism occurs exclusively among similar flocks is a natural expectation, its mechanism has not really been established. We propose a model of tag-based indirect reciprocity by assuming that each player may note strategies of others. We show that tag-based altruism can evolve to eradicate other strategies, including unconditional defectors for various initial strategy configurations and parameter sets. A prerequisite for altruism is that the strategy is sometimes, but not always, visible to others. Without visibility of strategies, policing does not take place and defection is optimal. With perfect visibility, what a player does is always witnessed by others and cooperation is optimal. In the intermediate regime, discriminators based on tag proximity, rather than mixture of generous players and defectors, are most likely to evolve. In this situation, altruism is realized based on homophily in which players are exclusively good to similar others.     

The evolution of reciprocal sharing

Genetical models of the evolution of reciprocal altruism (as distinct from cooperation, mutualism, or nepotism) have difficulty explaining the initial establishment of an altruist gene in a selfish deme. Though potential mechanisms have been suggested, there is an alternative: much “altruistic” behavior may in fact be purely selfish in origin and consequently reciprocity need not be invoked to provide a selective benefit to the actor. Sharing and helping are fundamentally different behavior categories and should not be confused. Patterns of resource sharing in chimpanzees correspond to predictions made by a selfish model but not to those of a reciprocal altruism model, and many observations of human gift exchange are consistent with the selfish, but not the altruistic, model. This suggests that presumed hominid meat exchange may have been the result of competition, not altruism or even cooperation, and that evolutionary models of “altruistic” behavior should be treated with caution.     

Effects of Relatedness,Dominance, Age,and Association on Reciprocal Allogrooming by Captive Impala

Wild impala display a highly reciprocal allogrooming system that, by virtue of its frequency and high degree of reciprocity, is unique among ungulates. A herd of 35 free-ranging captive impala provided opportunity to examine the degree of reciprocity of allogrooming exchanges and the influence of relatedness, dominance, age and association on partner preferences and distribution of grooming between allogrooming partners. As in wild impala, the exchange of allogrooming bouts in the captive impala was highly reciprocal regardless of partners. Kinship and dominance had no influence on partner preference or distribution of grooming between partners. Although mothers showed a significant preference to allogroom with their unweaned offspring, this preference practically disappeared with older offspring. Age-mates (no greater than 6 mo apart) tended to associate with one another and spatial proximity was positively correlated with grooming partner preference. It was not clear whether impala actively sought out age-mates for grooming, or randomly chose grooming partners from nearby age-mates. The failure to find a role for kinship and dominance is counter to what has generally been found in most Old World terrestrial primate studies. The absence of pronounced social influences, coupled with the known effectiveness of grooming in removing ectoparasites, suggest that a utilitarian role, especially removal of ticks, is an important function of the impala reciprocal allogrooming system.     

Evolution of indirect reciprocity by social information: the role of trust and reputation in evolution of altruism

The complexity of human's cooperative behavior cannot be fully explained by theories of kin selection and group selection. If reciprocal altruism is to provide an explanation for altruistic behavior, it would have to depart from direct reciprocity, which requires dyads of individuals to interact repeatedly. For indirect reciprocity to rationalize cooperation among genetically unrelated or even culturally dissimilar individuals, information about the reputation of individuals must be assessed and propagated in a population. Here, we propose a new framework for the evolution of indirect reciprocity by social information: information selectively retrieved from and propagated through dynamically evolving networks of friends and acquaintances. We show that for indirect reciprocity to be evolutionarily stable, the differential probability of trusting and helping a reputable individual over a disreputable individual, at a point in time, must exceed the cost-to-benefit ratio of the altruistic act. In other words, the benefit received by the trustworthy must out-weigh the cost of helping the untrustworthy.     

Grooming reciprocation among female primates: a meta-analysis

The theory of reciprocal altruism offers an explanation for the evolution of altruistic behaviours among unrelated animals. Among primates, grooming is one of the most common altruistic behaviours. Primates have been suggested to exchange grooming both for itself and for rank-related benefits. While previous meta-analyses have shown that they direct their grooming up the hierarchy and exchange it for agonistic support, no comprehensive evaluation of grooming reciprocation has been made. Here we report on a meta-analysis of grooming reciprocation among female primates based on 48 social groups belonging to 22 different species and 12 genera. The results of this meta-analysis showed that female primates groom preferentially those group mates that groom them most. To the extent allowed by the availability of kinship data, this result holds true when controlling for maternal kinship. These results, together with previous findings, suggest that primates are indeed able to exchange grooming both for itself and for different rank-related benefits.     

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.     

"Runaway" social evolution: reinforcing selection for inbreeding and altruism.

Kin selection theory predicts that altruistic behaviors, those that decrease the fitness of the individual performing the behavior but increase the fitness of the recipient, can increase in frequency if the individuals interacting are closely related. Several studies have shown that inbreeding therefore generally increases the effectiveness of kin selection when fitnesses are linear, additive functions of the number of altruists in the family, although with extreme forms of altruism, inbreeding can actually retard the evolution of altruism. These models assume that a constant proportion of the population mates at random and a constant proportion practices some form of inbreeding. In order to investigate the effect of inbreeding on the evolution of altruistic behavior when the mating structure is allowed to evolve, we examined a two-locus model by computer simulation of a diploid case and illustrated the important qualitative features by mathematical analysis of a haploid case. One locus determines an individual's propensity to perform altruistic social behavior and the second locus determines the probability that an individual will mate within its sibship. We assumed positive selection for altruism and no direct selection at the inbreeding locus. We observed that the altruistic allele and the inbreeding allele become positively associated, even when the initial conditions of the model assume independence between these loci. This linkage disequilibrium becomes established, because the altruistic allele increases more rapidly in the inbreeding segment of the population. This association subsequently results in indirect selection on the inbreeding locus. However, the dynamics of this model go beyond a simple "hitch-hiking" effect, because high levels of altruism lead to increased inbreeding, and high degrees of inbreeding accelerate the rate of change of the altruistic allele in the entire population. Thus, the dynamics of this model are similar to those of "runaway" sexual selection, with gene frequency change at the two loci interactively causing rapid evolutionary change.     

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.     

Environmentally induced responses co-opted for reproductive altruism

Reproductive altruism is an extreme form of altruism best typified by sterile castes in social insects and somatic cells in multicellular organisms. Although reproductive altruism is central to the evolution of multicellularity and eusociality, the mechanistic basis for the evolution of this behaviour is yet to be deciphered. Here, we report that the gene responsible for the permanent suppression of reproduction in the somatic cells of the multicellular green alga, Volvox carteri, evolved from a gene that in its unicellular relative, Chlamydomonas reinhardtii, is part of the general acclimation response to various environmental stress factors, which includes the temporary suppression of reproduction. Furthermore, we propose a model for the evolution of soma, in which by simulating the acclimation signal (i.e. a change in cellular redox status) in a developmental rather than environmental context, responses beneficial to a unicellular individual can be co-opted into an altruistic behaviour at the group level. The co-option of environmentally induced responses for reproductive altruism can contribute to the stability of this behaviour, as the loss of such responses would be costly for the individual. This hypothesis also predicts that temporally varying environments, which will select for more efficient acclimation responses, are likely to be more conducive to the evolution of reproductive altruism.     

Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection

From an evolutionary perspective, social behaviours are those which have fitness consequences for both the individual that performs the behaviour, and another individual. Over the last 43 years, a huge theoretical and empirical literature has developed on this topic. However, progress is often hindered by poor communication between scientists, with different people using the same term to mean different things, or different terms to mean the same thing. This can obscure what is biologically important, and what is not. The potential for such semantic confusion is greatest with interdisciplinary research. Our aim here is to address issues of semantic confusion that have arisen with research on the problem of cooperation. In particular, we: (i) discuss confusion over the terms kin selection, mutualism, mutual benefit, cooperation, altruism, reciprocal altruism, weak altruism, altruistic punishment, strong reciprocity, group selection and direct fitness; (ii) emphasize the need to distinguish between proximate (mechanism) and ultimate (survival value) explanations of behaviours. We draw examples from all areas, but especially recent work on humans and microbes.     

Strong reciprocity or strong ferocity? A population genetic view of the evolution of altruistic punishment

Strong reciprocity, defined as a predisposition to help others and to punish those that are not helping, has been proposed as a potent force leading to the evolution of cooperation and altruism. However, the conditions under which strong reciprocity might be favored are not clear. Here we investigate the selective pressure on strong reciprocity by letting both limited dispersal (i.e., spatial structure) and recombination between helping and punishment jointly determine the evolutionary dynamics of strong reciprocity. Our analytical model suggests that when helping and punishment are perfectly linked traits (no recombination occurring between them), strong reciprocity can spread even when the initial frequency of strong reciprocators is close to 0 in the population (i.e., a rare mutant can invade). By contrast, our results indicate that when recombination can occur between helping and punishment (i.e., both traits coevolve) and is stronger than selection, punishment is likely to invade a population of defectors only when it gives a direct fitness benefit to the actor. Overall, our results delineate the conditions under which strong reciprocity is selected for in a spatially structured population and highlight that the forces behind its evolution involves kinship (be it genetic or cultural).     

The evolution of generalized reciprocity on social interaction networks

Generalized reciprocity (help anyone, if helped by someone) is a minimal strategy capable of supporting cooperation between unrelated individuals. Its simplicity makes it an attractive model to explain the evolution of reciprocal altruism in animals that lack the information or cognitive skills needed for other types of reciprocity. Yet, generalized reciprocity is anonymous and thus defenseless against exploitation by defectors. Recognizing that animals hardly ever interact randomly, we investigate whether social network structure can mitigate this vulnerability. Our results show that heterogeneous interaction patterns strongly support the evolution of generalized reciprocity. The future probability of being rewarded for an altruistic act is inversely proportional to the average connectivity of the social network when cooperators are rare. Accordingly, sparse networks are conducive to the invasion of reciprocal altruism. Moreover, the evolutionary stability of cooperation is enhanced by a modular network structure. Communities of reciprocal altruists are protected against exploitation, because modularity increases the mean access time, that is, the average number of steps that it takes for a random walk on the network to reach a defector. Sparseness and community structure are characteristic properties of vertebrate social interaction patterns, as illustrated by network data from natural populations ranging from fish to primates.     

Altruism or solidarity? The motives for organ donation and two proposals

Proposals for increasing organ donation are often rejected as incompatible with altruistic motivation on the part of donors. This paper questions, on conceptual grounds, whether most organ donors really are altruistic. If we distinguish between altruism and solidarity--a more restricted form of other-concern, limited to members of a particular group--then most organ donors exhibit solidarity, rather than altruism. If organ donation really must be altruistic, then we have reasons to worry about the motives of existing donors. However, I argue that altruism is not necessary, because organ donation supplies important goods, whatever the motivation, and we can reject certain dubious motivations, such as financial profit, without insisting on altruism. Once solidaristic donation is accepted, certain reforms for increasing donation rates seem permissible. This paper considers two proposals. Firstly, it has been suggested that registered donors should receive priority for transplants. While this proposal appears based on a solidaristic norm of reciprocity, it is argued that such a scheme would be undesirable, since non-donors may contribute to society in other ways. The second proposal is that donors should be able to direct their organs towards recipients that they feel solidarity with. This is often held to be inconsistent with altruistic motivation, but most donation is not entirely undirected in the first place (for instance, donor organs usually go to co-nationals). While allowing directed donation would create a number of practical problems, such as preventing discrimination, there appears to be no reason in principle to reject it.     

Reciprocity explains food sharing in humans and other primates independent of kin selection and tolerated scrounging: a phylogenetic meta-analysis

Helping, i.e. behaviour increasing the fitness of others, can evolve when directed towards kin or reciprocating partners. These predictions have been tested in the context of food sharing both in human foragers and non-human primates. Here, we performed quantitative meta-analyses on 32 independent study populations to (i) test for overall effects of reciprocity on food sharing while controlling for alternative explanations, methodological biases, publication bias and phylogeny and (ii) compare the relative effects of reciprocity, kinship and tolerated scrounging, i.e. sharing owing to costs imposed by others. We found a significant overall weighted effect size for reciprocity of r = 0.20–0.48 for the most and least conservative measure, respectively. Effect sizes did not differ between humans and other primates, although there were species differences in in-kind reciprocity and trade. The relative effect of reciprocity in sharing was similar to those of kinship and tolerated scrounging. These results indicate a significant independent contribution of reciprocity to human and primate helping behaviour. Furthermore, similar effect sizes in humans and primates speak against cognitive constraints on reciprocity. This study is the first to use meta-analyses to quantify these effects on human helping and to directly compare humans and other primates.     

Donors to charity gain in both indirect reciprocity and political reputation

Darwinian evolution can explain human cooperative behaviour among non-kin by either direct or indirect reciprocity. In the latter case one does not expect a return for an altruistic act from the recipient as with direct reciprocity, but from another member of the social group. However, the widespread human behaviour of donating to poor people outside the social group, for example, to charity organizations, that are unlikely to reciprocate indirectly and thus are equivalent to defectors in the game is still an evolutionary puzzle. Here we show experimentally that donations made in public to a well-known relief organization resulted both in increased income (that the donors received from the members of their group) and in enhanced political reputation (they were elected to represent the interests of their group). Donations may thus function as an honest signal for one's social reliability.