Hamilton's legacy: kinship, cooperation and social tolerance in mammalian groups

Highlights

• W. D. Hamilton's (1964) kin selection theory has now inspired five decades of research.

• Inclusive benefits of short-lived social acts have been largely overlooked for social mammals.

• Kinship promotes associations and coalitions, but rarely tolerance in primates and nonprimates.

• Context-dependent costs (competition) and benefits (cooperation) are both important.

• Longitudinal data should be combined with new methods to elucidate lifetime fitness consequences.

In 1964, W. D. Hamilton proposed a novel solution to the long-standing evolutionary puzzle: why do individuals cooperate? Hamilton predicted that, if individuals possess the ability to discriminate on the basis of kinship, then they should gain inclusive fitness benefits by biasing helpful behaviour towards relatives and harmful behaviour away from them. The possibility that kin selection might favour social evolution has now inspired five decades of active research. Here, I synthesize this evidence for social mammals. First, I report on the methodological advances that allow for pedigree construction, and review the evidence for maternal and paternal kin discrimination. Second, I recognize that a substantial body of evidence for the evolution of cooperative breeding via kin selection exists, and then focus on the potential for kin selection to favour less well understood, yet equally salient, targets of selection: social partner choice, coalition formation and social tolerance (withholding aggression). I find that kin selection favours remarkably similar patterns of nepotism in primate and nonprimates with respect to these short-lived social acts. Although social alliances among maternal and paternal kin are common in mammalian societies, kinship largely fails to protect individuals from aggression. Thus, an individual's closest associates and allies, many of whom are kin, are most often an individual's closest competitors within mammalian social groups. Taken together, these findings highlight the value of Hamilton's holistic approach in simultaneously considering the direct benefits of competition and the indirect fitness benefits of cooperation. Despite major empirical advances since the inception of kin selection theory, future tests using newly available molecular and statistical methods in combination with longitudinal behavioural data are required to partition the relative contributions of direct and indirect fitness on the lifetime inclusive fitness. Such approaches will elucidate the relative influences of evolutionary and ecological forces favouring social evolution across the mammalian lineage of social mammals.