Hamilton's rule and the causes of social evolution

Hamilton''s rule is a central theorem of inclusive fitness (kin selection) theory and predicts that social behaviour evolves under specific combinations of relatedness, benefit and cost. This review provides evidence for Hamilton''s rule by presenting novel syntheses of results from two kinds of study in diverse taxa, including cooperatively breeding birds and mammals and eusocial insects. These are, first, studies that empirically parametrize Hamilton''s rule in natural populations and, second, comparative phylogenetic analyses of the genetic, life-history and ecological correlates of sociality. Studies parametrizing Hamilton''s rule are not rare and demonstrate quantitatively that (i) altruism (net loss of direct fitness) occurs even when sociality is facultative, (ii) in most cases, altruism is under positive selection via indirect fitness benefits that exceed direct fitness costs and (iii) social behaviour commonly generates indirect benefits by enhancing the productivity or survivorship of kin. Comparative phylogenetic analyses show that cooperative breeding and eusociality are promoted by (i) high relatedness and monogamy and, potentially, by (ii) life-history factors facilitating family structure and high benefits of helping and (iii) ecological factors generating low costs of social behaviour. Overall, the focal studies strongly confirm the predictions of Hamilton''s rule regarding conditions for social evolution and their causes.     

Social semantics: how useful has group selection been?

In our social semantics review (J. Evol. Biol., 2007, 415–432), we discussed some of the misconceptions and sources of confusion associated with group selection. Wilson (2007, this issue) claims that we made three errors regarding group selection. Here, we aim to expand upon the relevant points from our review in order to refute this claim. The last 45 years of research provide clear evidence of the relative use of the kin and group selection approaches. Kin selection methodologies are more tractable, allowing the construction of models that can be applied more easily to specific biological examples, including those chosen by Wilson to illustrate the utility of the group selection approach. In contrast, the group selection approach is not only less useful, but also appears to frequently have negative consequences by fostering confusion that leads to wasted effort. More generally, kin selection theory allows the construction of a unified conceptual overview that can be applied across all taxa, whereas there is no formal theory of group selection.     

Quantitative genetic versions of Hamilton's rule with empirical applications

Hamilton''s theory of inclusive fitness revolutionized our understanding of the evolution of social interactions. Surprisingly, an incorporation of Hamilton''s perspective into the quantitative genetic theory of phenotypic evolution has been slow, despite the popularity of quantitative genetics in evolutionary studies. Here, we discuss several versions of Hamilton''s rule for social evolution from a quantitative genetic perspective, emphasizing its utility in empirical applications. Although evolutionary quantitative genetics offers methods to measure each of the critical parameters of Hamilton''s rule, empirical work has lagged behind theory. In particular, we lack studies of selection on altruistic traits in the wild. Fitness costs and benefits of altruism can be estimated using a simple extension of phenotypic selection analysis that incorporates the traits of social interactants. We also discuss the importance of considering the genetic influence of the social environment, or indirect genetic effects (IGEs), in the context of Hamilton''s rule. Research in social evolution has generated an extensive body of empirical work focusing—with good reason—almost solely on relatedness. We argue that quantifying the roles of social and non-social components of selection and IGEs, in addition to relatedness, is now timely and should provide unique additional insights into social evolution.     

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.     

Nepotistic cooperation in non-human primate groups

Darwin was struck by the many similarities between humans and other primates and believed that these similarities were the product of common ancestry. He would be even more impressed by the similarities if he had known what we have learned about primates over the last 50 years. Genetic kinship has emerged as the primary organizing force in the evolution of primate social organization and the patterning of social behaviour in non-human primate groups. There are pronounced nepotistic biases across the primate order, from tiny grey mouse lemurs (Microcebus murinus) that forage alone at night but cluster with relatives to sleep during the day, to cooperatively breeding marmosets that rely on closely related helpers to rear their young, rhesus macaque (Macaca mulatta) females who acquire their mother''s rank and form strict matrilineal dominance hierarchies, male howler monkeys that help their sons maintain access to groups of females and male chimpanzees (Pan troglodytes) that form lasting relationships with their brothers. As more evidence of nepotism has accumulated, important questions about the evolutionary processes underlying these kin biases have been raised. Although kin selection predicts that altruism will be biased in favour of relatives, it is difficult to assess whether primates actually conform to predictions derived from Hamilton''s rule: br > c. In addition, other mechanisms, including contingent reciprocity and mutualism, could contribute to the nepotistic biases observed in non-human primate groups. There are good reasons to suspect that these processes may complement the effects of kin selection and amplify the extent of nepotistic biases in behaviour.     

Social semantics: toward a genuine pluralism in the study of social behaviour

Pluralism is the coexistence of equivalent theoretical frameworks, either because they are historically entrenched or because they achieve separate insights by viewing the same process in different ways. A recent article by West et al. [Journal of Evolutionary Biology (2007) vol. 20, 415-432] attempts to classify the many equivalent frameworks that have been developed to study the evolution of social behaviour. This article addresses shortcomings in the West et al.'s article, especially with respect to multilevel selection, in a common effort to maximize the benefits of pluralism while minimizing the semantic costs.     

Helping in cooperatively breeding long-tailed tits: a test of Hamilton's rule

Inclusive fitness theory provides the conceptual framework for our current understanding of social evolution, and empirical studies suggest that kin selection is a critical process in the evolution of animal sociality. A key prediction of inclusive fitness theory is that altruistic behaviour evolves when the costs incurred by an altruist (c) are outweighed by the benefit to the recipient (b), weighted by the relatedness of altruist to recipient (r), i.e. Hamilton''s rule rb > c. Despite its central importance in social evolution theory, there have been relatively few empirical tests of Hamilton''s rule, and hardly any among cooperatively breeding vertebrates, leading some authors to question its utility. Here, we use data from a long-term study of cooperatively breeding long-tailed tits Aegithalos caudatus to examine whether helping behaviour satisfies Hamilton''s condition for the evolution of altruism. We show that helpers are altruistic because they incur survival costs through the provision of alloparental care for offspring. However, they also accrue substantial benefits through increased survival of related breeders and offspring, and despite the low average relatedness of helpers to recipients, these benefits of helping outweigh the costs incurred. We conclude that Hamilton''s rule for the evolution of altruistic helping behaviour is satisfied in this species.     

Stable public goods cooperation and dynamic social interactions in yeast

Despite long-standing theoretical interest in the evolution of cooperation, empirical data on the evolutionary dynamics of cooperative traits remain limited. Here, we investigate the evolutionary dynamics of a simple public goods cooperative trait, invertase secretion, using a long-term selection experiment in Saccharomyces cerevisiae. We show that average investment in cooperation remains essentially constant over a period of hundreds of generations in viscous populations with high relatedness. Average cooperation remains constant despite transient local selection for high and low levels of cooperation that generate dynamic social interactions. Natural populations of yeast show similar variation in social strategies, which is consistent with the existence of similar selective pressures on public goods cooperation in nature.     

Kinship,parental manipulation and evolutionary origins of eusociality

One of the hallmarks of eusociality is that workers forego their own reproduction to assist their mother in raising siblings. This seemingly altruistic behaviour may benefit workers if gains in indirect fitness from rearing siblings outweigh the loss of direct fitness. If worker presence is advantageous to mothers, however, eusociality may evolve without net benefits to workers. Indirect fitness benefits are often cited as evidence for the importance of inclusive fitness in eusociality, but have rarely been measured in natural populations. We compared inclusive fitness of alternative social strategies in the tropical sweat bee, Megalopta genalis, for which eusociality is optional. Our results show that workers have significantly lower inclusive fitness than females that found their own nests. In mathematical simulations based on M. genalis field data, eusociality cannot evolve with reduced intra-nest relatedness. The simulated distribution of alternative social strategies matched observed distributions of M. genalis social strategies when helping behaviour was simulated as the result of maternal manipulation, but not as worker altruism. Thus, eusociality in M. genalis is best explained through kin selection, but the underlying mechanism is likely maternal manipulation.     

Benefits of foundress associations in the paper wasp Polistes dominulus: increased productivity and survival, but no assurance of fitness returns

Successful Polistes dominulus nests can be started by one ormore nest founding queens (foundresses). Consequently, thereis much interest in the specific benefits that induce cooperationamong foundresses. Here, we experimentally demonstrate one majorbenefit of cooperation, namely that multiple foundresses increasecolony productivity. This increase is close to the value predictedby subtracting the productivity of undisturbed single-foundresscolonies from the productivity of undisturbed multiple-foundresscolonies. However, we found no evidence that an associatingfoundress' contribution to colony growth is preserved if shedisappears (assured fitness returns). Our correlational datasuggest that cooperation provides survival benefits, multiple-foundresscolonies are more likely to survive to produce offspring thanare single-foundress colonies, and individual foundresses inmultiple-foundress groups are less likely to disappear beforeworker emergence than foundresses nesting alone. Therefore,association provides substantial productivity and survival benefitsfor cooperating foundresses.     

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.     

Within-host parasite cooperation and the evolution of virulence

Infections by multiple genotypes are common in nature and are known to select for higher levels of virulence for some parasites. When parasites produce public goods (PGs) within the host, such co-infections have been predicted to select for lower levels of virulence. However, this prediction is based on simplifying assumptions regarding epidemiological feedbacks on the multiplicity of infections (MOI). Here, we analyse the case of parasites producing a PG (for example, siderophore-producing bacteria) using a nested model that ties together within-host and epidemiological processes. We find that the prediction that co-infection should select for less virulent strains for PG-producing parasites is only valid if both parasite transmission and virulence are linear functions of parasite density. If there is a trade-off relationship such that virulence increases more rapidly than transmission, or if virulence also depends on the total amount of PGs produced, then more complex relationships between virulence and the MOI are predicted. Our results reveal that explicitly taking into account the distribution of parasite strains among hosts could help better understand the selective pressures faced by parasites at the population level.     

Fisher’s fundamental theorem of inclusive fitness and the change in fitness due to natural selection when conspecifics interact

Competition and cooperation is fundamental to evolution by natural selection, both in animals and plants. Here, I investigate the consequences of such interactions for response in fitness due to natural selection. I provide quantitative genetic expressions for heritable variance and response in fitness due to natural selection when conspecifics interact. Results show that interactions among conspecifics generate extra heritable variance in fitness, and that interacting with kin is the key to evolutionary success because it translates the extra heritable variance into response in fitness. This work also unifies Fisher’s fundamental theorem of natural selection (FTNS) and Hamilton’s inclusive fitness (IF). The FTNS implies that natural selection maximizes fitness, whereas Hamilton proposed maximization of IF. This work shows that the FTNS describes the increase in IF, rather than direct fitness, at a rate equal to the additive genetic variance in fitness. Thus, Hamilton’s IF and Fisher’s FTNS both describe the maximization of IF.     

The evolution of cooperation and altruism--a general framework and a classification of models

One of the enduring puzzles in biology and the social sciences is the origin and persistence of intraspecific cooperation and altruism in humans and other species. Hundreds of theoretical models have been proposed and there is much confusion about the relationship between these models. To clarify the situation, we developed a synthetic conceptual framework that delineates the conditions necessary for the evolution of altruism and cooperation. We show that at least one of the four following conditions needs to be fulfilled: direct benefits to the focal individual performing a cooperative act; direct or indirect information allowing a better than random guess about whether a given individual will behave cooperatively in repeated reciprocal interactions; preferential interactions between related individuals; and genetic correlation between genes coding for altruism and phenotypic traits that can be identified. When one or more of these conditions are met, altruism or cooperation can evolve if the cost-to-benefit ratio of altruistic and cooperative acts is greater than a threshold value. The cost-to-benefit ratio can be altered by coercion, punishment and policing which therefore act as mechanisms facilitating the evolution of altruism and cooperation. All the models proposed so far are explicitly or implicitly built on these general principles, allowing us to classify them into four general categories.     

Sex-biased dispersal, haplodiploidy and the evolution of helping in social insects

In his famous haplodiploidy hypothesis, W. D. Hamilton proposed that high sister-sister relatedness facilitates the evolution of kin-selected reproductive altruism among Hymenopteran females. Subsequent analyses, however, suggested that haplodiploidy cannot promote altruism unless altruists capitalize on relatedness asymmetries by helping to raise offspring whose sex ratio is more female-biased than the population at large. Here, we show that haplodiploidy is in fact more favourable than is diploidy to the evolution of reproductive altruism on the part of females, provided only that dispersal is male-biased (no sex-ratio bias or active kin discrimination is required). The effect is strong, and applies to the evolution both of sterile female helpers and of helping among breeding females. Moreover, a review of existing data suggests that female philopatry and non-local mating are widespread among nest-building Hymenoptera. We thus conclude that Hamilton was correct in his claim that 'family relationships in the Hymenoptera are potentially very favourable to the evolution of reproductive altruism'.     

The validity and value of inclusive fitness theory

Social evolution is a central topic in evolutionary biology, with the evolution of eusociality (societies with altruistic, non-reproductive helpers) representing a long-standing evolutionary conundrum. Recent critiques have questioned the validity of the leading theory for explaining social evolution and eusociality, namely inclusive fitness (kin selection) theory. I review recent and past literature to argue that these critiques do not succeed. Inclusive fitness theory has added fundamental insights to natural selection theory. These are the realization that selection on a gene for social behaviour depends on its effects on co-bearers, the explanation of social behaviours as unalike as altruism and selfishness using the same underlying parameters, and the explanation of within-group conflict in terms of non-coinciding inclusive fitness optima. A proposed alternative theory for eusocial evolution assumes mistakenly that workers' interests are subordinate to the queen's, contains no new elements and fails to make novel predictions. The haplodiploidy hypothesis has yet to be rigorously tested and positive relatedness within diploid eusocial societies supports inclusive fitness theory. The theory has made unique, falsifiable predictions that have been confirmed, and its evidence base is extensive and robust. Hence, inclusive fitness theory deserves to keep its position as the leading theory for social evolution.