Joint evolution of multiple social traits: a kin selection analysis

General models of the evolution of cooperation, altruism and other social behaviours have focused almost entirely on single traits, whereas it is clear that social traits commonly interact. We develop a general kin-selection framework for the evolution of social behaviours in multiple dimensions. We show that whenever there are interactions among social traits new behaviours can emerge that are not predicted by one-dimensional analyses. For example, a prohibitively costly cooperative trait can ultimately be favoured owing to initial evolution in other (cheaper) social traits that in turn change the cost–benefit ratio of the original trait. To understand these behaviours, we use a two-dimensional stability criterion that can be viewed as an extension of Hamilton''s rule. Our principal example is the social dilemma posed by, first, the construction and, second, the exploitation of a shared public good. We find that, contrary to the separate one-dimensional analyses, evolutionary feedback between the two traits can cause an increase in the equilibrium level of selfish exploitation with increasing relatedness, while both social (production plus exploitation) and asocial (neither) strategies can be locally stable. Our results demonstrate the importance of emergent stability properties of multidimensional social dilemmas, as one-dimensional stability in all component dimensions can conceal multidimensional instability.     

The genetical theory of kin selection

Natural selection operates both directly, via the impact of a trait upon the individual's own fitness, and indirectly, via the impact of the trait upon the fitness of the individual's genetically related social partners. These effects are often framed in terms of Hamilton's rule, rb - c > 0, which provides the central result of social-evolution theory. However, a number of studies have questioned the generality of Hamilton's rule, suggesting that it requires restrictive assumptions. Here, we use Fisher's genetical paradigm to demonstrate the generality of Hamilton's rule and to clarify links between different studies. We show that confusion has arisen owing to researchers misidentifying model parameters with the b and c terms in Hamilton's rule, and misidentifying measures of genotypic similarity or genealogical relationship with the coefficient of genetic relatedness, r. More generally, we emphasize the need to distinguish between general kin-selection theory that forms the foundations of social evolution, and streamlined kin-selection methodology that is used to solve specific problems.     

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.     

The evolution of trans-generational altruism: kin selection meets niche construction

A cornerstone result of sociobiology states that limited dispersal can induce kin competition to offset the kin selected benefits of altruism. Several mechanisms have been proposed to circumvent this dilemma but all assume that actors and recipients of altruism interact during the same time period. Here, this assumption is relaxed and a model is developed where individuals express an altruistic act, which results in posthumously helping relatives living in the future. The analysis of this model suggests that kin selected benefits can then feedback on the evolution of the trait in a way that promotes altruistic helping at high rates under limited dispersal. The decoupling of kin competition and kin selected benefits results from the fact that by helping relatives living in the future, an actor is helping individuals that are not in direct competition with itself. A direct consequence is that behaviours which actors gain by reducing the common good of present and future generations can be opposed by kin selection. The present model integrates niche-constructing traits with kin selection theory and delineates demographic and ecological conditions under which altruism can be selected for; and conditions where the 'tragedy of the commons' can be reduced.     

Detecting kin selection at work using inclusive fitness

A recent model shows that altruism can evolve with limited migration and variable group sizes, and the authors claim that kin selection cannot provide a sufficient explanation of their results. It is demonstrated, using a recent reformulation of Hamilton's original arguments, that the model falls squarely within the scope of inclusive fitness theory, which furthermore shows how to calculate inclusive fitness and the relevant relatedness. A distinction is drawn between inclusive fitness, which is a method of analysing social behaviour; and kin selection, a process that operates through genetic similarity brought about by common ancestry, but not by assortation by genotype or by direct assessment of genetic similarity. The recent model is analysed, and it turns out that kin selection provides a sufficient explanation to considerable quantitative accuracy, contrary to the authors' claims. A parallel analysis is possible and would be illuminating for all models of social behaviour in which individuals' effects on each other's offspring numbers combine additively.     

The joint effects of kin, multilevel selection and indirect genetic effects on response to genetic selection

Kin and levels-of-selection models are common approaches for modelling social evolution. Indirect genetic effect (IGE) models represent a different approach, specifying social effects on trait values rather than fitness. We investigate the joint effect of relatedness, multilevel selection and IGEs on response to selection. We present a measure for the degree of multilevel selection, which is the natural partner of relatedness in expressions for response. Response depends on both relatedness and the degree of multilevel selection, rather than only one or the other factor. Moreover, response is symmetric in relatedness and the degree of multilevel selection, indicating that both factors have exactly the same effect. Without IGEs, the key parameter is the product of relatedness and the degree of multilevel selection. With IGEs, however, multilevel selection without relatedness can explain evolution of social traits. Thus, next to relatedness and multilevel selection, IGEs are a key element in the genetical theory of 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.     

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.     

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: 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.     

Selective pressures for accurate altruism targeting: evidence from digital evolution for difficult-to-test aspects of inclusive fitness theory

Inclusive fitness theory predicts that natural selection will favour altruist genes that are more accurate in targeting altruism only to copies of themselves. In this paper, we provide evidence from digital evolution in support of this prediction by competing multiple altruist-targeting mechanisms that vary in their accuracy in determining whether a potential target for altruism carries a copy of the altruist gene. We compete altruism-targeting mechanisms based on (i) kinship (kin targeting), (ii) genetic similarity at a level greater than that expected of kin (similarity targeting), and (iii) perfect knowledge of the presence of an altruist gene (green beard targeting). Natural selection always favoured the most accurate targeting mechanism available. Our investigations also revealed that evolution did not increase the altruism level when all green beard altruists used the same phenotypic marker. The green beard altruism levels stably increased only when mutations that changed the altruism level also changed the marker (e.g. beard colour), such that beard colour reliably indicated the altruism level. For kin- and similarity-targeting mechanisms, we found that evolution was able to stably adjust altruism levels. Our results confirm that natural selection favours altruist genes that are increasingly accurate in targeting altruism to only their copies. Our work also emphasizes that the concept of targeting accuracy must include both the presence of an altruist gene and the level of altruism it produces.     

Sex‐biased dispersal,kin selection and the evolution of sexual conflict

There is growing interest in resolving the curious disconnect between the fields of kin selection and sexual selection. Rankin's (2011, J. Evol. Biol. 24 , 71–81) theoretical study of the impact of kin selection on the evolution of sexual conflict in viscous populations has been particularly valuable in stimulating empirical research in this area. An important goal of that study was to understand the impact of sex‐specific rates of dispersal upon the coevolution of male‐harm and female‐resistance behaviours. But the fitness functions derived in Rankin's study do not flow from his model's assumptions and, in particular, are not consistent with sex‐biased dispersal. Here, we develop new fitness functions that do logically flow from the model's assumptions, to determine the impact of sex‐specific patterns of dispersal on the evolution of sexual conflict. Although Rankin's study suggested that increasing male dispersal always promotes the evolution of male harm and that increasing female dispersal always inhibits the evolution of male harm, we find that the opposite can also be true, depending upon parameter values.     

Advanced eusociality, kin selection and male haploidy

Abstract  The generation-long primacy of kin selection in explaining the evolution of advanced eusociality in social insects has been challenged in recent papers. Does this challenge succeed? I consider three questions: is kin selection still the unchallengeable explanation for the evolution of eusociality; is the male haploidy of Hymenoptera important in this explanation; and, a subsidiary question of why are there no male workers in Hymenoptera? I briefly trace the origins of kin selection back to Darwin and then consider the explanations of mutualism, group selection, parental manipulation, and kin selection and its variant 'green beard' alleles. I stress that in the kin selection equation, however written, relatedness is deeply intertwined with ecology so that both are essential. Kin selection does remain unchallengeable but, for some, the role of male haploidy has lost favour recently despite several modelling efforts all finding that it favours the evolution of eusociality. Sex allocation is deep at the heart of the evolution of hymenopteran advanced eusociality, indicating the interacting roles of population genetics and general biology. Modellers have also found no reason for a lack of male workers, so that a biological superiority of females for this role is indicated for social Hymenoptera.     

Natural selection and the maximization of fitness

The notion that natural selection is a process of fitness maximization gets a bad press in population genetics, yet in other areas of biology the view that organisms behave as if attempting to maximize their fitness remains widespread. Here I critically appraise the prospects for reconciliation. I first distinguish four varieties of fitness maximization. I then examine two recent developments that may appear to vindicate at least one of these varieties. The first is the ‘new’ interpretation of Fisher's fundamental theorem of natural selection, on which the theorem is exactly true for any evolving population that satisfies some minimal assumptions. The second is the Formal Darwinism project, which forges links between gene frequency change and optimal strategy choice. In both cases, I argue that the results fail to establish a biologically significant maximization principle. I conclude that it may be a mistake to look for universal maximization principles justified by theory alone. A more promising approach may be to find maximization principles that apply conditionally and to show that the conditions were satisfied in the evolution of particular traits.     

Assortment and the analysis of natural selection on social traits

A central problem in evolutionary biology is to determine whether and how social interactions contribute to natural selection. A key method for phenotypic data is social selection analysis, in which fitness effects from social partners contribute to selection only when there is a correlation between the traits of individuals and their social partners (nonrandom phenotypic assortment). However, there are inconsistencies in the use of social selection that center around the measurement of phenotypic assortment. Here, we use data analysis and simulations to resolve these inconsistencies, showing that: (i) not all measures of assortment are suitable for social selection analysis; and (ii) the interpretation of assortment, and how to detect nonrandom assortment, will depend on the scale at which it is measured. We discuss links to kin selection theory and provide a practical guide for the social selection approach.     

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.     

Constraints on the origin and maintenance of genetic kin recognition

Kin-recognition mechanisms allow helping behaviors to be directed preferentially toward related individuals, and could be expected to evolve in many cases. However, genetic kin recognition requires a genetic polymorphism on which recognition is based, and kin discriminating behaviors will affect the evolution of such polymorphism. It is unclear whether genetic polymorphisms used in kin recognition should be maintained by extrinsic selection pressures or not, as opposite conclusions have been reached by analytical one-locus models and simulations exploring different population structures. We analyze a two-locus model in a spatially subdivided population following the island model of dispersal between demes of finite size. We find that in the absence of mutation, selection eliminates polymorphism in most cases, except with extreme spatial structure and low recombination. With mutation, the population may reach a stable limit cycle over which both loci are polymorphic; however, the average frequency of conditional helping can be high only under strong structure and low recombination. Finally, we review evidence for extrinsic selection maintaining polymorphism on which kin recognition is based.     

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.     

Natural selection. VI. Partitioning the information in fitness and characters by path analysis

Three steps aid in the analysis of selection. First, describe phenotypes by their component causes. Components include genes, maternal effects, symbionts and any other predictors of phenotype that are of interest. Second, describe fitness by its component causes, such as an individual's phenotype, its neighbours’ phenotypes, resource availability and so on. Third, put the predictors of phenotype and fitness into an exact equation for evolutionary change, providing a complete expression of selection and other evolutionary processes. The complete expression separates the distinct causal roles of the various hypothesized components of phenotypes and fitness. Traditionally, those components are given by the covariance, variance and regression terms of evolutionary models. I show how to interpret those statistical expressions with respect to information theory. The resulting interpretation allows one to read the fundamental equations of selection and evolution as sentences that express how various causes lead to the accumulation of information by selection and the decay of information by other evolutionary processes. The interpretation in terms of information leads to a deeper understanding of selection and heritability, and a clearer sense of how to formulate causal hypotheses about evolutionary process. Kin selection appears as a particular type of causal analysis that partitions social effects into meaningful components.     

Kin selection and the evolution of sexual conflict

Males and females do not always share the same evolutionary interests. This is particularly true in the case of multiple mating, where male–male competition can often lead to adaptations that are harmful to the female, and females can evolve counter adaptations to reduce the benefits males gain from such traits. Although social evolution has made substantial progress from kin selection theory, most studies of sexual conflict have ignored the effects of genetic relatedness. Here, I use a model of male harm and female resistance to investigate how kin selection affects the evolution of sexual conflict. Building on models of social evolution, I show that relatedness inhibits sexual conflict, in terms of male harm, whereas it has no effect on the evolution female resistance. This study examines a previously neglected mechanism that can potentially help to resolve sexual conflict over mating and highlights the potential importance of considering relatedness in empirical studies of sexual conflict.