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.     

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 Selection and Indirect Genetic Effects in Structured populations

Social selection and indirect genetic effects (IGEs) are established concepts in both behavioural ecology and evolutionary genetics. While IGEs describe effects of an individual’s genotype on phenotypes of social partners (and may thus affect their fitness indirectly), the concept of social selection assumes that a given phenotype in one individual affects the fitness of other individuals directly. Although different frameworks, both have been used to investigate the evolution of social traits, such as cooperative behaviour. Despite their similarities (both concepts consider interactions among individuals), they differ in the type of interaction. It remains unclear whether the two concepts make the same predictions about evolutionary trajectories or not. To address this question, we investigate four possible scenarios of social interactions and compare the effects of IGEs and social selection for trait evolution in a multi-trait multi-member model. We show that the two mechanisms can yield similar evolutionary outcomes and that both can create selection pressure at the group level. However, the effect of IGEs can be stronger due to the possibility of feedback loops. Finally, we demonstrate that IGEs, but not social selection gradients, may lead to differences in the direction of evolutionary response between genotypes and phenotypes.     

On indirect genetic effects in structured populations

Indirect genetic effects (IGEs) occur when the phenotype of an individual, and possibly its fitness, depends, at least in part, on the genes of its social partners. The effective result is that environmental sources of phenotypic variance can themselves evolve. Simple models have shown that IGEs can alter the rate and direction of evolution for traits involved in interactions. Here we expand the applicability of the theory of IGEs to evolution in metapopulations by including nonlinear interactions between individuals and population genetic structure. Although population subdivision alone generates some dramatic and nonintuitive evolutionary dynamics for interacting phenotypes, the combination of nonlinear interactions with subdivision reveals an even greater importance of IGEs. The presence of genetic structure links the evolution of interacting phenotypes and the traits that influence their expression ("effector traits") even in the absence of genetic correlations. When nonlinear social effects occur in subdivided populations, evolutionary response is altered and can even oppose the direction expected due to direct selection. Because population genetic structure allows for multilevel selection, we also investigate the role of IGEs in determining the response to individual and group selection. We find that nonlinear social effects can cause interference between levels of selection even when they act in the same direction. In some cases, interference can be so extreme that the actual evolutionary response to multilevel selection is opposite in direction to that predicted by summing selection at each level. This theoretical result confirms empirical data that show higher levels of selection cannot be ignored even when selection acts in the same direction at all levels.     

EXPERIMENTAL EVIDENCE FOR THE EVOLUTION OF INDIRECT GENETIC EFFECTS: CHANGES IN THE INTERACTION EFFECT COEFFICIENT,PSI (Ψ), DUE TO SEXUAL SELECTION

Indirect genetics effects (IGEs)—when the genotype of one individual affects the phenotypic expression of a trait in another—may alter evolutionary trajectories beyond that predicted by standard quantitative genetic theory as a consequence of genotypic evolution of the social environment. For IGEs to occur, the trait of interest must respond to one or more indicator traits in interacting conspecifics. In quantitative genetic models of IGEs, these responses (reaction norms) are termed interaction effect coefficients and are represented by the parameter psi (Ψ). The extent to which Ψ exhibits genetic variation within a population, and may therefore itself evolve, is unknown. Using an experimental evolution approach, we provide evidence for a genetic basis to the phenotypic response caused by IGEs on sexual display traits in Drosophila serrata. We show that evolution of the response is affected by sexual but not natural selection when flies adapt to a novel environment. Our results indicate a further mechanism by which IGEs can alter evolutionary trajectories—the evolution of interaction effects themselves.     

Social runaway: Fisherian elaboration (or reduction) of socially selected traits via indirect genetic effects

Our understanding of the evolutionary stability of socially selected traits is dominated by sexual selection models originating with R. A. Fisher, in which genetic covariance arising through assortative mating can trigger exponential, runaway trait evolution. To examine whether nonreproductive, socially selected traits experience similar dynamics—social runaway—when assortative mating does not automatically generate a covariance, we modeled the evolution of socially selected badge and donation phenotypes incorporating indirect genetic effects (IGEs) arising from the social environment. We establish a social runaway criterion based on the interaction coefficient, ψ , which describes social effects on badge and donation traits. Our models make several predictions. (1) IGEs can drive the original evolution of altruistic interactions that depend on receiver badges. (2) Donation traits are more likely to be susceptible to IGEs than badge traits. (3) Runaway dynamics in nonsexual, social contexts can occur in the absence of a genetic covariance. (4) Traits elaborated by social runaway are more likely to involve reciprocal, but nonsymmetrical, social plasticity. Models incorporating plasticity to the social environment via IGEs illustrate conditions favoring social runaway, describe a mechanism underlying the origins of costly traits, such as altruism, and support a fundamental role for phenotypic plasticity in rapid social evolution.     

Cultural transmission and the evolution of human behaviour: a general approach based on the Price equation

Transmitted culture can be viewed as an inheritance system somewhat independent of genes that is subject to processes of descent with modification in its own right. Although many authors have conceptualized cultural change as a Darwinian process, there is no generally agreed formal framework for defining key concepts such as natural selection, fitness, relatedness and altruism for the cultural case. Here, we present and explore such a framework using the Price equation. Assuming an isolated, independently measurable culturally transmitted trait, we show that cultural natural selection maximizes cultural fitness, a distinct quantity from genetic fitness, and also that cultural relatedness and cultural altruism are not reducible to or necessarily related to their genetic counterparts. We show that antagonistic coevolution will occur between genes and culture whenever cultural fitness is not perfectly aligned with genetic fitness, as genetic selection will shape psychological mechanisms to avoid susceptibility to cultural traits that bear a genetic fitness cost. We discuss the difficulties with conceptualizing cultural change using the framework of evolutionary theory, the degree to which cultural evolution is autonomous from genetic evolution, and the extent to which cultural change should be seen as a Darwinian process. We argue that the nonselection components of evolutionary change are much more important for culture than for genes, and that this and other important differences from the genetic case mean that different approaches and emphases are needed for cultural than genetic processes.     

Social traits,social networks and evolutionary biology

The social environment is both an important agent of selection for most organisms, and an emergent property of their interactions. As an aggregation of interactions among members of a population, the social environment is a product of many sets of relationships and so can be represented as a network or matrix. Social network analysis in animals has focused on why these networks possess the structure they do, and whether individuals’ network traits, representing some aspect of their social phenotype, relate to their fitness. Meanwhile, quantitative geneticists have demonstrated that traits expressed in a social context can depend on the phenotypes and genotypes of interacting partners, leading to influences of the social environment on the traits and fitness of individuals and the evolutionary trajectories of populations. Therefore, both fields are investigating similar topics, yet have arrived at these points relatively independently. We review how these approaches are diverged, and yet how they retain clear parallelism and so strong potential for complementarity. This demonstrates that, despite separate bodies of theory, advances in one might inform the other. Techniques in network analysis for quantifying social phenotypes, and for identifying community structure, should be useful for those studying the relationship between individual behaviour and group‐level phenotypes. Entering social association matrices into quantitative genetic models may also reduce bias in heritability estimates, and allow the estimation of the influence of social connectedness on trait expression. Current methods for measuring natural selection in a social context explicitly account for the fact that a trait is not necessarily the property of a single individual, something the network approaches have not yet considered when relating network metrics to individual fitness. Harnessing evolutionary models that consider traits affected by genes in other individuals (i.e. indirect genetic effects) provides the potential to understand how entire networks of social interactions in populations influence phenotypes and predict how these traits may evolve. By theoretical integration of social network analysis and quantitative genetics, we hope to identify areas of compatibility and incompatibility and to direct research efforts towards the most promising areas. Continuing this synthesis could provide important insights into the evolution of traits expressed in a social context and the evolutionary consequences of complex and nuanced social phenotypes.     

Indirect genetics effects and evolutionary constraint: an analysis of social dominance in red deer, Cervus elaphus

By determining access to limited resources, social dominance is often an important determinant of fitness. Thus, if heritable, standard theory predicts mean dominance should evolve. However, dominance is usually inferred from the tendency to win contests, and given one winner and one loser in any dyadic contest, the mean proportion won will always equal 0.5. Here, we argue that the apparent conflict between quantitative genetic theory and common sense is resolved by recognition of indirect genetic effects (IGEs). We estimate selection on, and genetic (co)variance structures for, social dominance, in a wild population of red deer Cervus elaphus, on the Scottish island of Rum. While dominance is heritable and positively correlated with lifetime fitness, contest outcomes depend as much on the genes carried by an opponent as on the genotype of a focal individual. We show how this dependency imposes an absolute evolutionary constraint on the phenotypic mean, thus reconciling theoretical predictions with common sense. More generally, we argue that IGEs likely provide a widespread but poorly recognized source of evolutionary constraint for traits influenced by competition.     

GxG epistasis in growth and condition and the maintenance of genetic polymorphism in Gambusia holbrooki

Theory on indirect genetic effects (IGEs) indicates that variation in the genetic composition of social groups can generate GxG epistasis that may promote the evolution of stable polymorphisms. Using a livebearing fish with a genetic polymorphism in coloration and associated behavioral differences, we tested whether genotypes of social partners interacted with focal individual genotypes to influence growth and condition over 16 weeks of development. We found that IGEs had a significant influence on patterns of feeding, regardless of focal fish genotype. There was no influence of social environment on juvenile length, but there was significant GxG epistasis for body condition. Each focal juvenile was in better condition when its own genotype was not present in adult social partners. These data are consistent with negative frequency‐dependent selection in which each morph performs better when it is rare. Neither variation in feeding nor activity‐related behaviors explained variation in body condition, suggesting that GxG epistasis for condition was caused by physiological differences between the two genotypes. These findings indicate that GxG epistasis in a given polymorphism can generate fitness landscapes that contribute to the maintenance of that polymorphism and to maintenance of genetic variation for additional fitness‐related traits.     

Socially flexible female choice differs among populations of the Pacific field cricket: geographical variation in the interaction coefficient psi (Ψ)

Indirect genetic effects (IGEs) occur when genes expressed in one individual affect the phenotype of a conspecific. Theoretical models indicate that the evolutionary consequences of IGEs critically depend on the genetic architecture of interacting traits, and on the strength and direction of phenotypic effects arising from social interactions, which can be quantified by the interaction coefficient Ψ. In the context of sexually selected traits, strong positive Ψ tends to exaggerate evolutionary change, whereas negative Ψ impedes sexual trait elaboration. Despite its theoretical importance, whether and how Ψ varies among geographically distinct populations is unknown. Such information is necessary to evaluate the potential for IGEs to contribute to divergence among isolated or semi-isolated populations. Here, we report substantial variation in Ψ for a behavioural trait involved in sexual selection in the field cricket Teleogryllus oceanicus: female choosiness. Both the strength and direction of Ψ varied among geographically isolated populations. Ψ also changed over time. In a contemporary population of crickets from Kauai, experience of male song increased female choosiness. In contrast, experience of male song decreased choosiness in an ancestral population from the same location. This rapid change corroborates studies examining the evolvability of Ψ and demonstrates how interpopulation variation in the interaction coefficient might influence sexual selection and accelerate divergence of traits influenced by IGEs that contribute to reproductive isolation in nascent species or subspecies.     

Runaway sexual selection without genetic correlations: social environments and flexible mate choice initiate and enhance the fisher process

Female mating preferences are often flexible, reflecting the social environment in which they are expressed. Associated indirect genetic effects (IGEs) can affect the rate and direction of evolutionary change, but sexual selection models do not capture these dynamics. We incorporate IGEs into quantitative genetic models to explore how variation in social environments and mate choice flexibility influence Fisherian sexual selection. The importance of IGEs is that runaway sexual selection can occur in the absence of a genetic correlation between male traits and female preferences. Social influences can facilitate the initiation of the runaway process and increase the rate of trait elaboration. Incorporating costs to choice do not alter the main findings. Our model provides testable predictions: (1) genetic covariances between male traits and female preferences may not exist, (2) social flexibility in female choice will be common in populations experiencing strong sexual selection, (3) variation in social environments should be associated with rapid sexual trait divergence, and (4) secondary sexual traits will be more elaborate than previously predicted. Allowing feedback from the social environment resolves discrepancies between theoretical predictions and empirical data, such as why indirect selection on female preferences, theoretically weak, might be sufficient for preferences to become elaborated.     

INDIRECT GENETIC EFFECTS INFLUENCE ANTIPREDATOR BEHAVIOR IN GUPPIES: ESTIMATES OF THE COEFFICIENT OF INTERACTION PSI AND THE INHERITANCE OF RECIPROCITY

How and why cooperation evolves, particularly among nonrelatives, remains a major paradox for evolutionary biologists and behavioral ecologists. Although much attention has focused on fitness consequences associated with cooperating, relatively little is known about the second component of evolutionary change, the inheritance of cooperation or reciprocity. The genetics of behaviors that can only be expressed in the context of interactions are particularly difficult to describe because the relevant genes reside in multiple social partners. Indirect genetic effects (IGEs) describe the influence of genes carried in social partners on the phenotype of a focal individual and thus provide a novel approach to quantifying the genetics underlying interactions such as reciprocal cooperation. We used inbred lines of guppies and a novel application of IGE theory to describe the dual genetic control of predator inspection and social behavior, both classic models of reciprocity. We identified effects of focal strain, social group strain, and interactions between focal and group strains on variation in focal behavior. We measured ψ, the coefficient of the interaction, which describes the degree to which an individual's phenotype is influenced by the phenotype of its social partners. The genetic identity of social partners substantially influences inspection behavior, measures of threat assessment, and schooling and does so in positively reinforcing manner. We therefore demonstrate strong IGEs for antipredator behavior that represent the genetic variation necessary for the evolution of reciprocity.     

The role of indirect genetic effects in the evolution of interacting reproductive behaviors in the burying beetle,Nicrophorus vespilloides

Social interactions can give rise to indirect genetic effects (IGEs), which occur when genes expressed in one individual affect the phenotype of another individual. The evolutionary dynamics of traits can be altered when there are IGEs. Sex often involves indirect effects arising from first‐order (current) or second‐order (prior) social interactions, yet IGEs are infrequently quantified for reproductive behaviors. Here, we use experimental populations of burying beetles that have experienced bidirectional selection on mating rate to test for social plasticity and IGEs associated with focal males mating with a female either without (first‐order effect) or with (second‐order effect) prior exposure to a competitor, and resource defense behavior (first‐order effect). Additive IGEs were detected for mating rate arising from (first‐order) interactions with females. For resource defense behavior, a standard variance partitioning analysis provided no evidence of additive genetic variance—either direct or indirect. However, behavior was predicted by focal size relative to that of the competitor, and size is also heritable. Assuming that behavior is causally dependent on relative size, this implies that both DGEs and IGEs do occur (and may potentially interact). The relative contribution of IGEs may differ among social behaviors related to mating which has consequences for the evolutionary trajectories of multivariate traits.     

HOW TO MEASURE INDIRECT GENETIC EFFECTS: THE CONGRUENCE OF TRAIT-BASED AND VARIANCE-PARTITIONING APPROACHES

Indirect genetic effects (IGEs), which occur when phenotypic expression in one individual is influenced by genes in another conspecific individual, may have a drastic effect on evolutionary response to selection. General evolutionary models of IGEs have been developed using two distinct theoretical frameworks derived from maternal effects theory. The first framework is trait-based and focuses on how phenotypes are influenced by specific traits in a social partner, with the strength of interactions defined by the matrix Ψ. The second framework partitions total genetic variance into components representing direct effects, indirect effects, and the covariance between them, without identifying specific social traits responsible for IGEs. The latter framework has been employed more commonly by empiricists because the methods for estimating variance components are relatively straightforward. Here, we show how these two theoretical frameworks are related to each other and derive equations that can be used to translate between them. This translation leads to a generalized method that can be used to estimate Ψ via standard quantitative genetic breeding designs or pedigrees from natural populations. This method can be used in a very general set of circumstances and is widely applicable to all IGEs, including maternal effects and other interactions among relatives.     

Indirect genetic effects and the evolution of aggression in a vertebrate system

Aggressive behaviours are necessarily expressed in a social context, such that individuals may be influenced by the phenotypes, and potentially the genotypes, of their social partners. Consequently, it has been hypothesized that indirect genetic effects (IGEs) arising from the social environment will provide a major source of heritable variation on which selection can act. However, there has been little empirical scrutiny of this to date. Here we test this hypothesis in an experimental population of deer mice (Peromyscus maniculatus). Using quantitative genetic models of five aggression traits, we find repeatable and heritable differences in agonistic behaviours of focal individuals when presented with an opponent mouse. For three of the traits, there is also support for the presence of IGEs, and estimated correlations between direct and indirect genetic (rAO,F) effects were high. As a consequence, any selection for aggression in the focal individuals should cause evolution of the social environment as a correlated response. In two traits, strong positive rAO,F will cause the rapid evolution of aggression, while in a third case changes in the phenotypic mean will be constrained by negative covariance between direct and IGEs. Our results illustrate how classical analyses may miss important components of heritable variation, and show that a full understanding of evolutionary dynamics requires explicit consideration of the genetic component of the social environment.     

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.     

Relatedness in trait group models of social evolution

Genetic relatedness is a central concept in the study of social evolution. Though originally defined in terms of genealogy, the modern version of relatedness accommodates genetic similarity of any origin. This paper examines relatedness in group structured modes, in which a trait affects the fitness of all group members. Such traits can be divided into two types, based on whether their group fitness effects encompass all group members including the actor ("whole-group traits"), or only group members other than the actor ("other-only traits"). Both trait types are common in nature as well as in theoretical models, but they have rarely been distinguished clearly. The average relatedness of recipients to actors differs for the two trait types within the same population and even the same individual, leading to different selection pressures and evolutionary outcomes. Total relatedness in group-structured models can be partitioned into two components: structural relatedness due to the size and number of groups in the population, and assortative relatedness due to the distribution of genotypes among groups. Each component differs for whole-group vs. other-only traits, both in terms of their values and the factors that influence them. Some key differences include: positive relatedness requires positive assortment for other-only but not for whole-group traits; negative relatedness is possible for other-only but not whole-group traits; relatedness depends on average group size for whole-group but not other-only traits, and non-random assortment into groups affects relatedness more strongly for other-only than whole-group traits. Recognizing the distinction between these trait types resolves some apparent contradictions in the literature, and clarifies the limits of some previous results.     

Altruism and fairness: Unnatural selection?

Darwin admitted that the evolution of moral phenomena such as altruism and fairness, which are usually in opposition to the maximization of individual reproductive success, was not easily accounted for by natural selection. Later, authors have proposed additional mechanisms, including kin selection, inclusive fitness, and reciprocal altruism. In the present work, we explore the extent to which sexual selection has played a role in the appearance of human moral traits. It has been suggested that because certain moral virtues, including altruism and kindness, are sexually attractive, their evolution could have been shaped by the process of sexual selection. Our review suggests that although it is possible that sexual selection played such a role, it is difficult to determine the extent of its relevance, the specific form of this influence, and its interplay with other evolutionary mechanisms.     

The group selection controversy

Many thought Darwinian natural selection could not explain altruism. This error led Wynne‐Edwards to explain sustainable exploitation in animals by selection against overexploiting groups. Williams riposted that selection among groups rarely overrides within‐group selection. Hamilton showed that altruism can evolve through kin selection. How strongly does group selection influence evolution? Following Price, Hamilton showed how levels of selection interact: group selection prevails if Hamilton’s rule applies. Several showed that group selection drove some major evolutionary transitions. Following Hamilton’s lead, Queller extended Hamilton’s rule, replacing genealogical relatedness by the regression on an actor’s genotypic altruism of interacting neighbours’ phenotypic altruism. Price’s theorem shows the generality of Hamilton’s rule. All instances of group selection can be viewed as increasing inclusive fitness of autosomal genomes. Nonetheless, to grasp fully how cooperation and altruism evolve, most biologists need more concrete concepts like kin selection, group selection and selection among individuals for their common good.