Opposite responses to selection and where to find them

We generally expect traits to evolve in the same direction as selection. However, many organisms possess traits that appear to be costly for individuals, while plant and animal breeding experiments reveal that selection may lead to no response or even negative responses to selection. We formalize both of these instances as cases of “opposite responses to selection.” Using quantitative genetic models for the response to selection, we outline when opposite responses to selection should be expected. These typically occur when social selection opposes direct selection, when individuals interact with others less related to them than a random member of the population, and if the genetic covariance between direct and indirect effects is negative. We discuss the likelihood of each of these occurring in nature and therefore summarize how frequent opposite responses to selection are likely to be. This links several evolutionary phenomena within a single framework.     

Indirect genetic effects and kin recognition: estimating IGEs when interactions differ between kin and strangers

Social interactions among individuals are widespread, both in natural and domestic populations. As a result, trait values of individuals may be affected by genes in other individuals, a phenomenon known as indirect genetic effects (IGEs). IGEs can be estimated using linear mixed models. The traditional IGE model assumes that an individual interacts equally with all its partners, whether kin or strangers. There is abundant evidence, however, that individuals behave differently towards kin as compared with strangers, which agrees with predictions from kin-selection theory. With a mix of kin and strangers, therefore, IGEs estimated from a traditional model may be incorrect, and selection based on those estimates will be suboptimal. Here we investigate whether genetic parameters for IGEs are statistically identifiable in group-structured populations when IGEs differ between kin and strangers, and develop models to estimate such parameters. First, we extend the definition of total breeding value and total heritable variance to cases where IGEs depend on relatedness. Next, we show that the full set of genetic parameters is not identifiable when IGEs differ between kin and strangers. Subsequently, we present a reduced model that yields estimates of the total heritable effects on kin, on non-kin and on all social partners of an individual, as well as the total heritable variance for response to selection. Finally we discuss the consequences of analysing data in which IGEs depend on relatedness using a traditional IGE model, and investigate group structures that may allow estimation of the full set of genetic parameters when IGEs depend on kin.     

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 quantitative genetics of indirect genetic effects: a selective review of modelling issues

Indirect genetic effects (IGE) occur when the genotype of an individual affects the phenotypic trait value of another conspecific individual. IGEs can have profound effects on both the magnitude and the direction of response to selection. Models of inheritance and response to selection in traits subject to IGEs have been developed within two frameworks; a trait-based framework in which IGEs are specified as a direct consequence of individual trait values, and a variance-component framework in which phenotypic variance is decomposed into a direct and an indirect additive genetic component. This work is a selective review of the quantitative genetics of traits affected by IGEs, with a focus on modelling, estimation and interpretation issues. It includes a discussion on variance-component vs trait-based models of IGEs, a review of issues related to the estimation of IGEs from field data, including the estimation of the interaction coefficient Ψ (psi), and a discussion on the relevance of IGEs for response to selection in cases where the strength of interaction varies among pairs of individuals. An investigation of the trait-based model shows that the interaction coefficient Ψ may deviate considerably from the corresponding regression coefficient when feedback occurs. The increasing research effort devoted to IGEs suggests that they are a widespread phenomenon, probably particularly in natural populations and plants. Further work in this field should considerably broaden our understanding of the quantitative genetics of inheritance and response to selection in relation to the social organisation of populations.     

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.     

The quantitative genetics of the prevalence of infectious diseases: hidden genetic variation due to indirect genetic effects dominates heritable variation and response to selection

Infectious diseases have profound effects on life, both in nature and agriculture. However, a quantitative genetic theory of the host population for the endemic prevalence of infectious diseases is almost entirely lacking. While several studies have demonstrated the relevance of transmission of infections for heritable variation and response to selection, current quantitative genetics ignores transmission. Thus, we lack concepts of breeding value and heritable variation for endemic prevalence, and poorly understand response of endemic prevalence to selection. Here, we integrate quantitative genetics and epidemiology, and propose a quantitative genetic theory for the basic reproduction number R₀ and for the endemic prevalence of an infection. We first identify the genetic factors that determine the prevalence. Subsequently, we investigate the population-level consequences of individual genetic variation, for both R0 and the endemic prevalence. Next, we present expressions for the breeding value and heritable variation, for endemic prevalence and individual binary disease status, and show that these depend strongly on the prevalence. Results show that heritable variation for endemic prevalence is substantially greater than currently believed, and increases strongly when prevalence decreases, while heritability of disease status approaches zero. As a consequence, response of the endemic prevalence to selection for lower disease status accelerates considerably when prevalence decreases, in contrast to classical predictions. Finally, we show that most heritable variation for the endemic prevalence is hidden in indirect genetic effects, suggesting a key role for kin-group selection in the evolutionary history of current populations and for genetic improvement in animals and plants.     

Multilevel selection theory and evidence: a critique of Gardner, 2015

Gardner (2015) recently developed a model of a ‘Genetical Theory of Multilevel Selection, which is a thoughtfully developed, but flawed model. The model's flaws appear to be symptomatic of common misunderstandings of the multi level selection (MLS) literature and the recent quantitative genetic literature. I use Gardner's model as a guide for highlighting how the MLS literature can address the misconceptions found in his model, and the kin selection literature in general. I discuss research on the efficacy of group selection, the roll of indirect genetic effects in affecting the response to selection and the heritability of group‐level traits. I also discuss why the Price multilevel partition should not be used to partition MLS, and why contextual analysis and, by association, direct fitness are appropriate for partitioning MLS. Finally, I discuss conceptual issues around questions concerning the level at which fitness is measured, the units of selection, and I present a brief outline of a model of selection in class‐structured populations. I argue that the results derived from the MLS research tradition can inform kin selection research and models, and provide insights that will allow researchers to avoid conceptual flaws such as those seen in the Gardner model.     

Natural selection. VII. History and interpretation of kin selection theory

Kin selection theory is a kind of causal analysis. The initial form of kin selection ascribed cause to costs, benefits and genetic relatedness. The theory then slowly developed a deeper and more sophisticated approach to partitioning the causes of social evolution. Controversy followed because causal analysis inevitably attracts opposing views. It is always possible to separate total effects into different component causes. Alternative causal schemes emphasize different aspects of a problem, reflecting the distinct goals, interests and biases of different perspectives. For example, group selection is a particular causal scheme with certain advantages and significant limitations. Ultimately, to use kin selection theory to analyse natural patterns and to understand the history of debates over different approaches, one must follow the underlying history of causal analysis. This article describes the history of kin selection theory, with emphasis on how the causal perspective improved through the study of key patterns of natural history, such as dispersal and sex ratio, and through a unified approach to demographic and social processes. Independent historical developments in the multivariate analysis of quantitative traits merged with the causal analysis of social evolution by kin selection.     

Routes to indirect fitness in cooperatively breeding vertebrates: kin discrimination and limited dispersal

Hamilton demonstrated that the evolution of cooperative behaviour is favoured by high relatedness, which can arise through kin discrimination or limited dispersal (population viscosity). These two processes are likely to operate with limited overlap: kin discrimination is beneficial when variation in relatedness is higher, whereas limited dispersal results in less variable and higher average relatedness, reducing selection for kin discrimination. However, most empirical work on eukaryotes has focused on kin discrimination. To address this bias, we analysed how kin discrimination and limited dispersal interact to shape helping behaviour across cooperatively breeding vertebrates. We show that kin discrimination is greater in species where the: (i) average relatedness in groups is lower and more variable; (ii) effect of helpers on breeders reproductive success is greater; and (iii) probability of helping was measured, rather than the amount of help provided. There was also an interaction between these effects with the correlation between the benefits of helping and kin discrimination being stronger in species with higher variance in relatedness. Overall, our results suggest that kin discrimination provides a route to indirect benefits when relatedness is too variable within groups to favour indiscriminate cooperation.     

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.     

The costs and benefits of resource sharing: reciprocity requires resource heterogeneity

The evolution of resource sharing requires that the fitness benefits to the recipients be much higher than the costs to the giver, which requires heterogeneity among individuals in the fitness value of acquiring additional resources. We develop four models of the evolution of resource sharing by either direct or indirect reciprocity, with equal or unequal partners. Evolution of resource sharing by reciprocity requires differences between interacting individuals in the fitness value of the resource, and these differences must reverse although previous acts of giving are remembered and both participants survive. Moreover, inequality in the expected reproductive value of the interacting individuals makes reciprocity more difficult to evolve, but may still allow evolution of sharing by kin selection. These constraints suggest that resource sharing should evolve much more frequently by kin selection than by reciprocity, a prediction that is well supported by observations in the natural world.     

Why genetic selection to reduce the prevalence of infectious diseases is way more promising than currently believed

Genetic selection for improved disease resistance is an important part of strategies to combat infectious diseases in agriculture. Quantitative genetic analyses of binary disease status, however, indicate low heritability for most diseases, which restricts the rate of genetic reduction in disease prevalence. Moreover, the common liability threshold model suggests that eradication of an infectious disease via genetic selection is impossible because the observed-scale heritability goes to zero when the prevalence approaches zero. From infectious disease epidemiology, however, we know that eradication of infectious diseases is possible, both in theory and practice, because of positive feedback mechanisms leading to the phenomenon known as herd immunity. The common quantitative genetic models, however, ignore these feedback mechanisms. Here, we integrate quantitative genetic analysis of binary disease status with epidemiological models of transmission, aiming to identify the potential response to selection for reducing the prevalence of endemic infectious diseases. The results show that typical heritability values of binary disease status correspond to a very substantial genetic variation in disease susceptibility among individuals. Moreover, our results show that eradication of infectious diseases by genetic selection is possible in principle. These findings strongly disagree with predictions based on common quantitative genetic models, which ignore the positive feedback effects that occur when reducing the transmission of infectious diseases. Those feedback effects are a specific kind of Indirect Genetic Effects; they contribute substantially to the response to selection and the development of herd immunity (i.e., an effective reproduction ratio less than one).     

The genetical theory of multilevel selection

The theory of multilevel selection (MLS) is beset with conceptual difficulties. Although it is widely agreed that covariance between group trait and group fitness may arise in the natural world and drive a response to ‘group selection’, ambiguity exists over the precise meaning of group trait and group fitness and as to whether group selection should be defined according to changes in frequencies of different types of individual or different types of group. Moreover, the theory of MLS has failed to properly engage with the problem of class structure, which greatly limits its empirical application to, for example, social insects whose colonies are structured into separate age, sex, caste and ploidy classes. Here, I develop a genetical theory of MLS, to address these problems. I show that taking a genetical approach facilitates a decomposition of group‐level traits – including reproductive success – into the separate contributions made by each constituent individual, even in the context of so‐called emergence. However, I uncover a novel problem with the group‐oriented approach: in many scenarios, it may not be possible to express a meaningful covariance between trait and fitness at the level of the social group, because the group's constituents belong to separate, irreconcilable classes.     

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.     

Direct, maternal, and sibsocial genetic effects on individual and colony traits in an ant

When social interactions occur, the phenotype of an individual is influenced directly by its own genes (direct genetic effects) but also indirectly by genes expressed in social partners (indirect genetic effects). Social insect colonies are characterized by extensive behavioral interactions among workers, brood, and queens so that indirect genetic effects are particularly relevant. I used a series of experimental manipulations to disentangle the contribution of direct effects, maternal (queen) effects, and sibsocial (worker) effects to variation for worker, gyne, and male mass; caste ratio; and sex ratio in the ant Temnothorax curvispinosus. The results indicate genetic variance for direct, maternal, and sibsocial effects for all traits, except for male mass there was no significant maternal variance, and for sex ratio the variance for direct effects was not separable from maternal variance for the primary sex ratio. Estimates of genetic correlations between direct, maternal, and sibsocial effects were generally negative, indicating that these effects may not evolve independently. These results have broad implications for social insect evolution. For example, the genetic architecture underlying social insect traits may constrain the realization of evolutionary conflicts between social partners.     

Stability of the G-matrix in a population experiencing pleiotropic mutation, stabilizing selection, and genetic drift

Abstract. Quantitative genetics theory provides a framework that predicts the effects of selection on a phenotype consisting of a suite of complex traits. However, the ability of existing theory to reconstruct the history of selection or to predict the future trajectory of evolution depends upon the evolutionary dynamics of the genetic variance-covariance matrix (G-matrix). Thus, the central focus of the emerging field of comparative quantitative genetics is the evolution of the G-matrix. Existing analytical theory reveals little about the dynamics of G, because the problem is too complex to be mathematically tractable. As a first step toward a predictive theory of G-matrix evolution, our goal was to use stochastic computer models to investigate factors that might contribute to the stability of G over evolutionary time. We were concerned with the relatively simple case of two quantitative traits in a population experiencing stabilizing selection, pleiotropic mutation, and random genetic drift. Our results show that G-matrix stability is enhanced by strong correlational selection and large effective population size. In addition, the nature of mutations at pleiotropic loci can dramatically influence stability of G. In particular, when a mutation at a single locus simultaneously changes the value of the two traits (due to pleiotropy) and these effects are correlated, mutation can generate extreme stability of G. Thus, the central message of our study is that the empirical question regarding G-matrix stability is not necessarily a general question of whether G is stable across various taxonomic levels. Rather, we should expect the G-matrix to be extremely stable for some suites of characters and unstable for others over similar spans of evolutionary time.     

Social structure and indirect genetic effects: genetics of social behaviour

The social environment modulates gene expression, physiology, behaviour and patterns of inheritance. For more than 50 years, this concept has been investigated using approaches that include partitioning the social component out of behavioural heritability estimates, studying maternal effects on offspring, and analysing dominance hierarchies. Recent advances have formalized this ‘social environment effect’ by providing a more nuanced approach to the study of social influences on behaviour while recognizing evolutionary implications. Yet, in most of these formulations, the dynamics of social interactions are not accounted for. Also, the reciprocity between individual behaviour and group‐level interactions has been largely ignored. Consistent with evolutionary theory, the principles of social interaction are conserved across a broad range of taxa. While noting parallels in diverse organisms, this review uses Drosophila melanogaster as a case study to revisit what is known about social interaction paradigms. We highlight the benefits of integrating the history and pattern of interactions among individuals for dissecting molecular mechanisms that underlie social modulation of behaviour.     

The effects of kin selection on rates of molecular evolution in social insects

The evolution of sociality represented a major transition point in biological history. The most advanced societies, such as those displayed by social insects, consist of reproductive and nonreproductive castes. The caste system fundamentally affects the way natural selection operates. Specifically, selection acts directly on reproductive castes, such as queens, but only indirectly through the process of kin selection on nonreproductive castes, such as workers. In this study, we present theoretical analyses to determine the rate of substitution at loci expressed exclusively in the queen or worker castes. We show that the rate of substitution is the same for queen- and worker-selected loci when the queen is singly mated. In contrast, when a queen is multiply mated, queen-selected loci show higher rates of substitution for adaptive alleles and lower rates of substitution for deleterious alleles than worker-selected loci. We compare our theoretical expectations to previously obtained genomic data from the honeybee, Apis mellifera, where queens mate multiply and the fire ant, Solenopsis invicta, where queens mate singly and find that rates of evolution of queen- and worker-selected loci are consistent with our predictions. Overall, our research tests theoretical expectations using empirically obtained genomic data to better understand the evolution of advanced societies.     

The role of maternal and paternal effects in the evolution of parental quality by sexual selection

Genetic models of maternal effects and models of mate choice have focused on the evolutionary effects of variation in parental quality. There have been, however, few attempts to combine these into a single model for the evolution of sexually selected traits. We present a quantitative genetic model that considers how male and female parental quality (together or separately) affect the expression of a sexually selected offspring trait. We allow female choice of males based on this parentally affected trait and examine the evolution of mate choice, parental quality and the indicator trait. Our model reveals a number of consequences of maternal and paternal effects. (1) The force of sexual selection owing to adaptive mate choice can displace parental quality from its natural selection optimum. (2) The force of sexual selection can displace female parental quality from its natural selection optimum even when nonadaptive mate choice occurs (e.g. runaway sexual selection), because females of higher parental quality produce more attractive sons and these sons counterbalance the loss in fitness owing to over-investment in each offspring. (3) Maternal and paternal effects can provide a source of genetic variation for offspring traits, allowing evolution by sexual selection even when those traits do not show direct genetic variation (i.e. are not heritable). (4) The correlation between paternal investment and the offspring trait influenced by the parental effects can result in adaptive mate choice and lead to the elaboration of both female preference and the male sexually selected trait. When parental effects exist, sexual selection can drive the evolution of parental quality when investment increases the attractiveness of offspring, leading to the elaboration of indicator traits and higher than expected levels of parental investment.