Jason B. Wolf

Evolutionary consequences of indirect genetic effects

Indirect genetic effects (IGEs) are environmental influences on the phenotype of one individual that are due to the expression of genes in a different, conspecific, individual. Historically, work has focused on the influence of parents on offspring but recent advances have extended this perspective to interactions among other relatives and even unrelated individuals. IGEs lead to complicated pathways of inheritance, where environmental sources of variation can be transmitted across generations and therefore contribute to evolutionary change. The existence of IGEs alters the genotype-phenotype relationship, changing the evolutionary process in some dramatic and non-intuitive ways.

INTERACTING PHENOTYPES AND THE EVOLUTIONARY PROCESS: I. DIRECT AND INDIRECT GENETIC EFFECTS OF SOCIAL INTERACTIONS

Interacting phenotypes are traits whose expression is affected by interactions with conspecifics. Commonly‐studied interacting phenotypes include aggression, courtship, and communication. More extreme examples of interacting phenotypes—traits that exist exclusively as a product of interactions—include social dominance, intraspecific competitive ability, and mating systems. We adopt a quantitative genetic approach to assess genetic influences on interacting phenotypes. We partition genetic and environmental effects so that traits in conspecifics that influence the expression of interacting phenotypes are a component of the environment. When the trait having the effect is heritable, the environmental influence arising from the interaction has a genetic basis and can be incorporated as an indirect genetic effect. However, because it has a genetic basis, this environmental component can evolve. Therefore, to consider the evolution of interacting phenotypes we simultaneously consider changes in the direct genetic contributions to a trait (as a standard quantitative genetic approach would evaluate) as well as changes in the environmental (indirect genetic) contribution to the phenotype. We then explore the ramifications of this model of inheritance on the evolution of interacting phenotypes. The relative rate of evolution in interacting phenotypes can be quite different from that predicted by a standard quantitative genetic analysis. Phenotypic evolution is greatly enhanced or inhibited depending on the nature of the direct and indirect genetic effects. Further, unlike most models of phenotypic evolution, a lack of variation in direct genetic effects does not preclude evolution if there is genetic variance in the indirect genetic contributions. The available empirical evidence regarding the evolution of behavior expressed in interactions, although limited, supports the predictions of our model.

INTERACTING PHENOTYPES AND THE EVOLUTIONARY PROCESS. II. SELECTION RESULTING FROM SOCIAL INTERACTIONS

Social interactions often affect the fitness of interactants. Because of this, social selection has been described as a process distinct from other forms of natural selection. Social selection has been predicted to result in different evolutionary dynamics for interacting phenotypes, including rapid or extreme evolution and evolution of altruism. Despite the critical role that social selection plays in theories of social evolution, few studies have measured the force of social selection or the conditions under which this force changes. Here we present a model of social selection acting on interacting phenotypes that can be evaluated independently from the genetics of interacting phenotypes. Our model of social selection is analogous to covariance models of other forms of selection. We observe that an opportunity for social selection exists whenever individual fitness varies as a result of interactions with conspecifics. Social selection occurs, therefore, when variation in fitness due to interactions covaries with traits, resulting in a net force of selection acting on the interacting phenotypes. Thus, there must be a covariance between the phenotypes of the interactants for social selection to exist. This interacting phenotype covariance is important because it measures the degree to which a particular trait covaries with the selective environment provided by conspecifics. A variety of factors, including nonrandom interactions, behavioral modification during interactions, relatedness, and indirect genetic effects may contribute to the covariance of interacting phenotypes, which promotes social selection. The independent force of social selection (measured as a social selection gradient) can be partitioned empirically from the force of natural selection (measured by the natural selection gradient) using partial regression. This measure can be combined with genetic models of interacting phenotypes to provide insights into social evolution.

What are maternal effects (and what are they not)

Maternal effects can play an important role in a diversity of ecological and evolutionary processes such as population dynamics, phenotypic plasticity, niche construction, life-history evolution and the evolutionary response to selection. However, although maternal effects were defined by quantitative geneticists well over half a century ago, there remains some confusion over exactly what phenomena should be characterized as maternal effects and, more importantly, why it matters and how they are defined. We suggest a definition of maternal effects as the causal influence of the maternal genotype or phenotype on the offspring phenotype. This definition differs from some definitions in that it treats maternal effects as a phenomenon, not as a statistical construct. The causal link to maternal genotype or phenotype is the critical component of this definition providing the link between maternal effects and evolutionary and ecological processes. We show why phenomena such as maternal cytoplasmic inheritance and genomic imprinting are distinct genetically from and have different evolutionary consequences than true maternal effects. We also argue that one should consider cases where the maternal effect is conditional on offspring genotype as a class of maternal effects.

INTERACTING PHENOTYPES AND THE EVOLUTIONARY PROCESS. III. SOCIAL EVOLUTION

Interactions among conspecifics influence social evolution through two distinct but intimately related paths. First, they provide the opportunity for indirect genetic effects (IGEs), where genes expressed in one individual influence the expression of traits in others. Second, interactions can generate social selection when traits expressed in one individual influence the fitness of others. Here, we present a quantitative genetic model of multivariate trait evolution that integrates the effects of both IGEs and social selection, which have previously been modeled independently. We show that social selection affects evolutionary change whenever the breeding value of one individual covaries with the phenotype of its social partners. This covariance can be created by both relatedness and IGEs, which are shown to have parallel roles in determining evolutionary response. We show that social selection is central to the estimation of inclusive fitness and derive a version of Hamiltons rule showing the symmetrical effects of relatedness and IGEs on the evolution of altruism. We illustrate the utility of our approach using altruism, greenbeards, aggression, and weapons as examples. Our model provides a general predictive equation for the evolution of social phenotypes that encompasses specific cases such as kin selection and reciprocity. The parameters can be measured empirically, and we emphasize the importance of considering both IGEs and social selection, in addition to relatedness, when testing hypotheses about social evolution.

Multilevel selection 2: Estimating the genetic parameters determining inheritance and response to selection.

Interactions among individuals are universal, both in animals and in plants and in natural as well as domestic populations. Understanding the consequences of these interactions for the evolution of populations by either natural or artificial selection requires knowledge of the heritable components underlying them. Here we present statistical methodology to estimate the genetic parameters determining response to multilevel selection of traits affected by interactions among individuals in general populations. We apply these methods to obtain estimates of genetic parameters for survival days in a population of layer chickens with high mortality due to pecking behavior. We find that heritable variation is threefold greater than that obtained from classical analyses, meaning that two-thirds of the full heritable variation is hidden to classical analysis due to social interactions. As a consequence, predicted responses to multilevel selection applied to this population are threefold greater than classical predictions. This work, combined with the quantitative genetic theory for response to multilevel selection presented in an accompanying article in this issue, enables the design of selection programs to effectively reduce competitive interactions in livestock and plants and the prediction of the effects of social interactions on evolution in natural populations undergoing multilevel selection.

A Maternal–Offspring Coadaptation Theory for the Evolution of Genomic Imprinting

Imprinted genes are expressed either from the maternally or paternally inherited copy only, and they play a key role in regulating complex biological processes, including offspring development and mother–offspring interactions. There are several competing theories attempting to explain the evolutionary origin of this monoallelic pattern of gene expression, but a prevailing view has emerged that holds that genomic imprinting is a consequence of conflict between maternal and paternal gene copies over maternal investment. However, many imprinting patterns and the apparent overabundance of maternally expressed genes remain unexplained and may be incompatible with current theory. Here we demonstrate that sole expression of maternal gene copies is favored by natural selection because it increases the adaptive integration of offspring and maternal genomes, leading to higher offspring fitness. This novel coadaptation theory for the evolution of genomic imprinting is consistent with results of recent studies on epigenetic effects, and it provides a testable hypothesis for the origin of previously unexplained major imprinting patterns across different taxa. In conjunction with existing hypotheses, our results suggest that imprinting may have evolved due to different selective pressures at different loci.

On the assignment of fitness to parents and offspring: whose fitness is it and when does it matter?

There has been a long‐standing conceptual debate over the legitimacy of assigning components of offspring fitness to parents for purposes of evolutionary analysis. The benefits and risks inherent in assigning fitness of offspring to parents have been given primarily as verbal arguments and no explicit theoretical analyses have examined quantitatively how the assignment of fitness can affect evolutionary inferences. Using a simple quantitative genetic model, we contrast the conclusions drawn about how selection acts on a maternal character when components of offspring fitness (such as early survival) are assigned to parents vs. when they are assigned directly to the individual offspring. We find that there are potential shortcomings of both possible assignments of fitness. In general, whenever there is a genetic correlation between the parental and direct effects on offspring fitness, assigning components of offspring fitness to parents yields incorrect dynamical equations and may even lead to incorrect conclusions about the direction of evolution. Assignment of offspring fitness to parents may also produce incorrect estimates of selection whenever environmental variation contributes to variance of the maternal trait. Whereas assignment of offspring fitness to the offspring avoids these potential problems, it introduces the possible problem of missing components of kin selection provided by the mother, which may not be detected in selection analyses. There are also certain conditions where either model can be appropriate because assignment of offspring fitness to parents may yield the same dynamical equations as assigning offspring fitness directly to offspring. We discuss these implications of the alternative assignments of fitness for modelling, selection analysis and experimentation in evolutionary biology.

Genetic architecture and evolutionary constraint when the environment contains genes

The environment provided by conspecifics is often the most important component of the environment experienced by individuals, frequently having profound effects on fitness and trait expression. Although these social effects on fitness and trait expression may appear to be purely environmental, they differ from other sorts of environmental influences, because they can have a genetic basis and thus can contribute to evolution. Theory has shown that these effects modify the definition of genetic architecture by making the phenotype the property of the genotypes of multiple individuals and alter evolutionary dynamics by introducing additional heritable components contributing to trait evolution. These effects suggest that genetic and evolutionary analyses of traits influenced by social environments must incorporate the genetic components of variation contributed by these environments. However, empirical studies incorporating these effects are generally lacking. In this paper, I quantify the contribution of genetically based environmental effects arising from social interactions during group rearing to the quantitative genetics of body size in Drosophila melanogaster. The results demonstrate that the genetic architecture of body size contains an important component of variation contributed by the social environment, which is hidden to ordinary genetic analyses and opposes the direct effects of genes on body-size development within a population. Using a model of trait evolution, I show that these effects significantly alter evolutionary predictions by providing hidden constraints on phenotypic evolution. The importance of relatedness of interactants and the potential impact of kin selection on the evolution of body size are also examined.

Genomic imprinting and parent-of-origin effects on complex traits

Parent-of-origin effects occur when the phenotypic effect of an allele depends on whether it is inherited from the mother or the father. Several phenomena can cause parent-of-origin effects, but the best characterized is parent-of-origin-dependent gene expression associated with genomic imprinting. The development of new mapping approaches applied to the growing abundance of genomic data has demonstrated that imprinted genes can be important contributors to complex trait variation. Therefore, to understand the genetic architecture and evolution of complex traits, including complex diseases and traits of agricultural importance, it is crucial to account for these parent-of-origin effects. Here, we discuss patterns of phenotypic variation associated with imprinting, evidence supporting its role in complex trait variation and approaches for identifying its molecular signatures.