Genetic architecture and evolutionary constraint SEE COMMENTARY when the environment contains genes Jason B. Wolf* Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN 37996 Edited by Mary Jane West-Eberhard, Smithsonian Tropical Research Institute, Ciudad Universitaria, Costa Rica, and approved January 21, 2003 (received for review September 19, 2002) The environment provided by conspecifics is often the most im- to investigate the genetic and evolutionary consequences of portant component of the environment experienced by individu- social influences on trait expression (8). IGEs are best under- als, frequently having profound effects on fitness and trait expres- stood by contrasting them with direct genetic effects (DGEs). sion. Although these social effects on fitness and trait expression DGEs occur when genes possessed by an individual directly may appear to be purely environmental, they differ from other influence that individual’s phenotype. In contrast, IGEs occur sorts of environmental influences, because they can have a genetic when genes expressed in one individual have phenotypic effects basis and thus can contribute to evolution. Theory has shown that in another (6, 8). IGE models solve the duality of these effects, these effects modify the definition of genetic architecture by as both environmental and genetic, by explicitly including the making the phenotype the property of the genotypes of multiple genetic basis of the environment in the definition of the indi- individuals and alter evolutionary dynamics by introducing addi- vidual phenotype (6, 9, 10). By using this approach, these models tional heritable components contributing to trait evolution. These have demonstrated that IGEs can alter our view of genetic effects suggest that genetic and evolutionary analyses of traits architecture, because the phenotype becomes the property of the influenced by social environments must incorporate the genetic genotypes of multiple individuals (6). The mapping of the components of variation contributed by these environments. How- individual phenotype to multiple genotypes can make the ge- ever, empirical studies incorporating these effects are generally netics of these traits particularly complex, because genetic lacking. In this paper, I quantify the contribution of genetically analysis requires some understanding of interactions between EVOLUTION based environmental effects arising from social interactions during individuals (9). The altered genetic architecture can also lead to group rearing to the quantitative genetics of body size in Dro- very different evolutionary dynamics, such as accelerated or sophila melanogaster. The results demonstrate that the genetic retarded responses to selection (6, 9, 10). Although IGEs can architecture of body size contains an important component of result from any sort of social interaction, with few exceptions (6, variation contributed by the social environment, which is hidden to 9), IGE models have focused on the particular influence that ordinary genetic analyses and opposes the direct effects of genes maternal genotypes have on the expression of traits in their on body-size development within a population. Using a model of offspring (so-called maternal genetic effects; see ref. 10). trait evolution, I show that these effects significantly alter evolu- IGE models are analogous to, but more general than, models tionary predictions by providing hidden constraints on phenotypic derived to examine kin selection (11–15). These models focus on evolution. The importance of relatedness of interactants and the the effect that genes in one individual have on the fitness of potential impact of kin selection on the evolution of body size are related individuals, and thus they are implicitly IGE models (e.g., also examined. equation 1 in ref. 11). These models have primarily been developed to gain an understanding of the conditions under ince its origin, one of the major goals of genetics has been to which altruism can evolve. Cheverud (12) made the relationship Sunderstand the relative contribution of heritable and envi- between kin selection and IGE models explicit by using a QG ronmental factors to trait variation. Quantitative genetic (QG) model of maternal effects on a fitness-related trait of progeny. methods have been developed as the primary means to achieve The QG model of Cheverud, and other more general related this goal, generally with the ultimate goal of understanding the models (13, 14, 16), can be used to model evolution by kin evolutionary potential of traits (1). QG analyses use statistical selection when IGEs directly affect either fitness or fitness- approaches that rely on hypothetical constructs, devised to related traits. Like kin-selection models, IGE models predict reflect causative influences producing variation in traits (e.g., that the evolutionary dynamics of traits can be strongly influ- ref. 2), to partition phenotypic variation into heritable compo- enced by the degree of relatedness of interactants. nents that contribute to trait evolution and nonheritable com- Despite the fact that theoretical models have demonstrated ponents that do not. The success of the QG approach for this that evolutionary dynamics can be quite different when IGEs are purpose depends critically on the validity of the underlying present, there is an absence of empirical studies that have model (3). Because of the primary interest in trait evolution, quantified the occurrence of IGEs outside of the parent– most analyses focus on the genetic components, casting envi- offspring interaction. There have been, however, a number of ronmental influences aside as sources of nonheritable random experiments that have implied the presence of IGEs (17–20), variation. However, in the case of the social environment (i.e., although none of these studies explicitly quantified their impor- the environment provided by conspecifics), there can be a tance. To investigate the importance of IGEs arising from other genetic component to the environment, because it is created by types of social interactions, this study focuses on the develop- traits expressed by individuals. This genetic component of the ment of body size in Drosophila melanogaster. Many aspects of environment blurs the distinction between genetic and envi- developmental and quantitative genetics are well understood in ronmental effects and thereby complicates the definition of genetic architecture. Because the environment itself can have a genetic basis, it can evolve. As a result, it must be included This paper was submitted directly (Track II) to the PNAS office. in genetic analysis if one wishes to gain a thorough under- Abbreviations: QG, quantitative genetic; IGE, indirect genetic effect; DGE, direct genetic standing of trait evolution (4–8). effect; sib, sibling. A modeling scheme that incorporates indirect genetic effects See commentary on page 4357. (IGEs) [also known as associate effects (9)] has been developed *E-mail: [email protected]. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0635741100 PNAS ͉ April 15, 2003 ͉ vol. 100 ͉ no. 8 ͉ 4655–4660 Downloaded by guest on September 29, 2021 ϩ D. melanogaster. This species has been one of the main model The first composite term on the right side of Eq. 3 [(Gff ␤ organisms for studies of developmental genetics (21) and has GfS) f] gives the response to selection when social partners are been extensively studied from a QG perspective (1). Despite this unrelated. This term illustrates that the evolution of a character enormous body of work, no previous investigation has directly described by Eq. 1 is determined by both changes in average ␤ examined the contribution of IGEs to genetic architecture, contribution of DGEs (Gff f) and correlated changes in the ␤ although previous work suggests that they should play an im- average contribution of IGEs via the social environment (GfS f). portant role in trait expression (22–25). Because flies develop The term also demonstrates that, when interacting individuals under high densities in an environment largely created by are unrelated, selection cannot act directly on the IGE compo- conspecifics [through the excretion of biotic residues (24), nent, because IGEs do not directly map to the individual ⌬៮ egestion of digestive enzymes (26), mechanical processing of phenotype (i.e., GSS does not contribute to zf). However, the medium, and direct competition for nutrients], there is consid- IGE component can evolve as a result of a correlated response erable opportunity for IGEs to affect development. To examine to selection when there is a genetic covariance between DGEs the importance of IGEs in this system, I begin by presenting a and IGEs. The change in the IGE component can be seen as an ៮ simple model of trait development and evolution that incorpo- evolutionary change in the mean social environment (⌬S), which rates IGEs (6). This model also forms the foundation for QG contributes to the cross-generational change in the mean phe- analysis by providing the expected components of variation used notype. Traditional QG models do not include this last term and in partition phenotypic variation into IGEs, DGEs, and their predict response to selection solely on the basis of strength of covariance. selection and direct additive genetic variance. Thus, the response to selection can be greater or less than expected from the A Model of Trait Expression and Evolution traditional QG model. When GfS is greater than Gff, the response Influences on