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.
Since its origin, one of the major goals of genetics has been to understand the relative contribution of heritable and environmental factors to trait variation. Quantitative genetic (QG) methods have been developed as the primary means to achieve this goal, generally with the ultimate goal of understanding the evolutionary potential of traits (1). QG analyses use statistical approaches that rely on hypothetical constructs, devised to reflect causative influences producing variation in traits (e.g., ref.2), to partition phenotypic variation into heritable components that contribute to trait evolution and nonheritable components that do not. The success of the QG approach for this purpose depends critically on the validity of the underlying model (3). Because of the primary interest in trait evolution, most analyses focus on the genetic components, casting environmental influences aside as sources of nonheritable random variation. However, in the case of the social environment (i.e., the environment provided by conspecifics), there can be a genetic component to the environment, because it is created by traits expressed by individuals. This genetic component of the environment blurs the distinction between genetic and environmental effects and thereby complicates the definition of genet...