Evolution in a genetically heritable social environment.

N early 40 years ago W. D. Hamilton (1) published his classic paper on the genetic evolution of social behavior. His mathematical theory of kin selection and the related concept of inclusive fitness played a major role in redirecting the evolutionary study of social behavior and accounting for apparently altruistic phenotypes observed in nature. Since that time, and especially after publication of E. O. Wilson’s book on sociobiology (2), the evolution of social behavior in animals has been studied as the balance between the fitness costs of behavior performed relative to the fitness benefits accrued by kin. This balance is summarized in Hamilton’s rule, altruism will increase in a population when the genetic correlation among interacting individuals (r) exceeds the ratio of costs to benefits ( c b). The development of sociobiology has been seen as a triumph for the application of the principles of Darwinian evolution to the understanding of social behavior. Darwinian evolutionary theory states that evolutionary change occurs through the natural selection of heritable variation. However, there remains a difficulty with traditional kin selection theory as a model of Darwinian evolution. Most models of kin selection fail to adequately account for the nature of heritable variation in systems of interacting individuals (3) and heritable variation is a key partner with selection in the evolutionary process. In this issue of PNAS, Wolf (4) provides an explicit, general model and an experimental system in which it is possible to fully define and measure heritable variation in systems of interacting individuals. The key concept in this model is that an individual’s characteristics are inf luenced by two kinds of genetic effects; direct genetic effects (DGEs) of the genes carried by that individual on its own traits and indirect genetic effects (IGEs) of genes carried by others. These indirect genetic effects are the effects of genes carried by an individual on the developmental environment of their social partners. A key and truly innovative element of Hamilton’s (1) kin selection model was to explicitly consider these indirect effects. However, in doing so, the potential direct effects of these genes on an individual’s characteristics were ignored. The approach taken by Wolf (4) has a long history that until recently has had little impact on studies of the evolution of social behavior. Given its origins, I will refer to it as the quantitative genetic kin selection model. Agricultural geneticists are faced with practical problems in scientific breeding and develop models to address these problems and guide their stock improvement plans. A particularly important and difficult problem involved selection for neonatal and early postnatal growth traits. These traits were sometimes refractory to artificial selec-