inclusive fitness 50 years on...,

royalsociety | The cardinal problem of evolutionary biology is to explain adaptation, or the appearance of design in the living world [1,2]. Darwin [3] convincingly argued that the process of adaptation is driven by natural selection: those heritable variations—i.e. genes—that are associated with greater individual reproductive success are those that will tend to accumulate in natural populations. To the extent that the individual's genes are causally responsible for her improved fitness, natural selection leads to the individual appearing designed as if to maximize her fitness. Thus, Darwinism is a theory of both the process and the purpose of adaptation. 

However, correlations between an individual's genes and her fitness need not reflect a direct, causal relationship. For example, genes for altruism can be associated with greater fitness, despite the direct cost that they inflict on their bearer, if relatives interact as social partners. This is because an individual who carries genes for altruism will tend to have more altruistic social partners. That altruism can be favoured by natural selection suggests that the purpose of adaptation is not, in general, to maximize the individual's personal fitness [4]. 

Although Darwin [3] recognized the potential for such indirect effects to drive the evolution of social behaviours, discussing the logic of kin selection theory in connection with the adaptations of sterile insect workers, it was William D. Hamilton (figure 1), more than a century later, who developed these insights into a full mathematical theory. By quantifying the relative strengths of direct selection, acting via the individual's own reproduction, and indirect selection, acting via the reproduction of the individual's relatives, Hamilton [4] revealed the ultimate criterion that natural selection uses to judge the fate of genes. 

Hamilton's rule states that any trait—altruistic or otherwise—will be favoured by natural selection if and only if the sum of its direct and indirect fitness effects exceeds zero [4–7]. That is where –c is the impact that the trait has on the individual's own reproductive success, b_i is its impact on the reproductive success of the individual's ith social partner and r_i is the genetic relatedness of the two individuals. This mathematical partition of fitness effects underpins the kin selection approach to evolutionary biology [8]. The general principle is that with regards to social behaviours, natural selection is mediated by any positive or negative consequences for recipients, according to their genetic relatedness to the actor. Consequently, individuals should show greater selfish restraint, and can even behave altruistically, when interacting with closer relatives [4]. 

Having clarified the process of social adaptation, Hamilton [4] revealed its true purpose: to maximize inclusive fitness (figure 2). That is, Darwinian individuals should strive to maximize the sum of the fitness effects that they have on all their relatives (including themselves), each increment or decrement being weighted by their genetic relatedness. This is the most fundamental revision that has been made to the logic of Darwinism and—aside from a possibly apocryphal quip attributed to J. B. S. Haldane, to the effect that he would give his life to save the lives of two brothers or eight cousins—it was wholly original to Hamilton.