When Do Individuals Maximize Their Inclusive Fitness?

Adaptation is often described in behavioral ecology as individuals maximizing their inclusive fitness. Under what conditions does this hold, and how does this relate to the gene-centered perspective of adaptation? We unify and extend the literature on these questions to class-structured populations. We demonstrate that the maximization (in the best-response sense) of class-specific inclusive fitness obtains in uninvadable population states (meaning that all deviating mutants become extinct). This defines a genuine actor-centered perspective on adaptation. But this inclusive fitness is assigned to all bearers of a mutant allele in a given class and depends on distributions of demographic and genetic contexts. These distributions, in turn, usually depend on events in previous generations and are thus not under individual control. This prevents, in general, envisioning individuals themselves as autonomous fitness maximizers, each with its own inclusive fitness. For weak selection, however, the dependence on earlier events can be neglected. We then show that each individual in each class appears to maximize its own inclusive fitness when all other individuals exhibit inclusive fitness-maximizing behavior. This defines a genuine individual-centered perspective of adaptation and justifies formally, as a first-order approximation, the long-heralded view of individuals appearing to maximize their own inclusive fitness.