Invasion fitness, inclusive fitness, and reproductive numbers in heterogeneous populations
How should fitness be measured to determine which phenotype or “strategy” is uninvadable when evolution occurs in subdivided populations subject to local demographic and environmental heterogeneity? Several invasion fitness measures, such as basic reproductive number, lifetime dispersal success of a local lineage, or inclusive fitness have been proposed to address this question, but the relationships between them and their generality remains unclear. Here, we ascertain uninvadability (all mutant strategies always go extinct) in terms of the growth rate of a mutant allele arising as a single copy in a population. We show from this growth rate that uninvadability is equivalently characterized by at least three conceptually distinct invasion fitness measures: (i) lineage fitness, giving the average personal fitness of a randomly sampled mutant lineage member; (ii) inclusive fitness, giving a reproductive value weighted average of the direct fitness cost and relatedness weighted indirect fitness benefits accruing to a randomly sampled mutant lineage member; and (iii) three types of reproductive numbers, giving lifetime success of a local lineage. Our analysis connects approaches that have been deemed different, generalizes the exact version of inclusive fitness to class-structured populations, and provides a biological interpretation of selection on a mutant allele under arbitrary strength of selection.