Is adaptation limited by mutation? A timescale-dependent effect of genetic diversity on the adaptive substitution rate in animals

Whether adaptation is limited by the beneficial mutation supply is a long-standing question of evolutionary genetics, which is more generally related to the determination of the adaptive substitution rate and its relationship with species effective population size (Ne) and genetic diversity. Empirical evidence reported so far is equivocal, with some but not all studies supporting a higher adaptive substitution rate in large-Ne than in small-Ne species. We gathered coding sequence polymorphism data and estimated the adaptive amino-acid substitution rate ωa, in 50 species from ten distant groups of animals with markedly different population mutation rate θ. We reveal the existence of a complex, timescale dependent relationship between species adaptive substitution rate and genetic diversity. We find a positive relationship between ωa and θ among closely related species, indicating that adaptation is indeed limited by the mutation supply, but this was only true in relatively low-θ taxa. In contrast, we uncover no significant correlation between ωa and θ at a larger taxonomic scale, suggesting that the proportion of beneficial mutations scales negatively with species' long-term Ne.