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

Abstract

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 (N _e) and genetic diversity. Empirical evidence reported so far is equivocal, with some but not all studies supporting a higher adaptive substitution rate in large-N _e than in small-N _e species. We gathered coding sequence polymorphism data and estimated the adaptive amino-acid substitution rate ω _a, 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 ω _a 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 ω _a and θ at a larger taxonomic scale, suggesting that the proportion of beneficial mutations scales negatively with species' long-term N _e.

Author summary

The determinants of the rate at which species adapt to environmental changes are so far poorly understood. In particular, whether adaptation is limited by the mutation supply, which is linked to species population size, is still an open question despite its importance in conservation biology.

Here, we used a comparative population genomic approach to assess the effect of the population mutation supply (approximated by the genetic diversity) on the adaptive substitution rate in animals.

For this we build and analyze a large coding sequence polymorphism dataset covering 50 species from ten diverse groups of animals including insects, molluscs, annelids, birds, and mammals. Thanks to our stratified sampling strategy, which allowed us to compare closely-related and distantly-related species in a single analysis, we reveal that (i) the supply of beneficial mutations only limits adaptation in low-diversity taxa, such as primates, but not in high-diversity taxa, such as fruit flies, and (ii) low-diversity taxa do not accumulate adaptive substitutions at a slower rate that high diversity taxa, as usually assumed, which may be due to the influence of long-term life history strategies on the proportion of adaptive mutations.