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

Marjolaine Rousselle,Benoit Nabholz,Marie-Ka Tilak,Emeric Figuet,Paul Simion,Nicolas Galtier,Jianzhi Zhang

doi:10.1371/journal.pgen.1008668

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 (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.

Highlights

It is widely recognized that adaptation is more efficient in large populations
Our results suggest that factors linked to species long-term effective population size affect the distribution of the fitness effects (DFE), i.e., the proportion and rate of beneficial mutation would be non-independent of the long-term Ne
We sampled a large variety of animals species and demonstrated a timescaledependent relationship between the adaptive substitution rate and the population mutation rate, that reconciles previous studies that were conducted at different taxonomic scales

Summary

Introduction

Large populations produce a greater number of mutants per generation than small ones, and for this reason are more likely to find the alleles required for adaptation, if missing from the gene pool. Large populations tend to be genetically more diverse and more likely to carry the alleles needed to respond to environmental changes [1]. The fixation probability of beneficial mutations is higher in large than in small populations due to the weaker effect of genetic drift in the former. Whether it be from standing variation or de novo mutations, one would expect to observe a higher rate of accumulation of adaptive changes, on average, in large than in small populations [2].

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Conclusion