The rate of adaptive molecular evolution in wild and domesticated Saccharomyces cerevisiae populations

Through its fermentative capacities, Saccharomyces cerevisiae was central in the development of civilization during the Neolithic period, and the yeast remains of importance in industry and biotechnology giving rise to bona fide domesticated lineages. Here, we conduct a population genomic study of both domesticated and wild lineages of S. cerevisiae. Using coalescent analyses, we report that the effective population size of yeast populations decreased since the divergence with S. paradoxus. We fitted models of distribution of fitness effects to population genomic data sets to infer the rate of adaptive non-synonymous substitutions in protein-coding genes. We report an overall limited contribution of positive selection to S. cerevisiae protein evolution, albeit with higher rates of adaptive evolution in wild compared to domesticated populations. We find that populations with a larger effective population size experience a lower rate of non-adaptive substitutions, as well as a higher rate of adaptive ones, suggesting that, in yeast, adaptive mutations accumulate at a faster rate in large populations. Our analyses revealed the signature of background selection but no Hill-Robertson interference, as recombination was found to mildly impact the efficacy of purifying selection and does not affect the rate of adaptive evolution in yeast. Conversely, the rate of adaptive non-synonymous substitutions is significantly correlated with the residue solvent exposure, a relation that cannot be explained by the population’s demography. Together, our results provide a detailed characterization of adaptive mutations across S. cerevisiae genomes and populations.