Recombination facilitates adaptive evolution in rhizobial soil bacteria

Abstract

AbstractHomologous recombination is expected to increase natural selection efficacy by decoupling the fate of beneficial and deleterious mutations and by readily creating new combinations of beneficial alleles. Here, we investigate how the proportion of amino acid substitutions fixed by adaptive evolution (α) depends on the recombination rate in bacteria. We analyze 3086 core protein-coding sequences from 196 genomes belonging to five closely-related species of the genus Rhizobium. These genes are found in all species and do not display any signs of introgression between species. We estimate α using the site frequency spectrum (SFS) and divergence data for all pairs of species. We evaluate the impact of recombination within each species by dividing genes into three equally sized recombination classes based on their average level of intragenic linkage disequilibrium. We find that α varies from 0.07 to 0.39 across species and is positively correlated with the level of recombination. This is both due to a higher estimated rate of adaptive evolution and a lower estimated rate of non-adaptive evolution, suggesting that recombination both increases the fixation probability of advantageous variants and decreases the probability of fixation of deleterious variants. Our results demonstrate that homologous recombination facilitates adaptive evolution measured by α in the core genome of prokaryote species in agreement with studies in eukaryotes.Significance statementWhether intraspecific homologous recombination has a net beneficial or detrimental effect on adaptive evolution is largely unexplored in natural bacterial populations. We address this question by evaluating polymorphism and divergence data across the core genomes of 196 bacterial sequences––belonging to five closely related species of the genus Rhizobium. We show that the proportion of amino acid changes fixed due to adaptive evolution (α) increases with an increased recombination rate. This correlation is observed both in the interspecies and intraspecific comparisons. By using a population genetics approach our results demonstrate that homologous recombination directly impacts the efficacy of natural selection in the core genome of prokaryotes, as previously reported in eukaryotes.