Abstract

BackgroundTheory and artificial selection experiments show that recombination can promote adaptation by enhancing the efficacy of natural selection, but the extent to which recombination affects levels of adaptation across the genome is still an open question. Because patterns of molecular evolution reflect long-term processes of mutation and selection in nature, interactions between recombination rate and genetic differentiation between species can be used to test the benefits of recombination. However, this approach faces a major difficulty: different evolutionary processes (i.e. negative versus positive selection) produce opposing relationships between recombination rate and genetic divergence, and obscure patterns predicted by individual benefits of recombination.ResultsWe use a combination of polymorphism and genomic data from the yeast Saccharomyces cerevisiae to infer the relative importance of nearly-neutral (i.e. slightly deleterious) evolution in different gene categories. For genes with high opportunities for slightly deleterious substitution, recombination substantially reduces the rate of molecular evolution, whereas divergence in genes with little opportunity for slightly deleterious substitution is not strongly affected by recombination.ConclusionThese patterns indicate that adaptation throughout the genome can be strongly influenced by each gene's recombinational environment, and suggest substantial long-term fitness benefits of enhanced purifying selection associated with sexual recombination.

Highlights

  • Theory and artificial selection experiments show that recombination can promote adaptation by enhancing the efficacy of natural selection, but the extent to which recombination affects levels of adaptation across the genome is still an open question

  • Because recombination rates vary between different regions of a genome [e.g. yeast: [8]; Drosophila: [9]; Mammals: [10]; plants: [11]], adaptation at the molecular level might be strongly affected by each gene's recombinational environment – genes evolving in low recombination regions are expected to be poorly adapted relative to those in high recombination regions [12,13]

  • Comparative genome analyses are potentially useful for assessing whether recombination promotes adaptation because long-term evolutionary processes are reflected in patterns of genetic divergence between species [13,14,15,16,17,18,19]

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Summary

Introduction

Theory and artificial selection experiments show that recombination can promote adaptation by enhancing the efficacy of natural selection, but the extent to which recombination affects levels of adaptation across the genome is still an open question. Because patterns of molecular evolution reflect long-term processes of mutation and selection in nature, interactions between recombination rate and genetic differentiation between species can be used to test the benefits of recombination. This approach faces a major difficulty: different evolutionary processes (i.e. negative versus positive selection) produce opposing relationships between recombination rate and genetic divergence, and obscure patterns predicted by individual benefits of recombination. Comparative genome analyses are potentially useful for assessing whether recombination promotes adaptation because long-term evolutionary processes are reflected in patterns of genetic divergence between species [13,14,15,16,17,18,19]. Genomic approaches face a major challenge – multiple processes can contribute to evolutionary divergence between species and each predicts a different relationship between protein evolution and recombination (page number not for citation purposes)

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