Broad-scale signatures of linked selection under divergent recombination landscapes and mating systems in natural populations of rye and barley

Abstract

Understanding the interactions between patterns of recombination, mating systems, and signatures of natural selection is a central aim in evolutionary biology. Patterns of recombination shape the evolution of genomes by affecting the efficacy of selection. Within populations, genetic shuffling is achieved through meiotic recombination, random chromosome segregation, and the frequency of outbreeding. Recombination landscapes vary between species and populations, and are further influenced by mating systems. Here, we use populations of two related grass species, rye (Secale cereale) and barley (Hordeum vulgare ssp. spontaneum), that differ in their mating system, to analyse signatures of linked selection under divergent recombination landscapes. Rye (outbreeding) and barley (inbreeding) are members of the Poaceae and diverged approximately 15 M years ago. We estimated population recombination rates, analysed patterns of genetic diversity, identified signatures of linked selection, and quantified the fraction and functional class of genes affected by linked selection. In this comparison, we detected signatures of linked selection in low-recombining regions in both species. In inbreeding barley, the low-recombining fraction of the genome was more than 2-fold larger than in outbreeding rye. Furthermore, considering differences in gene density across the genome, approximately 1.5 times more genes were affected by linked selection in barley than in rye. In both species, genomic regions affected by linked selection harbour mostly genes involved in basic cellular processes. We provide empirical evidence for quantitative differences in recombination landscapes between closely related species of divergent mating systems, and discuss the consequences of linked selection and the efficacy of natural selection. Significance statementThe ability of natural selection to disentangle beneficial from deleterious mutations across the genome is shaped by patterns of recombination, yet our understanding of the magnitude of this interaction is incomplete. In our work, we show that patterns of recombination differ between related outbreeding and inbreeding grass species, and that the efficacy of selection differs between them. We provide empirical evidence for quantitative differences in recombination landscapes and patterns of selection.