Mating systems and recombination landscape strongly shape genetic diversity and selection in wheat relatives

Abstract

Abstract How and why genetic diversity varies among species is a long-standing question in evolutionary biology. Life history traits have been shown to explain a large part of observed diversity. Among them, mating systems have one of the strongest impacts on genetic diversity, with selfing species usually exhibiting much lower diversity than outcrossing relatives. Theory predicts that a high rate of selfing amplifies selection at linked sites, reducing genetic diversity genome-wide, but frequent bottlenecks and rapid population turn-over could also explain low genetic diversity in selfers. However, how linked selection varies with mating systems and whether it is sufficient to explain the observed difference between selfers and outcrossers has never been tested. Here, we used the Aegilops/Triticum grass species, a group characterized by contrasted mating systems (from obligate outcrossing to high selfing) and marked recombination rate variation across the genome, to quantify the effects of mating system and linked selection on patterns of neutral and selected polymorphism. By analyzing phenotypic and transcriptomic data of 13 species, we show that selfing strongly affects genetic diversity and the efficacy of selection by amplifying the intensity of linked selection genome-wide. In particular, signatures of adaptation were only found in the highly recombining regions in outcrossing species. These results bear implications for the evolution of mating systems and, more generally, for our understanding of the fundamental drivers of genetic diversity.