Mating systems and recombination landscape strongly shape genetic diversity and selection in wheat relativesShow others and affiliations
2024 (English)In: Evolution Letters, E-ISSN 2056-3744, Vol. 8, no 6, p. 866-880Article in journal (Refereed) Published
Abstract [en]
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. Aegilops/Triticum grass species are the wild relatives of cultivated wheat. A main difference among these species is their mating system. Some species need to cross-fertilize to reproduce (outcrossing); some species mostly reproduce by auto-fertilization (selfing), while others reproduce by a mixture of outcrossing and selfing (mixed mating). The mating system has a strong impact on the genetic diversity, with selfing species usually exhibiting much lower diversity than outcrossing relatives. However, the reasons for this are not fully clear. Here, we show that selfing strongly reduces the diversity across the entire genome mainly because genome-wide linkage disequilibrium amplifies the effect of selection either against deleterious mutations or in favor of beneficial ones. Only outcrossing species showed genomic signatures of recurrent adaptation, suggesting that self-fertilization may have a long-term impact on species ability to evolve and adapt.
Place, publisher, year, edition, pages
Oxford University Press, 2024. Vol. 8, no 6, p. 866-880
Keywords [en]
self-fertilization, polymorphism, linked selection, fitness effect of mutations, selfing syndrome
National Category
Evolutionary Biology Genetics and Genomics
Identifiers
URN: urn:nbn:se:uu:diva-554852DOI: 10.1093/evlett/qrae039ISI: 001288347000001PubMedID: 39677571OAI: oai:DiVA.org:uu-554852DiVA, id: diva2:1953114
2025-04-172025-04-172025-04-17Bibliographically approved