Dioecy Is Associated with High Genetic Diversity and Adaptation Rates in the Plant Genus Silene

TY - JOUR

T1 - Dioecy Is Associated with High Genetic Diversity and Adaptation Rates in the Plant Genus Silene

AU - Muyle, Aline

AU - Martin, Hélène

AU - Zemp, Niklaus

AU - Mollion, Maéva

AU - Gallina, Sophie

AU - Tavares, Raquel

AU - Silva, Alexandre

AU - Bataillon, Thomas

AU - Widmer, Alex

AU - Glémin, Sylvain

AU - Touzet, Pascal

AU - Marais, Gabriel A.B.

N1 - Publisher Copyright: © The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. Copyright: This record is sourced from MEDLINE/PubMed, a database of the U.S. National Library of Medicine

PY - 2021/3/1

Y1 - 2021/3/1

N2 - About 15,000 angiosperm species (∼6%) have separate sexes, a phenomenon known as dioecy. Why dioecious taxa are so rare is still an open question. Early work reported lower species richness in dioecious compared with nondioecious sister clades, raising the hypothesis that dioecy may be an evolutionary dead-end. This hypothesis has been recently challenged by macroevolutionary analyses that detected no or even positive effect of dioecy on diversification. However, the possible genetic consequences of dioecy at the population level, which could drive the long-term fate of dioecious lineages, have not been tested so far. Here, we used a population genomics approach in the Silene genus to look for possible effects of dioecy, especially for potential evidence of evolutionary handicaps of dioecy underlying the dead-end hypothesis. We collected individual-based RNA-seq data from several populations in 13 closely related species with different sexual systems: seven dioecious, three hermaphroditic, and three gynodioecious species. We show that dioecy is associated with increased genetic diversity, as well as higher selection efficacy both against deleterious mutations and for beneficial mutations. The results hold after controlling for phylogenetic inertia, differences in species census population sizes and geographic ranges. We conclude that dioecious Silene species neither show signs of increased mutational load nor genetic evidence for extinction risk. We discuss these observations in the light of the possible demographic differences between dioecious and self-compatible hermaphroditic species and how this could be related to alternatives to the dead-end hypothesis to explain the rarity of dioecy.

AB - About 15,000 angiosperm species (∼6%) have separate sexes, a phenomenon known as dioecy. Why dioecious taxa are so rare is still an open question. Early work reported lower species richness in dioecious compared with nondioecious sister clades, raising the hypothesis that dioecy may be an evolutionary dead-end. This hypothesis has been recently challenged by macroevolutionary analyses that detected no or even positive effect of dioecy on diversification. However, the possible genetic consequences of dioecy at the population level, which could drive the long-term fate of dioecious lineages, have not been tested so far. Here, we used a population genomics approach in the Silene genus to look for possible effects of dioecy, especially for potential evidence of evolutionary handicaps of dioecy underlying the dead-end hypothesis. We collected individual-based RNA-seq data from several populations in 13 closely related species with different sexual systems: seven dioecious, three hermaphroditic, and three gynodioecious species. We show that dioecy is associated with increased genetic diversity, as well as higher selection efficacy both against deleterious mutations and for beneficial mutations. The results hold after controlling for phylogenetic inertia, differences in species census population sizes and geographic ranges. We conclude that dioecious Silene species neither show signs of increased mutational load nor genetic evidence for extinction risk. We discuss these observations in the light of the possible demographic differences between dioecious and self-compatible hermaphroditic species and how this could be related to alternatives to the dead-end hypothesis to explain the rarity of dioecy.

KW - Allee effect

KW - angiosperms

KW - population genetics

KW - RNA-seq

KW - selection efficacy

KW - sexual systems

UR - http://www.scopus.com/inward/record.url?scp=85100100202&partnerID=8YFLogxK

U2 - 10.1093/molbev/msaa229

DO - 10.1093/molbev/msaa229

M3 - Journal article

C2 - 32926156

AN - SCOPUS:85100100202

SN - 0737-4038

VL - 38

SP - 805

EP - 818

JO - Molecular Biology and Evolution

JF - Molecular Biology and Evolution

IS - 3

ER -