Demographic Processes Linked to Genetic Diversity and Positive Selection across a Species' Range

Abstract

Demography determines the strength of genetic drift, which generally reduces genetic variation and the efficacy of selection. Here, we disentangled the importance of demographic processes at a local scale (census size and mating system) and at a species-range scale (old split between population clusters, recolonization after the last glaciation cycle, and admixture) in determining within-population genomic diversity and genomic signatures of positive selection. Analyses were based on re-sequence data from 52 populations of North American Arabidopsis lyrata collected across its entire distribution. The mating system and range dynamics since the last glaciation cycle explained around 60% of the variation in genomic diversity among populations and 52% of the variation in the signature of positive selection. Diversity was lowest in selfing compared with outcrossing populations and in areas further away from glacial refugia. In parallel, reduced positive selection was found in selfing populations and in populations with a longer route of postglacial range expansion. The signature of positive selection was also reduced in populations without admixture. We conclude that recent range expansion can have a profound influence on diversity in coding and non-coding DNA, similar in magnitude to the shift toward selfing. Distribution limits may in fact be caused by reduced effective population size and compromised positive selection in recently colonized parts of the range.