Understanding the impacts of current human activities on within-species genetic variation requires a thorough description of the historical factors that have shaped the genomic and geographical distribution of nucleotide diversity. Past and current conditions influencing effective population size have important evolutionary implications for the efficacy of selection, increased accumulation of deleterious mutations, and loss of adaptive potential under the nearly neutral theory. Here, we gather extensive genome-wide data that represent the extant diversity of the Coho salmon (Oncoryhnchus kisutch) to address three issues. First, we demonstrate that a single glacial refugium is the source of the majority of present-day genetic diversity, with minor but detectable inputs from secondary micro-refugia. We propose a scenario whereby several ancestral populations located south of the ice sheets expanded in postglacial time, swamping out most of the diversity from other putative micro-refugia. Following this expansion, we identify particular populations having undergone continuous declines in population size (Ne). Second, we combine multiple evidence from demographic modelling, analysis of recombination landscape, and genome-wide landscape of diversity to demonstrate that selection at linked sites and Hill-Robertson interference played a major role in shaping genetic diversity across the Coho salmon genome. Third, we demonstrate that this demographic history generated subtle differences in the load of deleterious mutations among populations, a finding that mirrors recent results from human populations. Taken together, we found considerable support for the joint contributions of demographic history and linked selection in the load of deleterious mutations. We suggest that these inferences should be better integrated in conservation genetics of managed fish species which currently focuses largely on within-population adaptation.
Author SummaryReconstruction of a species' past demographic history from genome-wide data allows understanding how historical factors interact with intrinsic genomic properties to shape the distribution of genetic diversity along its genome and its geographic range. Here, we combine genotyping-by-sequencing and whole genome sequence data with demographic modelling to address these issues in the Coho salmon, a Pacific salmon species with rapidly declining census size in some parts of its range, notably in the south. Our demographic reconstructions indicate a linear decrease in genetic diversity towards the north of the species range, supporting the hypothesis of a major southern refugia for the Coho salmon and a northern route of postglacial recolonization. Accordingly, the number of candidate deleterious homozygous derived mutations was higher in northern populations. Demographic modelling also suggested the existence of cryptic refugia that may have been missed with the use of simpler summary statistics. We further showed that the species' genome was shaped by linked selection and biased gene conv...