Do genetic drift and accumulation of deleterious mutations preclude adaptation? Empirical investigation using RADseq in a northern lacustrine fish

Abstract

Understanding genomic signatures of divergent selection underlying long-term adaptation in populations located in heterogeneous environments is a key goal in evolutionary biology. In this study, we investigated neutral, adaptive and deleterious genetic variation using 7,192 SNPs in 31 Lake Trout (Salvelinus namaycush) populations (n = 673) from Québec, Canada. Average genetic diversity was low, weakly shared among lakes, and positively correlated with lake size, indicating a major role for genetic drift subsequent to lake isolation. Putatively deleterious mutations were on average at lower frequencies than the other SNPs, and their abundance relative to the entire polymorphism in each population was positively correlated with inbreeding, suggesting that the effectiveness of purifying selection was negatively correlated with inbreeding, as predicted from theory. Despite evidence for pronounced genetic drift and inbreeding, several outlier loci were associated with temperature and found in or close to genes with biologically relevant functions notably related to heat stress and immune responses. Outcomes of gene-temperature associations were influenced by the inclusion of the most inbred populations, in which allele frequencies deviated the most from model predictions. This result illustrates challenge in identifying gene-environment associations in cases of high genetic drift and restricted gene flow and suggests limited adaptation in populations experiencing higher inbreeding. We discuss the relevance of these findings for the conservation and management, notably regarding stocking and genetic rescue, of Lake Trout populations and other species inhabiting highly fragmented habitats.

Impact of supplementation on deleterious mutation distribution in an exploited salmonid

“…Detection of putative outliers was performed using two approaches: (a) SNPs potentially under balancing and divergent selection were identified using BAYESCAN v.2.1 (Foll & Gaggiotti, ) and (b) SNPs under polygenic selection linked to temperature were detected using a random forest algorithm (Boulesteix, Janitza, Kruppa, & Konig, ; Chen & Ishwaran, ; Goldstein, Polley, & Briggs, ). This second step was produced because different seasonal temperature variables may impose different selective pressures on Lake Trout (Perrier et al., ). The putative outliers were subsequently removed from the SNP datasets, such that only putative neutrals remained (hereafter called “neutral markers”) for the subsequent analyses.…”

“…We used the Rainbow Trout transcriptome because it was the best transcriptome available among salmonids at the time we produced this work and for the sake of similarity with Perrier et al. (). All hits with a similarity higher than 25 amino acid of 26 possible (considering 80‐bp‐long read) and more than 95% similarity between the query read and the transcriptome sequence were retained.…”

“…Pronounced genetic differentiation has been documented among natural/unstocked Lake Trout populations (Halbisen & Wilson, ; McCracken, Perry, Keefe, & Ruzzante, ; Northrup, Connor, & Taylor, ; Perrier et al., ; Piller, Wilson, Lee, & Lyons, ; Valiquette, Perrier, Thibault, & Bernatchez, ). Intrapopulation genetic diversity is typically low in this species (Bernatchez, Laporte, Perrier, Sirois, & Bernatchez, ; Valiquette et al., ) and positively correlated with lake size (Perrier et al., ). Together, they indicate the major role of genetic drift for determining the genetic diversity in lakes after their isolation following the last glacial retreat (Wilson & Mandrak, ).…”

“…In a study dealing specifically on wild (unstocked populations), Perrier et al. () detected 124 putative deleterious variants across all lacustrine populations they surveyed. The frequencies of such deleterious mutations, relative to the entire polymorphism within populations, were positively correlated with inbreeding, suggesting that the efficacy of purifying selection was negatively correlated with local level of inbreeding.…”

Assessing thermal adaptation using family‐based association andFSToutlier tests in a threatened trout species

“…The full magnitude of divergence between the PPP broodstock and the wild populations was not apparent before this study. Small effective population size increases genetic drift and may have produced different alleles and genetic backgrounds in the wild versus hatchery populations (Messer & Petrov, ; Perrier et al, ), limiting our ability to find shared loci across populations and tests. The limited number of outliers detected by bayescan in the two wild lake populations (and in previous analyses of stream populations) probably reflects this.…”