Geography, environment, and colonization history interact with morph type to shape genomic variation in an Arctic fish

Abstract

Polymorphic species are useful models for investigating the evolutionary processes driving diversification. Such processes include colonization history as well as contemporary selection, gene flow, and genetic drift, which can vary between intraspecific morphs as a function of their distinct life histories. The interactive and relative influence of such evolutionary processes on morph differentiation critically informs morph‐specific management decisions and our understanding of incipient speciation. We therefore investigated how geographic distance, environmental conditions, and colonization history interacted with morph migratory capacity in the highly polymorphic fish species, Arctic Charr (Salvelinus alpinus). Using an 87 k SNP chip we genetically characterized recently evolved anadromous, resident, and landlocked charr collected from 45 locations across a secondary contact zone of three charr glacial lineages in eastern Canada. A strong pattern of isolation by distance across all populations suggested geographic distance principally shaped genetic structure. Landlocked populations had lower genetic diversities and higher genetic differentiation than anadromous populations. However, effective population size was generally temporally stable in landlocked populations in comparison to anadromous populations. Genetic diversity positively correlated with latitude, potentially indicating southern anadromous populations' vulnerability to climate change and greater introgression between the Arctic and Atlantic glacial lineages in northern Labrador. Local adaptation was suggested by the observation of several environmental variables strongly associating with functionally relevant outlier genes including a region on chromosome AC21 potentially associated with anadromy. Our results demonstrate that gene flow, colonization history, and local adaptation uniquely interact to influence the genetic variation and evolutionary trajectory of populations.

Historical and contemporary processes driving the origin and structure of an admixed population within a contact zone between subspecies of a north temperate diadromous fish

“…In addition, genotype–environmental association (GEA) analyses have been successfully conducted in salmonid fishes, including Salvelinus , as an alternative way to generate hypotheses about how inter‐locality environmental differences may shape adaptive genomic variation (e.g. Micheletti et al., 2018; Salisbury et al., 2023). Such GEA analyses could be a fruitful way to test the idea that loci associated with excess NDV ancestry at specific locations in the Chignik Lake watershed are associated with particular environmental features, but the relatively small scale of the watershed may limit the power to detect such associations.…”

Loci associated with maturation, migration and appetite control are linked with signals of fine-scale local selection in a large Atlantic salmon population

“…In addition, we performed RDA with a partial model accounting for population structure, and with a "full" model not accounting for it. These two models detected very different SNPs (Figure S5), which likely reflects that the partial model prevented the detection of many potentially adaptive environmental/climate-associated SNPs identified by the other analyses, especially on Chr 9, because of their strong association with population structure (Forester et al, 2018;Salisbury et al, 2023). Thus, we also consider the results of the full RDA model relevant (see Forester et al, 2018).…”

“…We identified candidate SNPs ("pRDA candidates" from the pRDA and "full RDA candidates" from the full RDA) by using a relatively liberal cut-off of loadings > 3 SD from the mean distribution of each of the two RDA axes (as in e.g. Forester et al, 2018;Salisbury et al, 2023) in each RDA, corresponding to a two-tailed p-value threshold of 0.0027. Furthermore, we used variance partitioning in partial RDA to gain estimates of the contributions of defined sets of variables on the total observed genetic variation in the dataset (Table S4), i.e.…”

Post-glacial recolonization and multiple scales of secondary contact contribute to contemporary Atlantic salmon (Salmo salar) genomic variation in North America

“…Genomic evaluations now permit the impacts of isolation and post-glacial recolonization to be quantified genome-wide and have revealed signatures of glacial isolation as well as evidence of post glacial secondary contact and introgression among lineages (e.g., Souissi et al 2018;Lehnert et al 2019;Salisbury et al 2023). These studies support the hypothesis that Pleistocene glaciations have been a significant determinant of contemporary diversity in northern marine species, which is likely to influence population and species response to climate change in the coming decades (e.g., Luqman et al 2023).…”