Resolving fine‐scale population structure and fishery exploitation using sequenced microsatellites in a northern fish

Abstract

The resiliency of populations and species to environmental change is dependent on the maintenance of genetic diversity, and as such, quantifying diversity is central to combating ongoing widespread reductions in biodiversity. With the advent of next-generation sequencing, several methods now exist for resolving fine-scale population structure, but the comparative performance of these methods for genetic assignment has rarely been tested. Here, we evaluate the performance of sequenced microsatellites and a single nucleotide polymorphism (SNP) array to resolve fine-scale population structure in a critically important salmonid in north eastern Canada, Arctic Charr (Salvelinus alpinus). We also assess the utility of sequenced microsatellites for fisheries applications by quantifying the spatial scales of movement and exploitation through genetic assignment of fishery samples to rivers of origin and comparing these results with a 29-year tagging dataset. Self-assignment and simulation-based analyses of 111 genome-wide microsatellite loci and 500 informative SNPs from 28 populations of Arctic Charr in north-eastern Canada identified largely river-specific genetic structure. Despite large differences (~4X) in the number of loci surveyed between panels, mean self-assignment accuracy was similar with the microsatellite loci and the SNP panel (>90%). Subsequent analysis of 996 fishery-collected samples using the microsatellite panel revealed that larger rivers contribute greater numbers of individuals to the fishery and that coastal fisheries largely exploit individuals originating from nearby rivers, corroborating results from traditional tagging experiments. Our results demonstrate the efficacy of sequence-based microsatellite genotyping to advance understanding of fine-scale population structure and harvest composition in northern and understudied species.

Fast sequence-based microsatellite genotyping development workflow

“…The ability of SSRseq to characterize SNP and indel present along the sequences, in addition to the targeted microsatellite, represents a new opportunity to produce empirical data to apply existing theoretical and statistical frameworks that integrate linked polymorphism with different mutation characteristics (Payseur & Cutter, 2006). Genotyping relying on sequence data that are easier to normalize than traditional capillary electrophoresis genotyping through automated bioinformatics pipelines will facilitate sharing of data between laboratories and incrementing genotypic database that are paramount for applications in wildlife monitoring (Bradbury et al, 2018;Layton et al, 2020) or agronomical research (Li et al, 2017;Yang et al, 2019). Finally, the ease of parallel development for multiple species make these approach convenient to develop powerful multilocus datasets for comparative population and community genetics studies (Crutsinger, 2016), and to further investigate the functional implications (Bagshaw, 2017) and adaptive potential of microsatellite variation among natural populations (Xie et al, 2019).…”

“…Sequence data thus reduces allele homoplasy because alleles of the same size may contain molecular variation that does not translate into size variation such as SNP, indels masking variation in repeat number, or presence of two adjacent SSR motifs with complementary size variation (Darby et al, 2016). As a result, SSRseq offers refined genetic diversity estimation and population structure inference (Darby et al, 2016;Bradbury et al, 2018;Neophytou et al, 2018;Viruel et al, 2018;Layton et al, 2020).…”

“…Updating microsatellite genotyping to modern technologies remains important for several reasons. Firstly, some current scientific questions in ecology or evolutionary biology can be answered using a moderate number (e.g., a dozen (Harrison et al, 2013) to a hundred (Bradbury et al, 2018;Layton et al, 2020)) of highly polymorphic multi-allelic loci such as microsatellites. Secondly, variation in the number of repeated oligonucleotide motif is a unique kind of polymorphism with specific mutation mechanism and rate which in itself provides a complementary picture of genetic variation to nucleotide substitutions across populations (Haasl & Payseur, 2011) and genomes (Willems et al, 2014).…”

Population structure and genomic evidence for local adaptation to freshwater and marine environments in anadromous Arctic Char (Salvelinus alpinus) throughout Nunavik, Québec, Canada

“…In marine environments, Arctic Char tend to stay near the surface (< 3m), with occasional dives up to 50m (Harris et al 2020; Spares, Stokesbury, O’Dor & Dick, 2012) and preferably use nearshore habitats within 100 km from their natal river’s mouth (Dempson & Kristofferson, 1987; Layton et al, 2020; Moore et al 2016). Thus, one could expect this behaviour to lead to Arctic Char populations experiencing more diverse marine conditions than other anadromous species.…”

Peer Review #2 of "Fast sequence-based microsatellite genotyping development workflow (v0.2)"

“…Firstly, some current scientific questions in ecology or evolutionary biology can be answered using a moderate number (e.g. a dozen (Harrison et al, 2013) to a hundred (Bradbury et al, 2018;Layton et al, 2020)) of highly polymorphic multi-allelic loci such as microsatellites. Secondly, variation in the number of repeated oligonucleotide motif is a unique kind of polymorphism with specific mutation mechanism and rate which in itself provides a complementary picture of genetic variation to nucleotide substitutions across populations (Haasl & Payseur, 2011) and genomes (Willems et al, 2014).…”