Standing genetic variation and chromosomal rearrangements facilitate local adaptation in a marine fish

Abstract

Population genetic theory states that adaptation most frequently occurs from standing genetic variation, which results from the interplay between different evolutionary processes including mutation, chromosomal rearrangements, drift, gene flow and selection. To date, empirical work focusing on the contribution of standing genetic variation to local adaptation in the presence of high gene flow has been limited to a restricted number of study systems. Marine organisms are excellent biological models to address this issue since many species have to cope with variable environmental conditions acting as selective agents despite high dispersal abilities. In this study, we examined how, demographic history, standing genetic variation linked to chromosomal rearrangements and shared polymorphism among glacial lineages contribute to local adaptation to environmental conditions in the marine fish, the capelin (Mallotus villosus). We used a comprehensive dataset of genome-wide single nucleotide polymorphisms (25,904 filtered SNPs) genotyped in 1,359 individuals collected from 31 spawning sites in the northwest Atlantic (North America and Greenland waters). First, we reconstructed the history of divergence among three glacial lineages and showed that they diverged from 3.8 to 1.8 MyA. Depending on the pair of lineages considered, historical demographic modelling provided evidence for divergence with gene flow and secondary contacts, shaped by barriers to gene flow and linked selection. We next identified candidate loci associated with reproductive isolation of these lineages. Given the absence of physical or geographic barriers, we thus propose that these lineages may represent three cryptic species of capelin. Within each of these, our analyses provided evidence for large ܰ and high gene flow at both historical and contemporary time scales among spawning sites.Furthermore, we detected a polymorphic chromosomal rearrangement leading to the coexistence of three haplogroups within the Northwest Atlantic lineage, but absent in the other two clades.Genotype-environment associations revealed molecular signatures of local adaptation to environmental conditions prevailing at spawning sites. Altogether, our study shows that standing genetic variation associated with both chromosomal rearrangements and ancestral polymorphism contribute to local adaptation in the presence of high gene flow.

Thermal adaptation rather than demographic history drives genetic structure inferred by copy number variants in a marine fish

“…Barcodes were removed using cutadapt (Martin 2011) and trimmed to 80 bp, allowing for an error rate of 0.2. They were then demultiplexed using the 'process_radtags' module of Stacks v1.48 (Catchen et al 2013) and aligned to the capelin draft genome (Cayuela et al 2019) assembly using bwa-mem (Li 2013) with default parameters, as detailed below. Next, aligned reads were processed with Stacks v.1.48 for SNP calling and genotyping.…”

“…The goal of this study was to investigate how fitness, local thermal conditions and demographic history are associated with CNVs genotyped in multiple populations, and subsequently how copy number variation drives population genetic structure in a marine fish, the capelin (Mallotus villosus), an excellent biological model to address this issue. First, capelin has a complex demographic history and in the north Atlantic it comprises three glacial lineages (NWA, ARC, and GRE) that diverged in allopatry from 1.8 to 3.5 MyA (Cayuela et al 2019). Very low migration rates and the absence of admixture between lineages despite no obvious physical barriers suggest the existence of strong reproductive barriers and an ongoing speciation process (Cayuela et al 2019), allowing the consideration of copy-number variation at two taxonomic scales.…”

“…First, capelin has a complex demographic history and in the north Atlantic it comprises three glacial lineages (NWA, ARC, and GRE) that diverged in allopatry from 1.8 to 3.5 MyA (Cayuela et al 2019). Very low migration rates and the absence of admixture between lineages despite no obvious physical barriers suggest the existence of strong reproductive barriers and an ongoing speciation process (Cayuela et al 2019), allowing the consideration of copy-number variation at two taxonomic scales. Second, within-lineage populations may reproduce in either demersal or beach-spawning sites (Christiansen et al 2008).…”

“…In the latter case, populations span large environmental gradients in which temperature seems to be an important selective driver affecting fitness components (i.e., survival and growth rate) at early stages (i.e., embryo and larvae ;Frank & Leggett 1981, Leggett et al 1984 and probably later in life (Colbeck et al 2011, Kenchington et al 2015. In the NWA lineage, genotypetemperature associations based on SNPs suggest that beach-spawning individuals are locally adapted to thermal conditions prevailing in the intertidal zone (Cayuela et al 2019).…”

“…Fourth, we investigated the potential role of CNVs on the ongoing speciation process among glacial lineages by quantifying how the normalized read depth differs for each pair of lineages. We expected that variation in copy number of protein-coding genes and the rapid accumulation of class I (i.e., retrotransposons) and class II (i.e., DNA transposons) TEs could be involved in the reproductive isolation responsible for the absence of admixture between lineages (Cayuela et al 2019). Fifth, we examined how variation in copy number associated with thermal conditions and demographic history drive genetic structure in the study area.…”