Shared ancestral polymorphisms and chromosomal rearrangements as potential drivers of local adaptation in a marine fish

Abstract

Gene flow has tremendous importance for local adaptation, by influencing the fate of de novo mutations, maintaining standing genetic variation and driving adaptive introgression. Furthermore, structural variation as chromosomal rearrangements may facilitate adaptation despite high gene flow. However, our understanding of the evolutionary mechanisms impending or favouring local adaptation in the presence of gene flow is still limited to a restricted number of study systems. In this study, we examined how demographic history, shared ancestral polymorphism, and gene flow among glacial lineages contribute to local adaptation to sea conditions in a marine fish, the capelin (Mallotus villosus). We first assembled a 490‐Mbp draft genome of M. villosus to map our RAD sequence reads. Then, we used a large data set of genome‐wide single nucleotide polymorphisms (25,904 filtered SNPs) genotyped in 1,310 individuals collected from 31 spawning sites in the northwest Atlantic. We reconstructed the history of divergence among three glacial lineages and showed that they probably diverged from 3.8 to 1.8 million years ago and experienced secondary contacts. Within each lineage, our analyses provided evidence for large Ne and high gene flow among spawning sites. Within the Northwest Atlantic lineage, we detected a polymorphic chromosomal rearrangement leading to the occurrence of three haplogroups. Genotype–environment associations revealed molecular signatures of local adaptation to environmental conditions prevailing at spawning sites. Our study also suggests that both shared polymorphisms among lineages, resulting from standing genetic variation or introgression, and chromosomal rearrangements may contribute to local adaptation in the presence of high gene flow.

Copy number variants outperform SNPs to reveal genotype–temperature association in a marine species

“…This difference in structure is consistent with previous studies in humans showing that CNVs contribute to higher genetic divergence than SNPs (Levy et al., 2007; Pang et al., 2010; Sudmant et al., 2015). Furthermore, recent studies in marine fishes also showed that genomic regions including structural variants account for higher genetic divergence than SNPs that are distributed across the whole genome (Barth et al., 2019; Berg et al., 2016; Cayuela et al., 2020; Kess et al, 2020). Several hypotheses may explain this pattern.…”

“…They can have functional consequences, notably impacting the regulation of gene expression (Gamazon & Stranger, 2015) and recombination rate by diminishing the frequency of meiotic crossing‐over, which can preserve the integrity of an adaptive haplotype (Rowan et al., 2019). SVs are increasingly recognized for their important role in a wide spectrum of evolutionary processes such as in environmental adaptation (Van’t Hof et al., 2016; Wellenreuther, Rosenquist, Jakson, & Larson, 2017), reproductive isolation (Berdan, Blanckaert, Butlin, & Bank, 2019; Laporte et al., 2019), life cycles and development (Mérot et al, 2018; Cayuela et al., 2020) and speciation (Rieseberg, 2001; Serrato‐Capuchina & Matute, 2018).…”

Global drivers of recent diversification in a marine species complex

“…For example, Pleistocene glaciations shaped contemporary genetic structure of the abalone Haliotis asinina in the Indo‐Pacific (Benardine Jeffrey et al, 2007), the American lobster, Homarus americanus , along the northeastern coast of North America (Kenchington et al, 2009), and the octopod Pareledone turqueti in the Southern Ocean (Strugnell et al, 2012). Pleistocene glaciations were also responsible for the divergence of species complexes, such as the Damselfishes Pomacentrus coelestis (Sorenson et al, 2014) and the capelin Mallotus villosus (Cayuela et al, 2020; Dodson et al, 2007). Sequential glacial and interglacial periods have then further shaped the divergence history of species as a result of periods of isolation intercalated by gene flow (Weigelt et al, 2016).…”

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 version 1.48 (Catchen et al, 2013) and aligned to the capelin draft genome (Cayuela et al, 2020) assembly using bwa-mem (Li, 2013) with default parameters. Next, aligned reads were processed with stacks version 1.48 for SNP calling and genotyping.…”

“…Using the capelin reference genome (Cayuela et al, 2020), we examined if the putative CNVs discovered were located within sequences of protein genes or within intergenic regions. Note that the genome is assembled at the scaffold level; nevertheless, contig order F I G U R E 1 Map of the study area showing the sites sampled in the three capelin lineages.…”