Modular chromosome rearrangements reveal parallel and nonparallel adaptation in a marine fish

Abstract

Genomic architecture and standing variation can play a key role in ecological adaptation and contribute to the predictability of evolution. In Atlantic cod (Gadus morhua), four large chromosomal rearrangements have been associated with ecological gradients and migratory behavior in regional analyses. However, the degree of parallelism, the extent of independent inheritance, and functional distinctiveness of these rearrangements remain poorly understood. Here, we use a 12K single nucleotide polymorphism (SNP) array to demonstrate extensive individual variation in rearrangement genotype within populations across the species range, suggesting that local adaptation to fine-scale ecological variation is enabled by rearrangements with independent inheritance. Our results demonstrate significant association of rearrangements with migration phenotype and environmental gradients across the species range. Individual rearrangements exhibit functional modularity, but also contain loci showing multiple environmental associations. Clustering in genetic distance trees and reduced differentiation within rearrangements across the species range are consistent with shared variation as a source of contemporary adaptive diversity in Atlantic cod. Conversely, we also find that haplotypes in the LG12 and LG1 rearranged region have diverged across the Atlantic, despite consistent environmental associations. Exchange of these structurally variable genomic regions, as well as local selective pressures, has likely facilitated individual diversity within Atlantic cod stocks. Our results highlight the importance of genomic architecture and standing variation in enabling fine-scale adaptation in marine species.

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

“…This 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 reduced genomic regions involving structural variants account for higher genetic divergence than widely distributed SNPs (Berg et al, 2016;Barth et al 2019;Kess et al, 2020). Several hypotheses may explain this pattern.…”

Footprints of local adaptation span hundreds of linked genes in the Atlantic silverside genome

“…2019; Kess et al. 2020). The genomic breadth and magnitude of allele frequency differentiation (i.e., near fixation of opposite alleles across Mb‐scale regions against an almost complete absence of genome‐wide differentiation, as seen in the southern part of the range) represents, to our knowledge, one of the most extreme examples reported to date of the degree to which differentiation of locally adapted populations can vary across the genome (compare to other notable examples in Table 1).…”

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.…”