Chromosome structural variation may underpin ecologically important intraspecific diversity by reducing recombination within supergenes containing linked, coadapted alleles. Here, we confirm that an ancient chromosomal rearrangement is strongly associated with migratory phenotype and individual genetic structure in Atlantic cod (Gadus morhua) across the Northwest Atlantic. We reconstruct trends in effective population size over the last century and reveal declines in effective population size matching onset of industrialized harvest (after 1950). We find different demographic trajectories between individuals homozygous for the chromosomal rearrangement relative to heterozygous or homozygous individuals for the noninverted haplotype, suggesting different selective histories across the past 150 years. These results illustrate how chromosomal structural diversity can mediate fine-scale genetic, phenotypic, and demographic variation in a highly connected marine species and show how overfishing may have led to loss of biocomplexity within Northern cod stock.

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.

Recent advances in genetic and genomic analysis have greatly improved our understanding of spatial population structure in marine species. However, studies addressing phylogeographic patterns at oceanic spatial scales remain rare. In Atlantic cod (Gadus morhua), existing range‐wide examinations suggest significant transatlantic divergence, although the fine‐scale contemporary distribution of populations and potential for secondary contact are largely unresolved. Here, we explore transatlantic phylogeography in Atlantic cod using a data‐synthesis approach, integrating multiple genome‐wide single‐nucleotide polymorphism (SNP) datasets representative of different regions to create a single range‐wide dataset containing 1,494 individuals from 54 locations and genotyped at 796 common loci. Our analysis highlights significant transatlantic divergence and supports the hypothesis of westward post‐glacial colonization of Greenland from the East Atlantic. Accordingly, our analysis suggests the presence of transatlantic secondary contact off eastern North America and supports existing perspectives on the phylogeographic history of Atlantic cod with an unprecedented combination of genetic and geographic resolution. Moreover, we demonstrate the utility of integrating distinct SNP databases of high comparability.

Intraspecific phenotypic diversity is integral to ecological resilience and the provision of ecosystem services1. Chromosome structural variation may underpin intraspecific diversity and complex phenotypes2 by reducing recombination within supergenes containing linked, co-adapted alleles. Connecting ecologically-relevant phenotypes to genomic variation can enable more precise conservation of exploited marine species by protecting important genetic diversity3,4. Here, using genome-wide association analysis of a 12K single nucleotide polymorphism (SNP) array we confirm that an ancient, derived chromosomal rearrangement consisting of two adjacent inversions is strongly associated with migratory phenotype and individual-level genetic structure in Atlantic cod (Gadus morhua) across the Northwest Atlantic. The presence of all identified migration-associated loci within this rearrangement indicates that pervasive variation in migration phenotype is in part controlled by a recombination-resistant supergene, facilitating fine-scale individual phenotypic variation within Northern cod. Furthermore, we reconstruct trends in effective population size over the last century, and find genomic signatures of population collapse, and different patterns of population expansion and decline among individuals based on supergene alleles. We demonstrate declines in effective population size consistent with the onset of industrialized harvest (post 1950) and substantially reduced effective size of individuals homozygous for the derived chromosomal rearrangement relative to heterozygous individuals or those homozygous for the ancestral version of this chromosomal region. These results illustrate how chromosomal structural diversity can mediate fine-scale genetic and phenotypic variation in a highly connected marine species, and suggest a loss of biocomplexity from a migration-associated supergene within Northern cod by overfishing.