“Islands of Divergence” in the Atlantic Cod Genome Represent Polymorphic Chromosomal Rearrangements

Abstract

In several species genetic differentiation across environmental gradients or between geographically separate populations has been reported to center at “genomic islands of divergence,” resulting in heterogeneous differentiation patterns across genomes. Here, genomic regions of elevated divergence were observed on three chromosomes of the highly mobile fish Atlantic cod (Gadus morhua) within geographically fine-scaled coastal areas. The “genomic islands” extended at least 5, 9.5, and 13 megabases on linkage groups 2, 7, and 12, respectively, and coincided with large blocks of linkage disequilibrium. For each of these three chromosomes, pairs of segregating, highly divergent alleles were identified, with little or no gene exchange between them. These patterns of recombination and divergence mirror genomic signatures previously described for large polymorphic inversions, which have been shown to repress recombination across extensive chromosomal segments. The lack of genetic exchange permits divergence between noninverted and inverted chromosomes in spite of gene flow. For the rearrangements on linkage groups 2 and 12, allelic frequency shifts between coastal and oceanic environments suggest a role in ecological adaptation, in agreement with recently reported associations between molecular variation within these genomic regions and temperature, oxygen, and salinity levels. Elevated genetic differentiation in these genomic regions has previously been described on both sides of the Atlantic Ocean, and we therefore suggest that these polymorphisms are involved in adaptive divergence across the species distributional range.

Ancient DNA reveals the Arctic origin of Viking Age cod from Haithabu, Germany

“…We excluded the four chromosomes [linkage group (LG)01, 02, 07, and 12] that contain the large inversions (31)(32)(33), as these distort genetic analyses that assume linkage equilibrium. The PCA shows that three modern populations-North East Arctic (NEA), Lofoten and North Seaform a large, overlapping group, with Iceland clustering near the NEA (Fig.…”

“…Distinct genomic regions with elevated population differentiation have been identified for this species (22,(28)(29)(30). Several of these regions are colocalized into four Mbp-scale, polymorphic inversions with high linkage disequilibrium (31)(32)(33)(34). These polymorphisms segregate with a distinct geographical distribution and have been associated with temperature clines and ecotype-specific migratory behavior (31,32,34).…”

“…Several of these regions are colocalized into four Mbp-scale, polymorphic inversions with high linkage disequilibrium (31)(32)(33)(34). These polymorphisms segregate with a distinct geographical distribution and have been associated with temperature clines and ecotype-specific migratory behavior (31,32,34). Their divergence can be used to improve the traceability of individuals (22) and, given their large size (between ∼5 and ∼17 Mbp), the inversion state of ancient samples can be easily determined from low coverage sequencing data.…”

Population assignment and local adaptation along an isolation‐by‐distance gradient in Pacific cod (Gadus macrocephalus)

“…It therefore seems possible, that in addition to such extrinsic mechanisms maintaining isolation, intrinsic genomic mechanisms may be at play. Indeed, chromosome inversions in Atlantic cod in Scandinavia seem to enhance adaptive differentiation between populations (Barth et al., 2017), including stationary and migratory ecotypes (Berg et al., 2016), and populations inhabiting fjords and outer coasts (Sodeland et al., 2016). Such inversions are likely to cause genome regions of high differentiation among populations (“islands of divergence,” Sodeland et al., 2016).…”

“…Indeed, chromosome inversions in Atlantic cod in Scandinavia seem to enhance adaptive differentiation between populations (Barth et al., 2017), including stationary and migratory ecotypes (Berg et al., 2016), and populations inhabiting fjords and outer coasts (Sodeland et al., 2016). Such inversions are likely to cause genome regions of high differentiation among populations (“islands of divergence,” Sodeland et al., 2016). Given the weak evidence for adaptive divergence in Salish Sea cod found in our study, there is, however, currently no evidence for such inversions in Pacific cod.…”