A migration-associated supergene reveals loss of biocomplexity in Atlantic cod

Abstract

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.

Range‐wide genomic data synthesis reveals transatlantic vicariance and secondary contact in Atlantic cod

“…Interestingly, despite using a North American SNP panel, we are less able to reproduce migration associated divergence in North America than in Europe (e.g., Barney et al, ; Sinclair‐Waters et al, ). In some cases, such as the northern cod, this may reflect the finding that population structure at inversion sites seems to operate at the individual level (i.e., populations homozygous for one of the other form of an inversion appear to exist in sympatry (Kess et al, ). Other patterns observed in our data, for example, in Baltic Sea and north Sea divergence, may reflect contemporary local adaptation to a salinity and temperature gradient (Berg et al, ), and we found that removing putatively adaptive (outlier) loci from our analysis resulted in the North Sea and Baltic Sea clustering together.…”

Consequences of Single-Locus and Tightly Linked Genomic Architectures for Evolutionary Responses to Environmental Change

“…Fish populations that migrate between freshwater and saltwater for reproduction and feeding require different temperature and salinity adaptations compared to resident populations that do not migrate. Consequently, linked architectures in marine and freshwater fishes are associated with coexisting migratory ecotypes experiencing different environments ( Table 1 ; Pearse et al 2014 ; Berg et al 2016 ; Kirubakaran et al 2016 ; Arostegui et al 2019 ; Kess et al 2019 ; Pearse et al 2019 ). For example, a double inversion in steelhead/rainbow trout ( Oncorhynchus mykiss ) varies in frequency between anadromous (maturing at sea) and resident populations, as well as between fluvial (maturing in rivers) and adfluvial (maturing in lakes) populations, and exhibits latitudinal- and temperature-associated frequency clines ( Pearse et al 2014 ; Arostegui et al 2019 ; Pearse et al 2019 ).…”

Linking scales of life-history variation with population structure in Atlantic cod

“…As with recent studies, large FST differences were related to genomic regions under selection (Berg et al 2016Barth et al, 2017), suggesting adaptive genomic divergence while FST values based on the unlinked neutral SNPs were largely insignificant (data not shown) so truly biological distinct populations were not demonstrated. Studies of adaptive genomic divergence (Barth et al, 2019;Kess et al, 2019) and movements in other Atlantic cod stocks (Robichaud & Rose, 2004;Neuenfeld et al, 2011) suggest two general population types; small coastal resident populations exhibiting year round fidelity and larger populations of seasonal migrants. The temporal persistence of genetic differences within the present study area, coupled to tag based evidence on adult and juvenile movements (Wright et al, 2006 a,b;Neat et al, 2014;Wright et al, 2018), appear to at least partially conform to this pattern.…”

“…However, these genomic regions of adaptive divergence appear very relevant for advising on the appropriate scale for stock management as they appear to reflect reproductive barriers linked to local environmental adaptation and migratory phenotypes (Bradbury et al 2013;Barth et al, 2017;Kess et al, 2019). Variations in reproductive traits at scales less than the fished stock have been widely reported in this species (Marteinsdottir & Begg, 2002;Yoneda & Wright, 2004), although only in Norwegian coastal cod has this variability been related to genetic differences (Olsen et al, 2009).…”