Two adjacent inversions maintain genomic differentiation between migratory and stationary ecotypes of Atlantic cod

Abstract

Atlantic cod is composed of multiple migratory and stationary populations widely distributed in the North Atlantic Ocean. The Northeast Arctic cod (NEAC) population in the Barents Sea undertakes annual spawning migrations to the northern Norwegian coast. Although spawning occurs sympatrically with the stationary Norwegian coastal cod (NCC), phenotypic and genetic differences between NEAC and NCC are maintained. In this study, we resolve the enigma by revealing the mechanisms underlying these differences. Extended linkage disequilibrium (LD) and population divergence were demonstrated in a 17.4-Mb region on linkage group 1 (LG1) based on genotypes of 494 SNPs from 192 parents of farmed families of NEAC, NCC or NEACxNCC crosses. Linkage analyses revealed two adjacent inversions within this region that repress meiotic recombination in NEACxNCC crosses. We identified a NEAC-specific haplotype consisting of 186 SNPs that was fixed in NEAC sampled from the Barents Sea, but segregating under Hardy-Weinberg equilibrium in eight NCC stocks. Comparative genomic analyses determine the NEAC configuration of the inversions to be the derived state and date it to ~1.6-2.0 Mya. The haplotype block harbours 763 genes, including candidates regulating swim bladder pressure, haem synthesis and skeletal muscle organization conferring adaptation to long-distance migrations and vertical movements down to large depths. Our results suggest that the migratory ecotype experiences strong directional selection for the two adjacent inversions on LG1. Despite interbreeding between NEAC and NCC, the inversions are maintaining genetic differentiation, and we hypothesize the co-occurrence of multiple adaptive alleles forming a 'supergene' in the NEAC population.

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

“…Although speculative due to the currently small samples sizes from Orkney (n = 5) and Haithabu (n = 5), our results suggest that the divergent frequency distributions of these inversions indeed have remained stable in their respective populations. Given the low overall genomic differentiation outside of these inversions in modern populations (31)(32)(33), it appears that this divergence is sustained despite ongoing gene flow, which further supports a hypothesis that these alleles are maintained as a balanced polymorphism (65).…”

“…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.…”

“…In cod, these regions contribute to elevated genomic diversification between modern populations and ecotypes-despite low overall levels of divergence (25,(31)(32)(33)(34)64)-and they have been suspected to be under selection (22,28,29). The high genomic divergence of these alleles, in combination with their wide geographic distribution, suggests that these have been maintained as a polymorphism for hundreds of thousands, if not millions of years (32,33). Here, we directly observe the millennium-long maintenance of such inversions, which provides an opportunity to investigate their temporal stability.…”

“…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).…”

Atlantic cod (Gadus morhua) feeding over deep water in the high Arctic

“…The success of this highly exploited fish seems related to different life-history strategies of the multiple migratory and stationary populations (Kirubakaran et al 2016). As a result of careful management in combination with favorable climate conditions, the Barents Sea cod stock (also known as Northeast Arctic or Arcto-Norwegian cod: Ottersen et al 2014) is currently at its largest (Kjesbu et al 2014).…”