Abstract
Chromosomal rearrangements such as inversions can play a crucial role in maintaining polymorphism underlying complex traits and contribute to the process of speciation. In Atlantic cod (Gadus morhua), inversions of several megabases have been identified that dominate genomic differentiation between migratory and nonmigratory ecotypes in the Northeast Atlantic. Here, we show that the same genomic regions display elevated divergence and contribute to ecotype divergence in the Northwest Atlantic as well. The occurrence of these inversions on both sides of the Atlantic Ocean reveals a common evolutionary origin, predating the >100 000-year-old trans-Atlantic separation of Atlantic cod. The long-term persistence of these inversions indicates that they are maintained by selection, possibly facilitated by coevolution of genes underlying complex traits. Our data suggest that migratory behaviour is derived from more stationary, ancestral ecotypes. Overall, we identify several large genomic regions—each containing hundreds of genes—likely involved in the maintenance of genomic divergence in Atlantic cod on both sides of the Atlantic Ocean.
Highlights
Genomic islands of divergence (Wu, 2001; Nosil et al, 2009) are known to emerge through divergence hitchhiking (Via, 2012) but can evolve through other processes that reduce recombination in genomic regions, such as inversions (Kirkpatrick and Barton, 2006)
We investigated a total of 8165 single-nucleotide polymorphisms (SNPs), distributed throughout 23 linkage group (LG) with an average distance of 94 000 bp between SNPs, based on a genome size of 830 Mb (Star et al, 2011), in 316 individuals of cod from both sides of the Atlantic Ocean (Figure 1 and Table 1)
Elevated FST values predominantly occurred within distinct regions in LGs 2, 7 and 12 in the Northwest Atlantic populations, primarily in LGs 1, 2 and 7 in the Northeast Atlantic populations, and in a distinct region in LG23 and in a few SNPs in LG11 between the two continents (Supplementary Figure S1)
Summary
Genomic islands of divergence (Wu, 2001; Nosil et al, 2009) are known to emerge through divergence hitchhiking (Via, 2012) but can evolve through other processes that reduce recombination in genomic regions, such as inversions (Kirkpatrick and Barton, 2006). Inversions that differentiate migratory from nonmigratory ecotypes (Berg et al, 2016; Kirubakaran et al, 2016) have been documented for cod in the Northeast Atlantic, either in only a small fraction of the genome (Kirubakaran et al, 2016) or a few distinct populations (Berg et al, 2016; Sodeland et al, 2016). Existence of these inversions in the Northwest Atlantic or around Iceland has not yet been investigated, genomic islands of divergence have previously been documented for several populations (Bradbury et al, 2010, 2013; HemmerHansen et al, 2013; Berg et al, 2015, 2016). A subset of the single-nucleotide polymorphisms (SNPs) investigated by Bradbury et al (2010) has been associated with temperature in several other studies (Nielsen et al, 2009; Hemmer-Hansen et al, 2013; Therkildsen et al, 2013)
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