Adaptation to Low Salinity Promotes Genomic Divergence in Atlantic Cod ( Gadus morhua L.)

Abstract

How genomic selection enables species to adapt to divergent environments is a fundamental question in ecology and evolution. We investigated the genomic signatures of local adaptation in Atlantic cod (Gadus morhua L.) along a natural salinity gradient, ranging from 35‰ in the North Sea to 7‰ within the Baltic Sea. By utilizing a 12 K SNPchip, we simultaneously assessed neutral and adaptive genetic divergence across the Atlantic cod genome. Combining outlier analyses with a landscape genomic approach, we identified a set of directionally selected loci that are strongly correlated with habitat differences in salinity, oxygen, and temperature. Our results show that discrete regions within the Atlantic cod genome are subject to directional selection and associated with adaptation to the local environmental conditions in the Baltic- and the North Sea, indicating divergence hitchhiking and the presence of genomic islands of divergence. We report a suite of outlier single nucleotide polymorphisms within or closely located to genes associated with osmoregulation, as well as genes known to play important roles in the hydration and development of oocytes. These genes are likely to have key functions within a general osmoregulatory framework and are important for the survival of eggs and larvae, contributing to the buildup of reproductive isolation between the low-salinity adapted Baltic cod and the adjacent cod populations. Hence, our data suggest that adaptive responses to the environmental conditions in the Baltic Sea may contribute to a strong and effective reproductive barrier, and that Baltic cod can be viewed as an example of ongoing speciation.

Immigrant reproductive dysfunction facilitates ecological speciation

“…For example, selection on both osmoregulation and reproductive ability has been invoked to explain the divergence of Baltic Sea populations from Atlantic populations of Atlantic cod (Gadus morhua) (Berg et al 2015), and European flounder (Platichthys flesus) (Momigliano et al 2017), and this may also be true for other species that have diverged between the two environments (Serrao et al 1999;Johannesson and André 2006;Hemmer-Hansen et al 2007;Larmuseau et al 2009a;Johannesson et al, 2011;Limborg et al, 2012). For example, selection on both osmoregulation and reproductive ability has been invoked to explain the divergence of Baltic Sea populations from Atlantic populations of Atlantic cod (Gadus morhua) (Berg et al 2015), and European flounder (Platichthys flesus) (Momigliano et al 2017), and this may also be true for other species that have diverged between the two environments (Serrao et al 1999;Johannesson and André 2006;Hemmer-Hansen et al 2007;Larmuseau et al 2009a;Johannesson et al, 2011;Limborg et al, 2012).…”

“…A heterogeneous environment can restrict gene flow and increase the opportunity for local adaptation (Kawecki and Ebert 2004;Larmuseau et al 2009a;Hohenlohe et al 2010;Poulsen et al 2011;Hice et al 2012;Limborg et al 2012;Berg et al 2015). When immigrants to a population perform more poorly compared to locally adapted residents, natural selection will form a barrier against gene flow that can promote further reproductive isolation.…”

Adaptive genomic divergence under high gene flow between freshwater and brackish‐water ecotypes of prickly sculpin (Cottus asper) revealed by Pool‐Seq

“…; Berg et al . ), the presence of many small divergent regions scattered throughout the genome (e.g. threespine stickleback, Rösti et al .…”

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

“…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).…”