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.

Keywords: Atlantic cod; Baltic Sea; SNPs; ecological divergence; genomic adaptation; population genomics; speciation.

Fig. 1.—

Sampling locations of Atlantic cod specimens. Samples were obtained between 2002 and 2008 using trawl. Only mature specimens were selected for genetic analysis. See table 1 for a detailed description of the samples. Average surface salinity is denoted in ‰.

Fig. 2.—

Pairwise F_st values between Atlantic cod populations using 8,809 SNPs in 23 LGs. SNPs are ordered according to LG and position within LGs based on the results of a preliminary SNP linkage map (Lien S, unpublished data). LG nomenclature follows that of Hubert et al. (2010). Median F_st estimates between the population pairs are denoted in parentheses.

Fig. 3.—

Global outlier pattern and LD in Atlantic cod. The extent of pairwise LD among loci within 23 LGs, measured as r2, is estimated using all individuals and populations. A color bar on the right hand side denotes the strength of the r2 values. A global outlier pattern (underneath each LD plot) based on the same SNP data is visualized using a moving average of the median log10(BF), calculated using the global BAYESCAN outlier analyses (see text for details). The SNPs are plotted according to LG and their respective position within the LGs, based on the results of a preliminary SNP linkage map (Lien S, unpublished data). LG nomenclature follows Hubert et al. (2010).

Fig. 4.—

Global and pairwise outlier patterns in Atlantic cod. Manhattan plots of global and pairwise outlier analyses based on median log10(BF) from ten replicate runs of BAYESCAN. The SNPs are plotted according to LG and their respective position within the LGs along the X axis based on the results of a preliminary SNP linkage map (Lien S, unpublished data). LG nomenclature follows Hubert et al. (2010). The dotted line at log10(BF) = 1 indicates “strong association” and the solid line at 2 indicates “decisive association” according to Jeffreys (1961).

Fig. 5.—

SNPs associated with environmental variables in Atlantic cod. Manhattan plots of SNP association with salinity, temperature, and oxygen level (all at surface and at spawning depth, see table 1) based on median log10(BF) from 32 independent runs of BAYENV. The SNPs are plotted according to LG and their respective position within the LGs along the X axis, based on the results of a preliminary SNP linkage map (Lien S, unpublished data). LG nomenclature follows Hubert et al. (2010). The dotted line at log10(BF) = 1 indicates strong association and the solid line at 2 indicates decisive association according to Jeffreys (1961).