Highly localized divergence within supergenes in Atlantic cod (Gadus morhua) within the Gulf of Maine

Abstract

Background: Atlantic cod (Gadus morhua), is known to vary genetically across the North Atlantic, Greenland, and Newfoundland. This genetic variation occurs both spatially and temporally through decades of heavy fishing, and is concentrated in three linkage disequilibrium blocks, previously defined by pedigreed linkage mapping analysis. Variation within these genomic regions is correlated with both seawater temperature and behavioral ecotype. The full extent and nature of these linkage groups is important information for interpreting cod genetic structure as a tool for future fisheries management.

Results: We conducted whole genome sequencing for 31 individual cod from three sub-populations in the Gulf of Maine. Across the genome, we found 3,390,654 intermediate to high frequency Single Nucleotide Polymorphisms (SNPs). We show that pairwise linkage analysis among these SNPs is a powerful tool to detect linkage disequilibrium clusters by recovering the three previously detected linkage groups and identifying the 1031 genes contained therein. Across these genes, we found significant population differentiation among spawning groups in the Gulf of Maine and between Georges Bank and Gulf of Maine. Coordinated divergence among these genes and their differentiation at both short and long spatial scales suggests that they are acting as linked supergenes in local adaptation of cod populations.

Conclusions: Differentiation between SNPs in linkage disequilibrium blocks is the major signal of genetic differentiation between all groups tested within the Gulf of Maine. Our data provide a map of genes contained in these blocks, allowing an enhanced search for neutral genetic structure for demographic inference and fisheries modeling. Patterns of selection and the history of populations may be possible to identify in cod using this description of linkage disequilibrium blocks and future data sets to robustly separate neutral and selected genetic markers.

Keywords: Atlantic cod; Gadus morhua; Genomic divergence; Gulf of Maine; Linkage disequilibrium; Linkage map; Supergene.

Fig. 1

Sampling locations used in this study. Twenty one adults in spawning condition were sampled in northwestern Massachusetts Bay within the Gulf of Maine. These were subdivided into 11 spring spawning cod (site S) and 10 winter spawning cod (site W). Ten adults in spawning condition were sampled from Georges Bank (site G). Figure was generated using the marmap package in R

Fig. 2

Linkage and population differentiation for chromosomes 2, 7 and 12 inside and outside linkage blocks. Mean pairwise LD (as r ²) and F_ST are shown on the y-axis for every 250th SNP, with SNP position within its linkage group along the x-axis. The right hand figures show a regression of LD vs F_ST for each SNP

Fig. 3

Distributions of pairwise F_ST within LD blocks between sampled populations. Pairwise F_ST was determined within LD blocks (blue), on the same LG but not in the LD block (red), as well as the remainder of the genome (black) for LD blocks on LG02 (top row) LG07 (middle row), and LG12 (bottom row). Column 1 is the pairwise FST comparison between spring and winter spawners, column 2 is spring vs. Georges Bank, and column 3 is winter vs. Georges Bank

Fig. 4

Principal component analyses. PCA was performed on exonic SNPs from LG02 (top row), LG07 (middle row), and LG12 (bottom row). SNPs within the LD block on that LG are shown on the left, SNPs outside the LD block on the right. In all cases, as expected, SNPs within each LD block separate into three distinct vertical clusters along PC axis 1, indicating the three genotypes that individuals might possess for each LD block. This separation is lost, however, for PCA on SNPs outside the LD block, but in the same linkage group. Note that SNPs outside of the LD block on LG07 (D, above) may signify the presence of another, undiscovered linkage disequilibrium cluster, as the pattern appears diffusely similar to that in C