Adaptive genetic variation underlies biocomplexity of Atlantic Cod in the Gulf of Maine and on Georges Bank

Abstract

Atlantic cod (Gadus morhua) populations in the Gulf of Maine (GoM) are at a fraction of their historical abundance, creating economic hardships for fishermen and putting at risk the genetic diversity of the remaining populations. An understanding of the biocomplexity among GoM populations will allow for adaptive genetic diversity to be conserved to maximize the evolutionary potential and resilience of the fishery in a rapidly changing environment. We used restriction-site-associated DNA sequencing (RADseq) to characterize the population structure and adaptive genetic diversity of five spawning aggregations from the western GoM and Georges Bank. We also analyzed cod caught in the eastern GoM, an under-sampled area where spawning aggregations have been extirpated. Using 3,128 single nucleotide polymorphisms (SNPs), we confirmed the existence of three genetically separable spawning groups: (1) winter spawning cod from the western GoM, (2) spring spawning cod, also from the western GoM, and (3) Georges Bank cod. Non-spawning cod from the eastern GoM could not be decisively linked to either of the three spawning groups and may represent a unique component of the resource, a mixed sample, or cod from other unsampled source populations. The genetic differentiation among the three major spawning groups was primarily driven by loci putatively under selection, particularly loci in regions known to contain genomic inversions on linkage groups (LG) 7 and 12. These LGs have been found to be linked to thermal regime in cod across the Atlantic, and so it is possible that variation in timing of spawning in western GoM cod has resulted in temperature-driven adaptive divergence. This complex population structure and adaptive genetic differentiation could be crucial to ensuring the long-term productivity and resilience of the cod fishery, and so it should be considered in future management plans.

Fig 1. Locations of Atlantic cod groups analyzed in this study.

Samples from Ipswich and Massachusetts Bays and Georges Bank were from known spawning grounds (dark gray circles), whereas the sentinel fishery targeted non-spawning cod in the eastern GoM (circled region). We do not have exact catch locations for all of the eastern GoM samples, as fishermen were not required to declare them, and so we show the overall area in which they were caught. The management unit boundaries of the GoM, Georges Bank, and Scotian Shelf are indicated by the thin black lines.

Fig 2. Population differentiation using the full SNP dataset that includes both neutral and outlier SNPs.

a) PCA including all individuals, b) DAPC including all individuals, c) PCA after the Massachusetts Bay outlier individuals were removed, d) DAPC after the same Massachusetts Bay outlier individuals were removed. The percentage of the variation explained by each principle component is shown on the axis labels for the PCAs, and the cumulative percentage of variation explained by the discriminant functions is shown on the inset graphs for the DAPCs. The number of principle components retained in b) was 20 and in d) was 26, as assessed using cross-validation.

Fig 3. Individual assignment probabilities of sampled Atlantic cod to genetic clusters identified by Structure analysis.

Bar plots show aggregated results for K = 2–4 from ten replicate runs using the full SNP dataset, which includes both neutral and outlier SNPs, with location priors. Geographic sampling locations are indicated below.

Fig 4. Population differentiation using the neutral dataset.

a) PCA with all individuals; b) DAPC with all individuals. Removal of two outlying individuals from Massachusetts Bay winter largely collapses all groups in both c) PCA and d) DAPC. The percentage of the variation explained by each principle component is shown on the axis labels for the PCAs, and the cumulative percentage of variation explained by the discriminant functions is shown on the inset graphs for the DAPCs. The number of principle components retained in b) was 24 and in d) was 13, as assessed using cross-validation.

Fig 5. Manhattan plots showing pairwise, locus-specific F_ST values between groups for the full SNP dataset.

Fig 6

PCAs for each of the LD blocks on a) LG 7, b) LG 12, and c) LG 2. The percentage of the variance explained by each axis is shown on the axes labels.