Genomic stability through time despite decades of exploitation in cod on both sides of the Atlantic

Abstract

The mode and extent of rapid evolution and genomic change in response to human harvesting are key conservation issues. Although experiments and models have shown a high potential for both genetic and phenotypic change in response to fishing, empirical examples of genetic responses in wild populations are rare. Here, we compare whole-genome sequence data of Atlantic cod (Gadus morhua) that were collected before (early 20th century) and after (early 21st century) periods of intensive exploitation and rapid decline in the age of maturation from two geographically distinct populations in Newfoundland, Canada, and the northeast Arctic, Norway. Our temporal, genome-wide analyses of 346,290 loci show no substantial loss of genetic diversity and high effective population sizes. Moreover, we do not find distinct signals of strong selective sweeps anywhere in the genome, although we cannot rule out the possibility of highly polygenic evolution. Our observations suggest that phenotypic change in these populations is not constrained by irreversible loss of genomic variation and thus imply that former traits could be reestablished with demographic recovery.

Keywords: fisheries-induced evolution; genetic diversity; historical DNA; population genomics; selective sweeps.

Fig. 1.

Spatiotemporal population structure based on genome-wide data in Atlantic cod. (A) In total, 113 modern and historical specimens were analyzed from northern cod collected in Newfoundland, Canada (1940, yellow; 2013, dark yellow) and from northeast Arctic cod collected in the Lofoten archipelago, Norway (1907, orange; modern: 2011, red; 2014, dark red). (B) Age at 50% maturity over time in each population. (C) PCA as implemented in PCAngsd. Velicier’s minimum average partial (MAP) test identified a single significant PC and only one PC is shown. Individuals are colored according to A. (D) Model-based ADMIXTURE ancestry components for historical (1907, 1940) and modern (2013, 2014) populations (k = 2; NGSadmix). Each individual is represented by a column colored to show the proportion of each ancestry component for Canada (dark yellow) and Norway (orange). Population differentiation based on pairwise weighted F_ST is also shown. (E) The correlation between the allele frequencies in historical and modern populations. Colors reflect the relative density of points, from darker (more density) to lighter (less density). R², coefficient of correlation.

Fig. 2.

F_ST between temporal samples across the genome for (A) Canadian northern cod 1940 to 2013, and (B) northeast Arctic cod 1907 to 2014. F_ST was calculated in nonoverlapping 50-kb windows. The linkage group is labeled on the x axis. Point size indicates the number of SNPs in each window, and color indicates the linkage group. Four regions that are in the highest 99th percentile in the Canadian northern cod and all historical with contemporary northeast Arctic cod comparisons are marked in red. See SI Appendix, Fig. S7 for the comparisons involving the northeast Arctic cod 2011 sample.