Microgeographical population structure and adaptation in Atlantic cod Gadus morhua: spatio-temporal insights from gene-associated DNA markers

Recent technical advances have stimulated studies on spatial scales of adaptive genetic variation in marine fishes. However, very few studies have combined spatial and temporal sampling to investigate adaptive genetic structuring at local and microgeographical scales, i.e. scales at which neutral genetic markers have typically revealed very limited levels of population structure. In the present study we analyzed 92 gene-associated single-nucleotide polymorphism (SNP) markers in Atlantic cod Gadus morhua from several sampling sites within the North Sea and adjacent areas. To test for temporal stability, we included long-and short-term (i.e. from 24 to 38 and from 8 to 11 yr, respectively) temporally replicated samples from a subset of populations. As expected, we found very low levels of neutral genetic population structure (F-ST = 0.003). Three specific loci, however, showed highly elevated levels of genetic differentiation. Interestingly, these loci were identical to loci previously found to display signals of adaptive evolution on larger spatial scales. Analysis of historical samples revealed long-term temporally stable patterns of both neutral and adaptive divergence between some populations, indicating long-term temporal adaptive stability driven by strong local selection. In an environmentally dynamic area, on the other hand, patterns of genetic structuring were more variable. Overall, our results not only suggest separation of populations under both evolutionary and ecological paradigms, but also illustrate the usefulness of the spatio-temporal approach for making inferences about the dynamics and geographical distribution of adaptive genetic variation in natural populations.