The Arctic cod (Boreogadus saida) is an abundant marine fish that plays a vital role in the marine food web. To better understand the population genetic structure and the role of natural selection acting on the maternally-inherited mitochondrial genome (mitogenome), a molecule often associated with adaptations to temperature, we analyzed genetic data collected from 11 biparentally-inherited nuclear microsatellite DNA loci and nucleotide sequence data from from the mitochondrial DNA (mtDNA) cytochrome b (cytb) gene and, for a subset of individuals, the entire mitogenome. In addition, due to potential of species misidentification with morphologically similar Polar cod (Arctogadus glacialis), we used ddRAD-Seq data to determine the level of divergence between species and identify species-specific markers.
Based on the findings presented here, Arctic cod across the Pacific Arctic (Bering, Chukchi, and Beaufort Seas) comprise a single panmictic population with high genetic diversity compared to other gadids. High genetic diversity was indicated across all 13 protein-coding genes in the mitogenome. In addition, we found moderate levels of genetic diversity in the nuclear microsatellite loci, with highest diversity found in the Chukchi Sea. Our analyses of markers from both marker classes (nuclear microsatellite fragment data and mtDNA cytb sequence data) failed to uncover a signal of microgeographic genetic structure within Arctic cod across the three regions, within the Alaskan Beaufort Sea, or between near-shore or offshore habitats. Further, data from a subset of mitogenomes revealed no genetic differentiation between Bering, Chukchi, and Beaufort seas populations for Arctic cod, Saffron cod (Eleginus gracilis), or Walleye pollock (Gadus chalcogrammus). However, we uncovered significant differences in the distribution of microsatellite alleles between the southern Chukchi and central and eastern Beaufort Sea samples of Arctic cod. Finally, using ddRAD-Seq data, we identified species-specific markers and in conjunction with mitogenome data, identified an Arctic cod x Polar cod hybrid in western Canadian Beaufort Sea.
Overall, the lack of genetic structure among Arctic cod within the Bering, Chukchi and Beaufort seas of Alaska is concordant with the absence of geographic barriers to dispersal and typical among marine fishes. Arctic cod may exhibit a genetic pattern of isolation-by-distance, whereby populations in closer geographic proximity are more genetically similar than more distant populations. As this signal is only found between our two fartherest localities, data from populations elsewhere in the species’ global range are needed to determine if this is a general characteristic. Further, tests for selection suggested a limited role for natural selection acting on the mitochondrial genome of Arctic cod, but do not exclude the possibility of selection on genes involved in nuclear-mitogenome interactions. Unlike previous genetic assessment of Arctic cod sampled from the Chukchi Sea, the high levels of genetic diversity found in Arctic cod assayed in this study, across regions, suggests that the species in the Beaufort and Chukchi seas does not suffer from low levels of genetic variation, at least at neutral genetic markers. The large census size of Arctic cod may allow this species to retain high levels of genetic diversity. In addition, we discovered the presence of hybridization between Arctic and Polar cod (although low in frequency). Hybridization is expected to occur when environmental changes modify species distributions that result in contact between species that were previously separated. In such cases, hybridization may be an evolutionary mechanism that promotes an increase in genetic diversity that may provide species occupying changing environments with locally-adapted genotypes and, therefore, phenotypes. Natural selection can only act on the standing genetic variation present within a population. Therefore, given its higher levels of genetic diversity in combination with a large population size, Arctic cod may be resilient to current and future environmental change, as high genetic diversity is expected to increase opportunities for positive selection to act on genetic variants beneficial in different environments, regardless of the source of that genetic variation.