Genetic structure and dispersal in peripheral populations of a marine fish (Pacific cod, Gadus macrocephalus) and their importance for adaptation to climate change.

Small and isolated peripheral populations, which are often remnants of glacial refugia, offer an opportunity to determine the magnitude and direction of fine-scale connectivity in high gene flow marine species. When located at the equatorial edge of a species' range, these populations may also harbor genetic diversity related to survival and reproduction at higher temperatures, a critical resource for marine species facing warming ocean temperatures. Pacific cod (Gadus macrocephalus), a marine fish in the North Pacific, has already experienced major shifts in biomass and distribution linked to climate change. We estimated the magnitude and direction of connectivity between peripheral populations of Pacific cod at the southern edge of the species' range, by conducting restriction site-associated DNA (RAD) sequencing and individual assignment on fish collected around the Korean Peninsula during the spawning season. Three populations on the western, eastern, and southern Korean coasts were highly differentiated (FST  = 0.025-0.042) and relatively small (Ne  = 433-1,777). Ten putative dispersers and estimates of contemporary migration rates revealed asymmetrical, west-to-east movement around the Korean Peninsula, at a higher rate than predicted by indirect estimates of connectivity (FST ). Allele frequencies at 87 RAD loci were decisively correlated with strong marine temperature gradients between the warmer southern coast and the cooler waters of the eastern and western coasts. Despite relatively small sample sizes, our data suggest asymmetrical dispersal and gene flow, potentially involving adaptive alleles, between peripheral populations inhabiting markedly different thermal regimes. Our study emphasizes the conservation value of peripheral populations in high gene flow marine fish species.

Population assignment and local adaptation along an isolation-by-distance gradient in Pacific cod (Gadus macrocephalus).

The discernment of populations as management units is a fundamental prerequisite for sustainable exploitation of species. A lack of clear stock boundaries complicates not only the identification of spatial management units, but also the assessment of mixed fisheries by population assignment and mixed stock analysis. Many marine species, such as Pacific cod, are characterized by isolation by distance, showing significant differentiation but no clear stock boundaries. Here, we used restriction-site-associated DNA (RAD) sequencing to investigate population structure and assess power to genetically assign Pacific cod to putative populations of origin. Samples were collected across the species range in the eastern Pacific Ocean, from the Salish Sea to the Aleutian Islands. A total of 6,425 putative biallelic single nucleotide polymorphisms were identified from 276 individuals. We found a strong isolation-by-distance signal along coastlines that mirrored previous microsatellite results and pronounced genetic differentiation between coastal samples and those from the inland waters of the Salish Sea, with no evidence for hybridization between these two populations. Individual assignment success based on two methods was high overall (≥84%) but decreased from south to north. Assignment to geographic location of origin also was successful, with average distance between capture and assignment location of 220 km. Outlier analyses identified more loci potentially under selection along the coast than between Salish Sea and coastal samples, suggesting more diverse adaptation to latitudinal environmental factors than inshore vs. offshore environments. Our results confirm previous observations of sharp genetic differentiation of the Salish Sea population and isolation by distance along the coast, but also highlight the feasibility of using modern genomic techniques to inform stock boundaries and fisheries management in a low FST marine species.

Role of oceanography in shaping the genetic structure in the North Pacific hake Merluccius productus.

Determining the relative influence of biotic and abiotic factors on genetic connectivity among populations remains a major challenge in evolutionary biology and in the management and conservation of species. North Pacific hake (Merluccius productus) inhabits upwelling regions in the California Current ecosystem from the Gulf of California to the Gulf of Alaska. In this study, we examined mitochondrial DNA (mtDNA) and microsatellite variation to estimate levels of genetic differentiation of M. productus in relation to the role of oceanographic features as potential barriers to gene flow. Samples were obtained from nine sites spanning a large part of the geographic range of the species, from Puget Sound, Washington to Costa Rica. The microsatellite results revealed three genetically discrete populations: one spanning the eastern Pacific coast, and two apparently resident populations circumscribed to the Puget Sound and the northern Gulf of California (FST = 0.032, p = 0.036). Cytochrome b sequence data indicated that isolation between the Puget Sound and northern Gulf of California populations from the coastal Pacific were recent phenomena (18.5 kyr for Puget Sound and 40 kyr for the northern Gulf of California). Oceanographic data obtained from the Gulf of California support the hypothesis that permanent fronts within the region, and strong gradients at the entrance to the Gulf of California act as barriers to gene flow. A seascape genetics approach found significant genetic-environment associations, where the daytime sea surface temperature and chlorophyll concentrations were the best predictive variables for the observed genetic differentiation. Considering the potential causes of genetic isolation among the three populations, e.g. spawning areas in different latitudes associated with upwelling processes, oceanographic barriers, asymmetric migration and specialized diet, oceanographic barriers appear to be a likely mechanism restricting gene flow.

Multiple ice-age refugia in Pacific cod, Gadus macrocephalus.

Pleistocene ice-ages greatly influenced the historical abundances of Pacific cod, Gadus macrocephalus, in the North Pacific and its marginal seas. We surveyed genetic variation at 11 microsatellite loci and mitochondrial (mt) DNA in samples from twelve locations from the Sea of Japan to Washington State. Both microsatellite (mean H = 0.868) and mtDNA haplotype (mean h = 0.958) diversities were large and did not show any geographical trends. Genetic differentiation between samples was significantly correlated with geographical distance between samples for both microsatellites (FST = 0.028, r(2) = 0.33) and mtDNA (FST = 0.027, r(2) = 0.18). Both marker classes showed a strong genetic discontinuity between northwestern and northeastern Pacific populations that likely represents groups previously isolated during glaciations that are now in secondary contact. Significant differences appeared between samples from the Sea of Japan and Okhotsk Sea that may reflect ice-age isolations in the northwest Pacific. In the northeast Pacific, a microsatellite and mtDNA partition was detected between coastal and Georgia Basin populations. The presence of two major coastal mtDNA lineages on either side of the Pacific Ocean basin implies at least two ice-age refugia and separate postglacial population expansions facilitated by different glacial histories. Northward expansions into the Gulf of Alaska were possible 14-15 kyr ago, but deglaciation and colonization of the Georgia Basin probably occurred somewhat later. Population expansions were evident in mtDNA mismatch distributions and in Bayesian skyline plots of the three major lineages, but the start of expansions appeared to pre-date the last glacial maximum.

Biogeographic evidence for selection on mitochondrial DNA in North Pacific walleye pollock Theragra chalcogramma.

Three major mitochondrial DNA (mtDNA) haplogroups were identified in 5 data sets for North Pacific and Bering Sea walleye pollock. The common haplogroup A showed mirror-image clines on both sides of the North Pacific with high frequencies in southern areas (P(A) > 0.84) and low frequencies in the Bering Sea (P(A) < 0.36). Two additional haplogroups showed complimentary, but weaker, clines in the opposite direction. These clines are unlikely to have arisen by chance during postglacial colonizations of coastal waters in the North Pacific and Bering Sea, and they do not appear to reflect isolation by distance. Contrary to these trends, pollock at the western end of the Aleutian Island Archipelago were genetically more similar to Asian than to North American pollock, a pattern likely reflecting postglacial colonization. Haplogroup F(ST) values for a given haplotype diversity were significantly larger than expected under the island model of migration and random drift, a result implicating natural selection. Frequencies of haplogroup A were highly correlated with sea surface temperature (r > 0.91), whereas frequencies of groups B and C showed negative correlations with temperature. Selection may be operating directly on mtDNA variability or may be mediated through cytonuclear interactions. This biogeographic evidence adds to a growing body of literature indicating that selection may play a greater role in sculpting mtDNA variability than previously thought.