Genomic differentiation in Pacific cod using Pool-Seq.

Patterns of genetic differentiation across the genome can provide insight into selective forces driving adaptation. We used pooled whole genome sequencing, gene annotation, and environmental covariates to evaluate patterns of genomic differentiation and to investigate mechanisms responsible for divergence among proximate Pacific cod (Gadus macrocephalus) populations from the Bering Sea and Aleutian Islands and more distant Washington Coast cod. Samples were taken from eight spawning locations, three of which were replicated to estimate consistency in allele frequency estimation. A kernel smoothing moving weighted average of relative divergence (F ST) identified 11 genomic islands of differentiation between the Aleutian Islands and Bering Sea samples. In some islands of differentiation, there was also elevated absolute divergence (d XY) and evidence for selection, despite proximity and potential for gene flow. Similar levels of absolute divergence (d XY) but roughly double the relative divergence (F ST) were observed between the distant Bering Sea and Washington Coast samples. Islands of differentiation were much smaller than the four large inversions among Atlantic cod ecotypes. Islands of differentiation between the Bering Sea and Aleutian Island were associated with SNPs from five vision system genes, which can be associated with feeding, predator avoidance, orientation, and socialization. We hypothesize that islands of differentiation between Pacific cod from the Bering Sea and Aleutian Islands provide evidence for adaptive differentiation despite gene flow in this commercially important marine species.

Evidence for selection and spatially distinct patterns found in a putative zona pellucida gene in Pacific cod, and implications for management.

Genetic differentiation has been observed in marine species even when no obvious barriers to gene flow exist, and understanding such differentiation is essential for effective fisheries management. Highly differentiated outlier loci can provide information on how genetic variation might not only contribute to local adaptation but may also be affected by historical demographic events. A locus which aligned to a predicted zona pellucida sperm-binding protein 3 gene (ZP3) in Atlantic cod (Gadus morhua) was previously identified as the highest outlier based on F ST in a RADseq study of Pacific cod (Gadus macrocephalus) across the West Coast of North America. However, because of the limited length of the RAD sequence and restricted geographic area of sampling, no conclusion on the functional significance of the observed variation was possible. In other marine species, ZP3 is involved in reproductive isolation, local adaptation, and has neofunctionalized as an antifreeze gene, and so it may provide important insights in functional population structure of Pacific cod. Here, we sequenced a 544-bp region of ZP3 in 230 Pacific cod collected from throughout their geographic range. We observed striking patterns of spatial structuring of ZP3 haplotypes, with a sharp break near Kodiak, Alaska, USA where populations within ~200 km of each other are nearly fixed for different haplotypes, contrasting a pattern of isolation by distance at other genetic markers in this region (F ST = 0.003). Phylogenetic analysis of ZP3 haplotypes revealed that the more southern haplotypes appear to be ancestral, with the northern haplotype evolving more recently, potentially in response to a novel selective pressure as Pacific cod recolonized northern latitudes after glaciation. The sharp break in haplotype frequencies suggests strong selective pressures are operating on small spatial scales and illustrates that selection can create high divergence even in marine species with ample opportunities for gene flow.

Ecosystem response persists after a prolonged marine heatwave.

Some of the longest and most comprehensive marine ecosystem monitoring programs were established in the Gulf of Alaska following the environmental disaster of the Exxon Valdez oil spill over 30 years ago. These monitoring programs have been successful in assessing recovery from oil spill impacts, and their continuation decades later has now provided an unparalleled assessment of ecosystem responses to another newly emerging global threat, marine heatwaves. The 2014-2016 northeast Pacific marine heatwave (PMH) in the Gulf of Alaska was the longest lasting heatwave globally over the past decade, with some cooling, but also continued warm conditions through 2019. Our analysis of 187 time series from primary production to commercial fisheries and nearshore intertidal to offshore oceanic domains demonstrate abrupt changes across trophic levels, with many responses persisting up to at least 5 years after the onset of the heatwave. Furthermore, our suite of metrics showed novel community-level groupings relative to at least a decade prior to the heatwave. Given anticipated increases in marine heatwaves under current climate projections, it remains uncertain when or if the Gulf of Alaska ecosystem will return to a pre-PMH state.

Genetic evidence of a northward range expansion in the eastern Bering Sea stock of Pacific cod.

Poleward species range shifts have been predicted to result from climate change, and many observations have confirmed such movement. Poleward shifts may represent a homogeneous shift in distribution, seasonal northward movement of specific populations, or colonization processes at the poleward edge of the distribution. The ecosystem of the Bering Sea has been changing along with the climate, moving from an arctic to a subarctic system. Several fish species have been observed farther north than previously reported and in increasing abundances. We examined one of these fish species, Pacific cod, in the northern Bering Sea (NBS) to assess whether they migrated from another stock in the eastern Bering Sea (EBS), Gulf of Alaska, or Aleutian Islands, or whether they represent a separate population. Genetic analyses using 3,599 single nucleotide polymorphism markers indicated that nonspawning cod collected in August 2017 in the NBS were similar to spawning stocks of cod in the EBS. This result suggests escalating northward movement of the large EBS stock during summer months. Whether the cod observed in the NBS migrate south during winter to spawn or remain in the NBS as a sink population is unknown.

Molecular phylogenetics of snailfishes (Cottoidei: Liparidae) based on MtDNA and RADseq genomic analyses, with comments on selected morphological characters.

Phylogenetic relationships of snailfishes of the family Liparidae were analyzed on the basis of two sets of molecular sequence data: one from the mitochondrial DNA cytochrome c oxidase subunit one gene (COI) and another from restriction-site associated genome-wide sequences (RADseq). The analysis of COI sequence data from at least 122 species of 18 genera from the Pacific, Atlantic, and Southern oceans resulted in a moderately well-resolved phylogeny among the major clades, albeit with significant polytomy among central clades. Nectoliparis was the sister of all other members of the family, followed by Liparis. Liparis, Careproctus, and Paraliparis were paraphyletic. Liparis was recovered in two closely related clades, with L. fucensis sister of all other liparids except Nectoliparis, and both Careproctus and Paraliparis were each recovered among at least three widely separated clades. The RADseq analysis of 26 species of 11 genera from the eastern North Pacific strongly confirmed the overall results of the COI analysis, with the exception of the paraphyly of Liparis due to the absence of L. fucensis. Our results show that the pelvic disc has been independently lost multiple times and the pectoral-fin girdle has been independently reduced in multiple lineages.

Inferring genetic connectivity in real populations, exemplified by coastal and oceanic Atlantic cod.

Genetic data are commonly used to estimate connectivity between putative populations, but translating them to demographic dispersal rates is complicated. Theoretical equations that infer a migration rate based on the genetic estimator FST , such as Wright's equation, FST ≈ 1/(4Nem + 1), make assumptions that do not apply to most real populations. How complexities inherent to real populations affect migration was exemplified by Atlantic cod in the North Sea and Skagerrak and was examined within an age-structured model that incorporated genetic markers. Migration was determined under various scenarios by varying the number of simulated migrants until the mean simulated level of genetic differentiation matched a fixed level of genetic differentiation equal to empirical estimates. Parameters that decreased the Ne /Nt ratio (where Ne is the effective and Nt is the total population size), such as high fishing mortality and high fishing gear selectivity, increased the number of migrants required to achieve empirical levels of genetic differentiation. Higher maturity-at-age and lower selectivity increased Ne /Nt and decreased migration when genetic differentiation was fixed. Changes in natural mortality, fishing gear selectivity, and maturity-at-age within expected limits had a moderate effect on migration when genetic differentiation was held constant. Changes in population size had the greatest effect on the number of migrants to achieve fixed levels of FST , particularly when genetic differentiation was low, FST ≈ 10-3 Highly variable migration patterns, compared with constant migration, resulted in higher variance in genetic differentiation and higher extreme values. Results are compared with and provide insight into the use of theoretical equations to estimate migration among real populations.

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.

Twelve microsatellite loci for lake trout (Salvelinus namaycush).

We describe 12 microsatellite loci isolated from lake trout (Salvelinus namaycush). The number of alleles at these loci ranged from two to 11 with an average of 5.3 alleles per locus. The expected heterozygosity ranged from 0.29 to 0.76, with an average of 0.68. Accidental (or illegal) introductions of lake trout into watersheds are decimating native trout populations in the northern Rocky Mountains, and these loci will be useful for identifying the source of these introductions and for estimating the number of founding individuals.

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.