Population structure and adaptive differentiation in the sea cucumber Apostichopus californicus and implications for spatial resource management.

A growing body of evidence suggests that spatial population structure can develop in marine species despite large population sizes and high gene flow. Characterizing population structure is important for the effective management of exploited species, as it can be used to identify appropriate scales of management in fishery and aquaculture contexts. The California sea cucumber, Apostichopus californicus, is one such exploited species whose management could benefit from further characterization of population structure. Using restriction site-associated DNA (RAD) sequencing, we developed 2075 single nucleotide polymorphisms (SNPs) to quantify genetic structure over a broad section of the species' range along the North American west coast and within the Salish Sea, a region supporting the Washington State A. californicus fishery and developing aquaculture production of the species. We found evidence for population structure (global fixation index (FST) = 0.0068) with limited dispersal driving two patterns of differentiation: isolation-by-distance and a latitudinal gradient of differentiation. Notably, we found detectable population differences among collection sites within the Salish Sea (pairwise FST = 0.001-0.006). Using FST outlier detection and gene-environment association, we identified 10.2% of total SNPs as putatively adaptive. Environmental variables (e.g., temperature, salinity) from the sea surface were more correlated with genetic variation than those same variables measured near the benthos, suggesting that selection on pelagic larvae may drive adaptive differentiation to a greater degree than selection on adults. Our results were consistent with previous estimates of and patterns in population structure for this species in other extents of the range. Additionally, we found that patterns of neutral and adaptive differentiation co-varied, suggesting that adaptive barriers may limit dispersal. Our study provides guidance to decision-makers regarding the designation of management units for A. californicus and adds to the growing body of literature identifying genetic population differentiation in marine species despite large, nominally connected populations.

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.

The pink salmon genome: Uncovering the genomic consequences of a two-year life cycle.

Pink salmon (Oncorhynchus gorbuscha) adults are the smallest of the five Pacific salmon native to the western Pacific Ocean. Pink salmon are also the most abundant of these species and account for a large proportion of the commercial value of the salmon fishery worldwide. A two-year life history of pink salmon generates temporally isolated populations that spawn either in even-years or odd-years. To uncover the influence of this genetic isolation, reference genome assemblies were generated for each year-class and whole genome re-sequencing data was collected from salmon of both year-classes. The salmon were sampled from six Canadian rivers and one Japanese river. At multiple centromeres we identified peaks of Fst between year-classes that were millions of base-pairs long. The largest Fst peak was also associated with a million base-pair chromosomal polymorphism found in the odd-year genome near a centromere. These Fst peaks may be the result of a centromere drive or a combination of reduced recombination and genetic drift, and they could influence speciation. Other regions of the genome influenced by odd-year and even-year temporal isolation and tentatively under selection were mostly associated with genes related to immune function, organ development/maintenance, and behaviour.

Functional genetic diversity in an exploited marine species and its relevance to fisheries management.

The timing of reproduction influences key evolutionary and ecological processes in wild populations. Variation in reproductive timing may be an especially important evolutionary driver in the marine environment, where the high mobility of many species and few physical barriers to migration provide limited opportunities for spatial divergence to arise. Using genomic data collected from spawning aggregations of Pacific herring (Clupea pallasii) across 1600 km of coastline, we show that reproductive timing drives population structure in these pelagic fish. Within a specific spawning season, we observed isolation by distance, indicating that gene flow is also geographically limited over our study area. These results emphasize the importance of considering both seasonal and spatial variation in spawning when delineating management units for herring. On several chromosomes, we detected linkage disequilibrium extending over multiple Mb, suggesting the presence of chromosomal rearrangements. Spawning phenology was highly correlated with polymorphisms in several genes, in particular SYNE2, which influences the development of retinal photoreceptors in vertebrates. SYNE2 is probably within a chromosomal rearrangement in Pacific herring and is also associated with spawn timing in Atlantic herring (Clupea harengus). The observed genetic diversity probably underlies resource waves provided by spawning herring. Given the ecological, economic and cultural significance of herring, our results support that conserving intraspecific genetic diversity is important for maintaining current and future ecosystem processes.

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.