Variable parallelism in the genomic basis of age at maturity across spatial scales in Atlantic Salmon.

Complex traits often exhibit complex underlying genetic architectures resulting from a combination of evolution from standing variation, hard and soft sweeps, and alleles of varying effect size. Increasingly, studies implicate both large-effect loci and polygenic patterns underpinning adaptation, but the extent that common genetic architectures are utilized during repeated adaptation is not well understood. Sea age or age at maturation represents a significant life history trait in Atlantic Salmon (Salmo salar), the genetic basis of which has been studied extensively in European Atlantic populations, with repeated identification of large-effect loci. However, the genetic basis of sea age within North American Atlantic Salmon populations remains unclear, as does the potential for a parallel trans-Atlantic genomic basis to sea age. Here, we used a large single-nucleotide polymorphism (SNP) array and low-coverage whole-genome resequencing to explore the genomic basis of sea age variation in North American Atlantic Salmon. We found significant associations at the gene and SNP level with a large-effect locus (vgll3) previously identified in European populations, indicating genetic parallelism, but found that this pattern varied based on both sex and geographic region. We also identified nonrepeated sets of highly predictive loci associated with sea age among populations and sexes within North America, indicating polygenicity and low rates of genomic parallelism. Despite low genome-wide parallelism, we uncovered a set of conserved molecular pathways associated with sea age that were consistently enriched among comparisons, including calcium signaling, MapK signaling, focal adhesion, and phosphatidylinositol signaling. Together, our results indicate parallelism of the molecular basis of sea age in North American Atlantic Salmon across large-effect genes and molecular pathways despite population-specific patterns of polygenicity. These findings reveal roles for both contingency and repeated adaptation at the molecular level in the evolution of life history variation.

Multifaceted framework for defining conservation units: An example from Atlantic salmon (Salmo salar) in Canada.

Conservation units represent important components of intraspecific diversity that can aid in prioritizing and protecting at-risk populations, while also safeguarding unique diversity that can contribute to species resilience. In Canada, identification and assessments of conservation units is done by the Committee on the Status of Endangered Wildlife in Canada (COSEWIC). COSEWIC can recognize conservation units below the species level (termed "designatable units"; DUs) if the unit has attributes that make it both discrete and evolutionarily significant. There are various ways in which a DU can meet criteria of discreteness and significance, and increasing access to "big data" is providing unprecedented information that can directly inform both criteria. Specifically, the incorporation of genomic data for an increasing number of non-model species is informing more COSEWIC assessments; thus, a repeatable, robust framework is needed for integrating these data into DU characterization. Here, we develop a framework that uses a multifaceted, weight of evidence approach to incorporate multiple data types, including genetic and genomic data, to inform COSEWIC DUs. We apply this framework to delineate DUs of Atlantic salmon (Salmo salar, L.), an economically, culturally, and ecologically significant species, that is also characterized by complex hierarchical population structure. Specifically, we focus on an in-depth example of how our approach was applied to a previously data limited region of northern Canada that was defined by a single large DU. Application of our framework with newly available genetic and genomic data led to subdividing this DU into three new DUs. Although our approach was developed to meet criteria of COSEWIC, it is widely applicable given similarities in the definitions of a conservation unit.

Fine-scale environmentally associated spatial structure of lumpfish (Cyclopterus lumpus) across the Northwest Atlantic.

Lumpfish, Cyclopterus lumpus, have historically been harvested throughout Atlantic Canada and are increasingly in demand as a solution to controlling sea lice in Atlantic salmon farms-a process which involves both the domestication and the transfer of lumpfish between geographic regions. At present, little is known regarding population structure and diversity of wild lumpfish in Atlantic Canada, limiting attempts to assess the potential impacts of escaped lumpfish individuals from salmon pens on currently at-risk wild populations. Here, we characterize the spatial population structure and genomic-environmental associations of wild populations of lumpfish throughout the Northwest Atlantic using both 70K SNP array data and whole-genome re-sequencing data (WGS). At broad spatial scales, our results reveal a large environmentally associated genetic break between the southern populations (Gulf of Maine and Bay of Fundy) and northern populations (Newfoundland and the Gulf of St. Lawrence), linked to variation in ocean temperature and ice cover. At finer spatial scales, evidence of population structure was also evident in a distinct coastal group in Newfoundland and significant isolation by distance across the northern region. Both evidence of consistent environmental associations and elevated genome-wide variation in F ST values among these three regional groups supports their biological relevance. This study represents the first extensive description of population structure of lumpfish in Atlantic Canada, revealing evidence of broad and fine geographic scale environmentally associated genomic diversity. Our results will facilitate the commercial use of lumpfish as a cleaner fish in Atlantic salmon aquaculture, the identification of lumpfish escapees, and the delineation of conservation units of this at-risk species throughout Atlantic Canada.

Whole-genome sequencing reveals fine-scale environment-associated divergence near the range limits of a temperate reef fish.

Environmental variation is increasingly recognized as an important driver of diversity in marine species despite the lack of physical barriers to dispersal and the presence of pelagic stages in many taxa. A robust understanding of the genomic and ecological processes involved in structuring populations is lacking for most marine species, often hindering management and conservation action. Cunner (Tautogolabrus adspersus) is a temperate reef fish with both pelagic early life-history stages and strong site-associated homing as adults; the species is also of interest for use as a cleaner fish in salmonid aquaculture in Atlantic Canada. We aimed to characterize genomic and geographic differentiation of cunner in the Northwest Atlantic. To achieve this, a chromosome-level genome assembly for cunner was produced and used to characterize spatial population structure throughout Atlantic Canada using whole-genome sequencing. The genome assembly spanned 0.72 Gbp and 24 chromosomes; whole-genome sequencing of 803 individuals from 20 locations from Newfoundland to New Jersey identified approximately 11 million genetic variants. Principal component analysis revealed four regional Atlantic Canadian groups. Pairwise FST and selection scans revealed signals of differentiation and selection at discrete genomic regions, including adjacent peaks on chromosome 10 across multiple pairwise comparisons (i.e. FST 0.5-0.75). Redundancy analysis suggested association of environmental variables related to benthic temperature and oxygen range with genomic structure. Results suggest regional scale diversity in this temperate reef fish and can directly inform the collection and translocation of cunner for aquaculture applications and the conservation of wild populations throughout the Northwest Atlantic.

Genomic and machine learning-based screening of aquaculture-associated introgression into at-risk wild North American Atlantic salmon (Salmo salar) populations.

The negative genetic impacts of gene flow from domestic to wild populations can be dependent on the degree of domestication and exacerbated by the magnitude of pre-existing genetic differences between wild populations and the domestication source. Recent evidence of European ancestry within North American aquaculture Atlantic salmon (Salmo salar) has elevated the potential impact of escaped farmed salmon on often at-risk wild North American salmon populations. Here, we compare the ability of single nucleotide polymorphism (SNP) and microsatellite (SSR) marker panels of different sizes (7-SSR, 100-SSR and 220K-SNP) to detect introgression of European genetic information into North American wild and aquaculture populations. Linear regression comparing admixture predictions for a set of individuals common to the three datasets showed that the 100-SSR panel and 7-SSR panels replicated the full 220K-SNP-based admixture estimates with low accuracy (r2 of .64 and .49, respectively). Additional tests explored the effects of individual sample size and marker number, which revealed that ~300 randomly selected SNPs could replicate the 220K-SNP admixture predictions with greater than 95% fidelity. We designed a custom SNP panel (301-SNP) for European admixture detection in future monitoring work and then developed and tested a python package, salmoneuadmix (https://github.com/CNuge/SalmonEuAdmix), which uses a deep neural network to make de novo estimates of individuals' European admixture proportion without the need to conduct complete admixture analysis utilizing baseline samples. The results demonstrate the mobilization of targeted SNP panels and machine learning in support of at-risk species conservation and management.

Geography, environment, and colonization history interact with morph type to shape genomic variation in an Arctic fish.

Polymorphic species are useful models for investigating the evolutionary processes driving diversification. Such processes include colonization history as well as contemporary selection, gene flow, and genetic drift, which can vary between intraspecific morphs as a function of their distinct life histories. The interactive and relative influence of such evolutionary processes on morph differentiation critically informs morph-specific management decisions and our understanding of incipient speciation. We therefore investigated how geographic distance, environmental conditions, and colonization history interacted with morph migratory capacity in the highly polymorphic fish species, Arctic Charr (Salvelinus alpinus). Using an 87 k SNP chip we genetically characterized recently evolved anadromous, resident, and landlocked charr collected from 45 locations across a secondary contact zone of three charr glacial lineages in eastern Canada. A strong pattern of isolation by distance across all populations suggested geographic distance principally shaped genetic structure. Landlocked populations had lower genetic diversities and higher genetic differentiation than anadromous populations. However, effective population size was generally temporally stable in landlocked populations in comparison to anadromous populations. Genetic diversity positively correlated with latitude, potentially indicating southern anadromous populations' vulnerability to climate change and greater introgression between the Arctic and Atlantic glacial lineages in northern Labrador. Local adaptation was suggested by the observation of several environmental variables strongly associating with functionally relevant outlier genes including a region on chromosome AC21 potentially associated with anadromy. Our results demonstrate that gene flow, colonization history, and local adaptation uniquely interact to influence the genetic variation and evolutionary trajectory of populations.

Genomic evidence of recent European introgression into North American farmed and wild Atlantic salmon.

Gene flow between wild and domestic populations has been repeatedly demonstrated across a diverse range of taxa. Ultimately, the genetic impacts of gene flow from domestic into wild populations depend both on the degree of domestication and the original source of the domesticated population. Atlantic salmon, Salmo salar, used in North American aquaculture are ostensibly of North American origin. However, evidence of European introgression into North American aquaculture salmon has accumulated in recent decades, even though the use of diploid European salmon has never been approved in Canada. The full extent of such introgression as well as the potential impacts on wild salmon in the Northwest Atlantic remains uncertain. Here, we extend previous work comparing North American and European wild salmon (n = 5799) using a 220 K SNP array to quantify levels of recent European introgression into samples of domestic salmon, aquaculture escapees, and wild salmon collected throughout Atlantic Canada. Analysis of North American farmed salmon (n = 403) and escapees (n = 289) displayed significantly elevated levels of European ancestry by comparison with wild individuals (p < 0.001). Of North American farmed salmon sampled between 2011 and 2018, ~17% had more than 10% European ancestry and several individuals exceeded 40% European ancestry. Samples of escaped farmed salmon similarly displayed elevated levels of European ancestry, with two individuals classified as 100% European. Analysis of juvenile salmon collected in rivers proximate to aquaculture locations also revealed evidence of elevated European ancestry and larger admixture tract in comparison to individuals collected at distance from aquaculture. Overall, our results demonstrate that even though diploid European salmon have never been approved for use in Canada, individuals of full and partial European ancestry have been in use over the last decade, and that some of these individuals have escaped and hybridized in the wild.

The Genomic Consistency of the Loss of Anadromy in an Arctic Fish (Salvelinus alpinus).

AbstractThe potentially significant genetic consequences associated with the loss of migratory capacity of diadromous fishes that have become landlocked in freshwater are poorly understood. Consistent selective pressures associated with freshwater residency may drive repeated differentiation both between allopatric landlocked and anadromous populations and within landlocked populations (resulting in sympatric morphs). Alternatively, the strong genetic drift anticipated in isolated landlocked populations could hinder consistent adaptation, limiting genetic parallelism. Understanding the degree of genetic parallelism underlying differentiation has implications for both the predictability of evolution and management practices. We employed an 87k single-nucleotide polymorphism (SNP) array to examine the genetic characteristics of landlocked and anadromous Arctic char (Salvelinus alpinus) populations from five drainages within Labrador, Canada. One gene was detected as an outlier between sympatric, size-differentiated morphs in each of two landlocked lakes. While no single locus differentiated all replicate pairs of landlocked and anadromous populations, several SNPs, genes, and paralogs were consistently detected as outliers in at least 70% of these pairwise comparisons. A significant C-score suggested that the amount of shared outlier SNPs across all paired landlocked and anadromous populations was greater than expected by chance. Our results indicate that despite their isolation, selection due to the loss of diadromy may drive consistent genetic responses in landlocked populations.

Distinct early life stage gene expression effects of hybridization among European and North American farmed and wild Atlantic salmon populations.

Due to multigeneration domestication selection, farmed and wild Atlantic salmon diverge genetically, which raises concerns about potential genetic interactions among escaped farmed and wild populations and disruption of local adaptation through introgression. When farmed strains of distant geographic origin are used, it is unknown whether the genetic consequences posed by escaped farmed fish will be greater than if more locally derived strains are used. Quantifying gene transcript expression differences among divergent farmed, wild and F1  hybrids under controlled conditions is one of the ways to explore the consequences of hybridization. We compared the transcriptomes of fry at the end of yolk sac absorption of a European (EO) farmed ("StofnFiskur", Norwegian strain), a North American (NA) farmed (Saint John River, NB strain), a Newfoundland (NF) wild population with EO ancestry, and related F1  hybrids using 44 K microarrays. Our findings indicate that the wild population showed greater transcriptome differences from the EO farmed strain than that of the NA farmed strain. We also found the largest differences in global gene expression between the two farmed strains. We detected the fewest differentially expressed transcripts between F1  hybrids and domesticated/wild maternal strains. We also found that the differentially expressed genes between cross types over-represented GO terms associated with metabolism, development, growth, immune response, and redox homeostasis processes. These findings suggest that the interbreeding of escaped EO/NA farmed and NF wild population would alter gene transcription, and the consequences of hybridization would be greater from escaped EO farmed than NA farmed salmon, resulting in potential effects on the wild populations.

Reference genome of lumpfish Cyclopterus lumpus Linnaeus provides evidence of male heterogametic sex determination through the AMH pathway.

Teleosts exhibit extensive diversity of sex determination (SD) systems and mechanisms, providing the opportunity to study the evolution of SD and sex chromosomes. Here we sequenced the genome of the common lumpfish (Cyclopterus lumpus Linnaeus), a species of increasing importance to aquaculture, and identified the SD region and master SD locus using a 70 K single nucleotide polymorphism array and tissue-specific expression data. The chromosome-level assembly identified 25 diploid chromosomes with a total size of 572.89 Mb, a scaffold N50 of 23.86 Mb and genome annotation-predicted 21,480 protein-coding genes. Genome-wide association analysis located a highly sex-associated region on chromosome 13, suggesting that anti-Müllerian hormone (AMH) is the putative SD factor. Linkage disequilibrium and heterozygosity across chromosome 13 support a proto-XX/XY system, with an absence of widespread chromosome divergence between sexes. We identified three copies of AMH in the lumpfish primary and alternate haplotype assemblies localized in the SD region. Comparison to sequences from other teleosts suggested a monophyletic relationship and conservation within the Cottioidei. One AMH copy showed similarity to AMH/AMHY in a related species and was also the only copy with expression in testis tissue, suggesting this copy may be the functional copy of AMH in lumpfish. The two other copies arranged in tandem inverted duplication were highly similar, suggesting a recent duplication event. This study provides a resource for the study of early sex chromosome evolution and novel genomic resources that benefits lumpfish conservation management and aquaculture.

Environmentally associated chromosomal structural variation influences fine-scale population structure of Atlantic Salmon (Salmo salar).

Chromosomal rearrangements (e.g., inversions, fusions, and translocations) have long been associated with environmental variation in wild populations. New genomic tools provide the opportunity to examine the role of these structural variants in shaping adaptive differences within and among wild populations of non-model organisms. In Atlantic Salmon (Salmo salar), variations in chromosomal rearrangements exist across the species natural range, yet the role and importance of these structural variants in maintaining adaptive differences among wild populations remains poorly understood. We genotyped Atlantic Salmon (n = 1429) from 26 populations within a highly genetically structured region of southern Newfoundland, Canada with a 220K SNP array. Multivariate analysis, across two independent years, consistently identified variation in a structural variant (translocation between chromosomes Ssa01 and Ssa23), previously associated with evidence of trans-Atlantic secondary contact, as the dominant factor influencing population structure in the region. Redundancy analysis suggested that variation in the Ssa01/Ssa23 chromosomal translocation is strongly correlated with temperature. Our analyses suggest environmentally mediated selection acting on standing genetic variation in genomic architecture introduced through secondary contact may underpin fine-scale local adaptation in Placentia Bay, Newfoundland, Canada, a large and deep embayment, highlighting the importance of chromosomal structural variation as a driver of contemporary adaptive divergence.

Harnessing the power of multi-omics data for predicting climate change response.

Predicting how species will respond to future climate change is of central importance in the midst of the global biodiversity crisis, and recent work has demonstrated the utility of population genomics for improving these predictions. Here, we suggest a broadening of the approach to include other types of genomic variants that play an important role in adaptation, like structural (e.g. copy number variants) and epigenetic variants (e.g. DNA methylation). These data could provide additional power for forecasting response, especially in weakly structured or panmictic species. Incorporating structural and epigenetic variation into estimates of climate change vulnerability, or maladaptation, may not only improve prediction power but also provide insight into the molecular mechanisms underpinning species' response to climate change.

Genomic basis of deep-water adaptation in Arctic Charr (Salvelinus alpinus) morphs.

The post-glacial colonization of Gander Lake in Newfoundland, Canada, by Arctic Charr (Salvelinus alpinus) provides the opportunity to study the genomic basis of adaptation to extreme deep-water environments. Colonization of deep-water (>50 m) habitats often requires extensive adaptation to cope with novel environmental challenges from high hydrostatic pressure, low temperature, and low light, but the genomic mechanisms underlying evolution in these environments are rarely known. Here, we compare genomic divergence between a deep-water morph adapted to depths of up to 288 m and a larger, piscivorous pelagic morph occupying shallower depths. Using both a SNP array and resequencing of whole nuclear and mitochondrial genomes, we find clear genetic divergence (FST  = 0.11-0.15) between deep and shallow water morphs, despite an absence of morph divergence across the mitochondrial genome. Outlier analyses identified many diverged genomic regions containing genes enriched for processes such as gene expression and DNA repair, cardiac function, and membrane transport. Detection of putative copy number variants (CNVs) uncovered 385 genes with CNVs distinct to piscivorous morphs, and 275 genes with CNVs distinct to deep-water morphs, enriched for processes associated with synapse assembly. Demographic analyses identified evidence for recent and local morph divergence, and ongoing reductions in diversity consistent with postglacial colonization. Together, these results show that Arctic Charr morph divergence has occurred through genome-wide differentiation and elevated divergence of genes underlying multiple cellular and physiological processes, providing insight into the genomic basis of adaptation in a deep-water habitat following postglacial recolonization.

Genomic stability through time despite decades of exploitation in cod on both sides of the Atlantic.

The mode and extent of rapid evolution and genomic change in response to human harvesting are key conservation issues. Although experiments and models have shown a high potential for both genetic and phenotypic change in response to fishing, empirical examples of genetic responses in wild populations are rare. Here, we compare whole-genome sequence data of Atlantic cod (Gadus morhua) that were collected before (early 20th century) and after (early 21st century) periods of intensive exploitation and rapid decline in the age of maturation from two geographically distinct populations in Newfoundland, Canada, and the northeast Arctic, Norway. Our temporal, genome-wide analyses of 346,290 loci show no substantial loss of genetic diversity and high effective population sizes. Moreover, we do not find distinct signals of strong selective sweeps anywhere in the genome, although we cannot rule out the possibility of highly polygenic evolution. Our observations suggest that phenotypic change in these populations is not constrained by irreversible loss of genomic variation and thus imply that former traits could be reestablished with demographic recovery.

Chromosome level reference of Atlantic halibut Hippoglossus hippoglossus provides insight into the evolution of sexual determination systems.

Changes in the genetic mechanisms that control sexual determination have occurred independently across the tree of life, and with exceptional frequency in teleost fishes. To investigate the genomic changes underlying the evolution of sexual determination, we sequenced a chromosome-level genome, multitissue transcriptomes, and reduced representation population data for the Atlantic halibut (Hippoglossus hippoglossus), which has an XY/XX sex determination mechanism and has recently diverged (0.9-3.8 Ma) from the Pacific halibut (Hippoglossus stenolepis), which has a ZZ/ZW system. We used frequency and coverage-based population approaches to identify a putative sex-determining factor, GSDF. We characterized regions with elevated heterozygosity and linkage disequilibrium indicating suppression of recombination across a nascent sex chromosome. We detected testis-specific expression of GSDF, the sequence of which is highly conserved across flatfishes. Based on evidence from genome-wide association, coverage, linkage disequilibrium, testis and brain transcriptomes, and sequence conservation with other flatfishes, we propose a mechanism for the recent evolution of an XY sex-determination mechanism in Atlantic halibut. Changes to the ancestral sex-determining gene DMRT1 in regulating the downstream gene GSDF probably coincided with GSDF, or a proximal regulatory element of it, becoming the primary sex-determining factor. Our results suggest changes to a small number of elements can have drastic repercussions for the genomic substrate available to sex-specific evolutionary forces, providing insight into how certain elements repeatedly evolve to control sex across taxa. Our chromosome-level assembly, multitissue transcriptomes, and population genomic data provide a valuable resource and understanding of the evolution of sexual systems in fishes.

Limited genetic parallelism underlies recent, repeated incipient speciation in geographically proximate populations of an Arctic fish (Salvelinus alpinus).

The genetic underpinnings of incipient speciation, including the genomic mechanisms which contribute to morphological and ecological differentiation and reproductive isolation, remain poorly understood. The repeated evolution of consistently, phenotypically distinct morphs of Arctic Charr (Salvelinus alpinus) within the Quaternary period offer an ideal model to study the repeatability of evolution at the genomic level. Sympatric morphs of Arctic Charr are found across this species' circumpolar distribution. However, the specific genetic mechanisms driving this morph differentiation are largely unknown despite the cultural and economic importance of the anadromous morph. We used a newly designed 87k SNP chip to investigate the character and consistency of the genomic differences among sympatric morphs within three recently deglaciated and geographically proximate lakes in Labrador, Canada. We found genetically distinct small and large morph Arctic Charr in all three lakes consistent with resident and anadromous morphs, respectively. A degree of reproductive isolation among sympatric morphs is likely given genome-wide distributions of outlier SNPs and high genome-wide FST s. Across all lakes, outlier SNPs were largely nonoverlapping suggesting a lack of genetic parallelism driving morph differentiation. Alternatively, several genes and paralogous copies of the same gene consistently differentiated morphs across multiple lakes suggesting their importance to the manifestation of morphs. Our results confirm the utility of Arctic Charr as a model for investigating the predictability of evolution and support the importance of both genetic parallelism and nonparallelism to the incipient speciation of Arctic Charr morphs.

Multiple decades of stocking has resulted in limited hatchery introgression in wild brook trout (Salvelinus fontinalis) populations of Nova Scotia.

Many populations of freshwater fishes are threatened with losses, and increasingly, the release of hatchery individuals is one strategy being implemented to support wild populations. However, stocking of hatchery individuals may pose long-term threats to wild populations, particularly if genetic interactions occur between wild and hatchery individuals. One highly prized sport fish that has been heavily stocked throughout its range is the brook trout (Salvelinus fontinalis). In Nova Scotia, Canada, hatchery brook trout have been stocked since the early 1900s, and despite continued stocking efforts, populations have suffered declines in recent decades. Before this study, the genetic structure of brook trout populations in the province was unknown; however, given the potential negative consequences associated with hatchery stocking, it is possible that hatchery programs have adversely affected the genetic integrity of wild populations. To assess the influence of hatchery supplementation on wild populations, we genotyped wild brook trout from 12 river systems and hatchery brook trout from two major hatcheries using 100 microsatellite loci. Genetic analyses of wild trout revealed extensive population genetic structure among and within river systems and significant isolation-by-distance. Hatchery stocks were genetically distinct from wild populations, and most populations showed limited to no evidence of hatchery introgression (<5% hatchery ancestry). Only a single location had a substantial number of hatchery-derived trout and was located in the only river where a local strain is used for supplementation. The amount of hatchery stocking within a watershed did not influence the level of hatchery introgression. Neutral genetic structure of wild populations was influenced by geography with some influence of climate and stocking indices. Overall, our study suggests that long-term stocking has not significantly affected the genetic integrity of wild trout populations, highlighting the variable outcomes of stocking and the need to evaluate the consequences on a case-by-case basis.

Resolving fine-scale population structure and fishery exploitation using sequenced microsatellites in a northern fish.

The resiliency of populations and species to environmental change is dependent on the maintenance of genetic diversity, and as such, quantifying diversity is central to combating ongoing widespread reductions in biodiversity. With the advent of next-generation sequencing, several methods now exist for resolving fine-scale population structure, but the comparative performance of these methods for genetic assignment has rarely been tested. Here, we evaluate the performance of sequenced microsatellites and a single nucleotide polymorphism (SNP) array to resolve fine-scale population structure in a critically important salmonid in north eastern Canada, Arctic Charr (Salvelinus alpinus). We also assess the utility of sequenced microsatellites for fisheries applications by quantifying the spatial scales of movement and exploitation through genetic assignment of fishery samples to rivers of origin and comparing these results with a 29-year tagging dataset. Self-assignment and simulation-based analyses of 111 genome-wide microsatellite loci and 500 informative SNPs from 28 populations of Arctic Charr in north-eastern Canada identified largely river-specific genetic structure. Despite large differences (~4X) in the number of loci surveyed between panels, mean self-assignment accuracy was similar with the microsatellite loci and the SNP panel (>90%). Subsequent analysis of 996 fishery-collected samples using the microsatellite panel revealed that larger rivers contribute greater numbers of individuals to the fishery and that coastal fisheries largely exploit individuals originating from nearby rivers, corroborating results from traditional tagging experiments. Our results demonstrate the efficacy of sequence-based microsatellite genotyping to advance understanding of fine-scale population structure and harvest composition in northern and understudied species.

Divergent and linked selection shape patterns of genomic differentiation between European and North American Atlantic salmon (Salmo salar).

As populations diverge many processes can shape genomic patterns of differentiation. Regions of high differentiation can arise due to divergent selection acting on selected loci, genetic hitchhiking of nearby loci, or through repeated selection against deleterious alleles (linked background selection); this divergence may then be further elevated in regions of reduced recombination. Atlantic salmon (Salmo salar) from Europe and North America diverged >600,000 years ago and despite some evidence of secondary contact, the majority of genetic data indicate substantial divergence between lineages. This deep divergence with potential gene flow provides an opportunity to investigate the role of different mechanisms that shape the genomic landscape during early speciation. Here, using 184,295 single nucleotide polymorphisms (SNPs) and 80 populations, we investigate the genomic landscape of differentiation across the Atlantic Ocean with a focus on highly differentiated regions and the processes shaping them. We found evidence of high (mean FST  = 0.26) and heterogeneous genomic differentiation between continents. Genomic regions associated with high trans-Atlantic differentiation ranged in size from single loci (SNPs) within important genes to large regions (1-3 Mbp) on four chromosomes (Ssa06, Ssa13, Ssa16 and Ssa19). These regions showed signatures consistent with selection, including high linkage disequilibrium, despite no significant reduction in recombination. Genes and functional enrichment of processes associated with differentiated regions may highlight continental differences in ocean navigation and parasite resistance. Our results provide insight into potential mechanisms underlying differences between continents, and evidence of near-fixed and potentially adaptive trans-Atlantic differences concurrent with a background of high genome-wide differentiation supports subspecies designation in Atlantic salmon.

Modular chromosome rearrangements reveal parallel and nonparallel adaptation in a marine fish.

Genomic architecture and standing variation can play a key role in ecological adaptation and contribute to the predictability of evolution. In Atlantic cod (Gadus morhua), four large chromosomal rearrangements have been associated with ecological gradients and migratory behavior in regional analyses. However, the degree of parallelism, the extent of independent inheritance, and functional distinctiveness of these rearrangements remain poorly understood. Here, we use a 12K single nucleotide polymorphism (SNP) array to demonstrate extensive individual variation in rearrangement genotype within populations across the species range, suggesting that local adaptation to fine-scale ecological variation is enabled by rearrangements with independent inheritance. Our results demonstrate significant association of rearrangements with migration phenotype and environmental gradients across the species range. Individual rearrangements exhibit functional modularity, but also contain loci showing multiple environmental associations. Clustering in genetic distance trees and reduced differentiation within rearrangements across the species range are consistent with shared variation as a source of contemporary adaptive diversity in Atlantic cod. Conversely, we also find that haplotypes in the LG12 and LG1 rearranged region have diverged across the Atlantic, despite consistent environmental associations. Exchange of these structurally variable genomic regions, as well as local selective pressures, has likely facilitated individual diversity within Atlantic cod stocks. Our results highlight the importance of genomic architecture and standing variation in enabling fine-scale adaptation in marine species.