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.

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.

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.

Application of Omics Tools in Designing and Monitoring Marine Protected Areas For a Sustainable Blue Economy.

A key component of the global blue economy strategy is the sustainable extraction of marine resources and conservation of marine environments through networks of marine protected areas (MPAs). Connectivity and representativity are essential factors that underlie successful implementation of MPA networks, which can safeguard biological diversity and ecosystem function, and ultimately support the blue economy strategy by balancing ocean use with conservation. New "big data" omics approaches, including genomics and transcriptomics, are becoming essential tools for the development and maintenance of MPA networks. Current molecular omics techniques, including population-scale genome sequencing, have direct applications for assessing population connectivity and for evaluating how genetic variation is represented within and among MPAs. Effective baseline characterization and long-term, scalable, and comprehensive monitoring are essential for successful MPA management, and omics approaches hold great promise to characterize the full range of marine life, spanning the microbiome to megafauna across a range of environmental conditions (shallow sea to the deep ocean). Omics tools, such as eDNA metabarcoding can provide a cost-effective basis for biodiversity monitoring in large and remote conservation areas. Here we provide an overview of current omics applications for conservation planning and monitoring, with a focus on metabarcoding, metagenomics, and population genomics. Emerging approaches, including whole-genome sequencing, characterization of genomic architecture, epigenomics, and genomic vulnerability to climate change are also reviewed. We demonstrate that the operationalization of omics tools can enhance the design, monitoring, and management of MPAs and thus will play an important role in a modern and comprehensive blue economy strategy.

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.

Application of Temporary, Cell-Containing Alginate Microcarriers to Facilitate the Fabrication of Spatially Defined Cell Pockets in 3D Collagen Hydrogels.

Mimicking the complexity of natural tissue is a major challenge in the field of tissue engineering. Here, a facile 2-step fabrication method to prepare 3D constructs with distinct regions of high cell concentrations and without the need for elaborate equipment is proposed. The initial incorporation of cells in a sacrificial alginate matrix allows the addition of other, cell relevant biopolymers, such as, collagen to form a spatially confined, interpenetrating network at the microscale. A layered structure at the macroscale can be achieved by incorporating these cell-containing microspheres in thin collagen layers. Cells are locally released by de-gelling the alginate matrix and their attachment to the collagen hydrogel layers has been studied. The use of the murine pre-osteoblast cell line MC3T3-E1 as an example cell line shows that the cells behave differently in their cell migration pattern based on the initial composition of the alginate microspheres.

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.

Tailoring the assembly of collagen fibers in alginate microspheres.

The application of microspheres instead of bulk hydrogels in cell-laden biomaterials offers multiple advantages such as a high surface-to-volume-ratio and, consequently, a better nutrition and oxygen transfer to and from cells. The preparation of inert alginate microspheres is facile, quick, and well-established and the fabrication of alginate-collagen microspheres has been previously reported. However, no detailed characterization of the collagen fibrillogenesis in the alginate matrix is available. We use second-harmonic imaging microscopy reflection confocal microscopy and turbidity assay to study the assembly of collagen in alginate microspheres. We show that the assembly of collagen fibers in a gelled alginate matrix is a complex process that can be aided by addition of small polar molecules, such as glycine and by a careful selection of the gelling buffer used to prepare alginate hydrogels.

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.

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.

A migration-associated supergene reveals loss of biocomplexity in Atlantic cod.

Chromosome structural variation may underpin ecologically important intraspecific diversity by reducing recombination within supergenes containing linked, coadapted alleles. Here, we confirm that an ancient chromosomal rearrangement is strongly associated with migratory phenotype and individual genetic structure in Atlantic cod (Gadus morhua) across the Northwest Atlantic. We reconstruct trends in effective population size over the last century and reveal declines in effective population size matching onset of industrialized harvest (after 1950). We find different demographic trajectories between individuals homozygous for the chromosomal rearrangement relative to heterozygous or homozygous individuals for the noninverted haplotype, suggesting different selective histories across the past 150 years. These results illustrate how chromosomal structural diversity can mediate fine-scale genetic, phenotypic, and demographic variation in a highly connected marine species and show how overfishing may have led to loss of biocomplexity within Northern cod stock.

Chromosome polymorphisms track trans-Atlantic divergence and secondary contact in Atlantic salmon.

Pleistocene glaciations drove repeated range contractions and expansions shaping contemporary intraspecific diversity. Atlantic salmon (Salmo salar) in the western and eastern Atlantic diverged >600,000 years before present, with the two lineages isolated in different southern refugia during glacial maxima, driving trans-Atlantic genomic and karyotypic divergence. Here, we investigate the genomic consequences of glacial isolation and trans-Atlantic secondary contact using 108,870 single nucleotide polymorphisms genotyped in 80 North American and European populations. Throughout North America, we identified extensive interindividual variation and discrete linkage blocks within and between chromosomes with known trans-Atlantic differences in rearrangements: Ssa01/Ssa23 translocation and Ssa08/Ssa29 fusion. Spatial genetic analyses suggest independence of rearrangements, with Ssa01/Ssa23 showing high European introgression (>50%) in northern populations indicative of post-glacial trans-Atlantic secondary contact, contrasting with low European ancestry genome-wide (3%). Ssa08/Ssa29 showed greater intrapopulation diversity, suggesting a derived chromosome fusion polymorphism that evolved within North America. Evidence of potential selection on both genomic regions suggests that the adaptive role of rearrangements warrants further investigation in Atlantic salmon. Our study highlights how Pleistocene glaciations can influence large-scale intraspecific variation in genomic architecture of northern species.

Demographic and genetic description of Greenland's only indigenous Atlantic salmon Salmo salar population.

A survey of the Kapisillit River system was conducted in 2005 and 2012 to study the only indigenous Atlantic salmon Salmo salar population in Greenland. Little is known about its characteristics or its relationship with other S. salar populations across the species range. Juvenile S. salar were captured in all stations surveyed within the lower river with the highest densities lower in the river and decreasing densities with increasing distance from the river mouth. Captured juveniles ranged from 0+ to 7+ years old and the predominant smolt age was between 4 and 6 years. Median length of 0+ and 1+ juveniles in August-September was 38.8 and 70.4 mm, respectively. The proportion of mature male parr increased from 4% for 1+ year old fish to 95% for fish greater than 2 years old. Genetic analysis using 96 single nucleotide polymorphisms (SNP) revealed a high degree of genetic similarity between collections, extremely low genetic diversity and low estimates of effective population size (Ne = 28.7; 95% CI = 19.7-42.4). Genetic comparison to range-wide S. salar populations demonstrated that the Kapisillit River S. salar is an outgroup of the eastern Atlantic stock complex, which is consistent with the hypothesised colonisation from the east. River morphology and the absence of glacier runoff are hypothesised to be the main reasons for the relatively high river temperatures supporting this self-sustaining population of S. salar. Given its uniqueness and persistence, this population represents an important part of range-wide biodiversity of S. salar.

Fine-scale temperature-associated genetic structure between inshore and offshore populations of sea scallop (Placopecten magellanicus).

In the northwest Atlantic Ocean, sea scallop (Placopecten magellanicus) has been characterized by a latitudinal genetic cline with a breakpoint between northern and southern genetic clusters occurring at ~45°N along eastern Nova Scotia, Canada. Using 96 diagnostic single-nucleotide polymorphisms (SNPs) capable of discriminating between northern and southern clusters, we examined fine-scale genetic structure of scallops among 27 sample locations, spanning the largest geographic range evaluated in this species to date (~37-51°N). Here, we confirmed previous observations of northern and southern groups, but we show that the boundary between northern and southern clusters is not a discrete latitudinal break. Instead, at latitudes near the previously described boundary, we found unexpected patterns of fine-scale genetic structure occurring between inshore and offshore sites. Scallops from offshore sites, including St. Pierre Bank and the eastern Scotian Shelf, clustered with southern stocks, whereas inshore sites at similar latitudes clustered with northern stocks. Our analyses revealed significant genetic divergence across small spatial scales (i.e., 129-221 km distances), and that spatial structure over large and fine scales was strongly associated with temperature during seasonal periods of thermal minima. Clear temperature differences between inshore and offshore locations may explain the fine-scale structuring observed, such as why southern lineages of scallop occur at higher latitudes in deeper, warmer offshore waters. Our study supports growing evidence that fine-scale population structure in marine species is common, often environmentally associated, and that consideration of environmental and genomic data can significantly enhance the identification of marine diversity and management units.

Temporal dynamics of genetic clines of invasive European green crab (Carcinus maenas) in eastern North America.

Two genetically distinct lineages of European green crabs (Carcinus maenas) were independently introduced to eastern North America, the first in the early 19th century and the second in the late 20th century. These lineages first came into secondary contact in southeastern Nova Scotia, Canada (NS), where they hybridized, producing latitudinal genetic clines. Previous studies have documented a persistent southward shift in the clines of different marker types, consistent with existing dispersal and recruitment pathways. We evaluated current clinal structure by quantifying the distribution of lineages and fine-scale hybridization patterns across the eastern North American range (25 locations, ~39 to 49°N) using informative single nucleotide polymorphisms (SNPs; n = 96). In addition, temporal changes in the genetic clines were evaluated using mitochondrial DNA and microsatellite loci (n = 9-11) over a 15-year period (2000-2015). Clinal structure was consistent with prior work demonstrating the existence of both northern and southern lineages with a hybrid zone occurring between southern New Brunswick (NB) and southern NS. Extensive later generation hybrids were detected in this region and in southeastern Newfoundland. Temporal genetic analysis confirmed the southward progression of clines over time; however, the rate of this progression was slower than predicted by forecasting models, and current clines for all marker types deviated significantly from these predictions. Our results suggest that neutral and selective processes contribute to cline dynamics, and ultimately, highlight how selection, hybridization, and dispersal can collectively influence invasion success.

Significant differences in maternal carotenoid provisioning and effects on offspring fitness in Chinook salmon colour morphs.

In oviparous species, maternal carotenoid provisioning can deliver diverse fitness benefits to offspring via increased survival, growth and immune function. Despite demonstrated advantages of carotenoids, large intra- and interspecific variation in carotenoid utilization exists, suggesting trade-offs associated with carotenoids. In Chinook salmon (Oncorhynchus tshawytscha), extreme variation in carotenoid utilization delineates two colour morphs (red and white) that differ genetically in their ability to deposit carotenoids into tissues. Here, we take advantage of this natural variation to examine how large differences in maternal carotenoid provisioning influence offspring fitness. Using a full factorial breeding design crossing morphs and common-garden rearing, we measured differences in a suite of fitness-related traits, including survival, growth, viral susceptibility and host response, in offspring of red (carotenoid-rich eggs) and white (carotenoid-poor eggs) females. Eggs of red females had significantly higher carotenoid content than those of white females (6× more); however, this did not translate into measurable differences in offspring fitness. Given that white Chinook salmon may have evolved to counteract their maternal carotenoid deficiency, we also examined the relationship between egg carotenoid content and offspring fitness within each morph separately. Egg carotenoids only had a positive effect within the red morph on survival to eyed-egg (earliest measured trait), but not within the white morph. Although previous work shows that white females benefit from reduced egg predation, our study also supports a hypothesis that white Chinook salmon have evolved additional mechanisms to improve egg survival despite low carotenoids, providing novel insight into evolutionary mechanisms that maintain this stable polymorphism.

Environmental extremes drive population structure at the northern range limit of Atlantic salmon in North America.

Conservation of exploited species requires an understanding of both genetic diversity and the dominant structuring forces, particularly near range limits, where climatic variation can drive rapid expansions or contractions of geographic range. Here, we examine population structure and landscape associations in Atlantic salmon (Salmo salar) across a heterogeneous landscape near the northern range limit in Labrador, Canada. Analysis of two amplicon-based data sets containing 101 microsatellites and 376 single nucleotide polymorphisms (SNPs) from 35 locations revealed clear differentiation between populations spawning in rivers flowing into a large marine embayment (Lake Melville) compared to coastal populations. The mechanisms influencing the differentiation of embayment populations were investigated using both multivariate and machine-learning landscape genetic approaches. We identified temperature as the strongest correlate with genetic structure, particularly warm temperature extremes and wider annual temperature ranges. The genomic basis of this divergence was further explored using a subset of locations (n = 17) and a 220K SNP array. SNPs associated with spatial structuring and temperature mapped to a diverse set of genes and molecular pathways, including regulation of gene expression, immune response, and cell development and differentiation. The results spanning molecular marker types and both novel and established methods clearly show climate-associated, fine-scale population structure across an environmental gradient in Atlantic salmon near its range limit in North America, highlighting valuable approaches for predicting population responses to climate change and managing species sustainability.