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.

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.

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.

Extensive hybridization following a large escape of domesticated Atlantic salmon in the Northwest Atlantic.

Domestication is rife with episodes of interbreeding between cultured and wild populations, potentially challenging adaptive variation in the wild. In Atlantic salmon, Salmo salar, the number of domesticated individuals far exceeds wild individuals, and escape events occur regularly, yet evidence of the magnitude and geographic scale of interbreeding resulting from individual escape events is lacking. We screened juvenile Atlantic salmon using 95 single nucleotide polymorphisms following a single, large aquaculture escape in the Northwest Atlantic and report the landscape-scale detection of hybrid and feral salmon (27.1%, 17/18 rivers). Hybrids were reproductively viable, and observed at higher frequency in smaller wild populations. Repeated annual sampling of this cohort revealed decreases in the presence of hybrid and feral offspring over time. These results link previous observations of escaped salmon in rivers with reports of population genetic change, and demonstrate the potential negative consequences of escapes from net-pen aquaculture on wild populations.

A comparison of muscle- and scale-derived delta13C and delta15N across three life-history stages of Atlantic salmon, Salmo salar.

Stable isotope signatures were obtained from paired scale and muscle tissue samples from smolt, post-smolt and one-sea-winter adult Atlantic salmon (Salmo salar). Post-smolt and adult scales were separated into central and outer (marine) portions with analyses carried out on the marine growth section of both life-history stages and the central portion for the adult scales. Muscle and scale delta(13)C and delta(15)N signatures were assessed (1) to determine whether a linear relationship exists between tissue types, (2) to determine if a constant offset exists between tissue signatures across all life-history stages, and (3) to evaluate whether underplating imparts a significant bias to life-history scale segments that would preclude their use in retrospective analyses of any ontogenetic dietary changes between life-history stages. Significant correlations were found to exist between muscle and scale stable isotope signatures obtained from smolts (delta(13)C and delta(15)N) and adults (delta(15)N). Both the muscle and the scale signatures captured the dietary shift associated with the transition from freshwater to the marine environment. Post-smolt and adult scales were depleted relative to muscle tissue, which may be attributed to isotopic differences in amino acid composition between muscle and scale tissues. The results suggest that scales may better represent dietary carbon sources because they are not influenced by lipid dynamics. The scale, however, appears less responsive to short-term shifts in diet relative to muscle and, therefore, must be used only to infer seasonally integrated dietary patterns for slow-growing life-history stages.

A field-derived oxygen isotope fractionation equation for Salvelinus species.

Field-collected otolith samples of young-of the-year Arctic charr (Salvelinus alpinus) and brook charr (Salvelinus fontinalis) and monitored water temperatures were used to estimate a delta(18)O fractionation equation for the genus Salvelinus. When compared to literature reported equations, the developed fractionation equation had a statistically similar slope but dissimilar intercept. Statistical similarities among fractionation equation slope estimates suggest a common otolith delta(18)O incorporation response among fish species that may be interpreted as widespread equilibrium otolith delta(18)O deposition. Statistical dissimilarities among intercept estimates question broad applicability of any single fractionation equation to all fish species and were interpreted here to have biological meaning as a result of known differences in standard metabolic rates among species. Attempts to statistically cross-validate fractionation equations by prediction of water temperatures used in other fractionation studies indicated significant biases in the range of -7.9 to 6.7 degrees C that preclude the broad use of any single fractionation equation for accurate thermal reconstructions. Differences in equation intercepts and the prevalence of predictive biases do not support the conclusion of previous studies concerning the wide applicability and/or general accuracy of fractionation equations and suggest fractionation equations are best developed at the species- or taxon-specific (e.g., genus) level.

General effects of climate change on Arctic fishes and fish populations.

Projected shifts in climate forcing variables such as temperature and precipitation are of great relevance to arctic freshwater ecosystems and biota. These will result in many direct and indirect effects upon the ecosystems and fish present therein. Shifts projected for fish populations will range from positive to negative in overall effect, differ among species and also among populations within species depending upon their biology and tolerances, and will be integrated by the fish within their local aquascapes. This results in a wide range of future possibilities for arctic freshwater and diadromous fishes. Owing to a dearth of basic knowledge regarding fish biology and habitat interactions in the north, complicated by scaling issues and uncertainty in future climate projections, only qualitative scenarios can be developed in most cases. This limits preparedness to meet challenges of climate change in the Arctic with respect to fish and fisheries.

An overview of effects of climate change on selected arctic freshwater and anadromous fishes.

Arctic freshwater and diadromous fish species will respond to the various effects of climate change in many ways. For wide-ranging species, many of which are key components of northern aquatic ecosystems and fisheries, there is a large range of possible responses due to inter- and intra-specific variation, differences in the effects of climate drivers within ACIA regions, and differences in drivers among regions. All this diversity, coupled with limited understanding of fish responses to climate parameters generally, permits enumeration only of a range of possible responses which are developed here for selected important fishes. Accordingly, in-depth examination is required of possible effects within species within ACIA regions, as well as comparative studies across regions. Two particularly important species (Arctic char and Atlantic salmon) are examined as case studies to provide background for such studies.

Effects of climate change and UV radiation on fisheries for arctic freshwater and anadromous species.

Fisheries for arctic freshwater and diadromous fish species contribute significantly to northern economies. Climate change, and to a lesser extent increased ultraviolet radiation, effects in freshwaters will have profound effects on fisheries from three perspectives: quantity of fish available, quality of fish available, and success of the fishers. Accordingly, substantive adaptation will very likely be required to conduct fisheries sustainably in the future as these effects take hold. A shift to flexible and rapidly responsive 'adaptive management' of commercial fisheries will be necessary; local land- and resource-use patterns for subsistence fisheries will change; and, the nature, management and place for many recreational fisheries will change. Overall, given the complexity and uncertainty associated with climate change and related effects on arctic freshwaters and their biota, a much more conservative approach to all aspects of fishery management will be required to ensure ecosystems and key fished species retain sufficient resiliency and capacity to meet future changes.