Vincent Bourret

SNP-array reveals genome-wide patterns of geographical and potential adaptive divergence across the natural range of Atlantic salmon (Salmo salar)

Atlantic salmon (Salmo salar) is one of the most extensively studied fish species in the world due to its significance in aquaculture, fisheries and ongoing conservation efforts to protect declining populations. Yet, limited genomic resources have hampered our understanding of genetic architecture in the species and the genetic basis of adaptation to the wide range of natural and artificial environments it occupies. In this study, we describe the development of a medium‐density Atlantic salmon single nucleotide polymorphism (SNP) array based on expressed sequence tags (ESTs) and genomic sequencing. The array was used in the most extensive assessment of population genetic structure performed to date in this species. A total of 6176 informative SNPs were successfully genotyped in 38 anadromous and freshwater wild populations distributed across the species natural range. Principal component analysis clearly differentiated European and North American populations, and within Europe, three major regional genetic groups were identified for the first time in a single analysis. We assessed the potential for the array to disentangle neutral and putative adaptive divergence of SNP allele frequencies across populations and among regional groups. In Europe, secondary contact zones were identified between major clusters where endogenous and exogenous barriers could be associated, rendering the interpretation of environmental influence on potentially adaptive divergence equivocal. A small number of markers highly divergent in allele frequencies (outliers) were observed between (multiple) freshwater and anadromous populations, between northern and southern latitudes, and when comparing Baltic populations to all others. We also discuss the potential future applications of the SNP array for conservation, management and aquaculture.

Population genetics of the American eel (Anguilla rostrata): FST = 0 and North Atlantic Oscillation effects on demographic fluctuations of a panmictic species

We performed population genetic analyses on the American eel (Anguilla rostrata) with three main objectives. First, we conducted the most comprehensive analysis of neutral genetic population structure to date to revisit the null hypothesis of panmixia in this species. Second, we used this data to provide the first estimates of contemporary effective population size (Ne) and to document temporal variation in effective number of breeders (Nb) in American eel. Third, we tested for statistical associations between temporal variation in the North Atlantic Oscillation (NAO), the effective number of breeders and two indices of recruit abundance. A total of 2142 eels from 32 sampling locations were genotyped with 18 microsatellite loci. All measures of differentiation were essentially zero, and no evidence for significant spatial or temporal genetic differentiation was found. The panmixia hypothesis should thus be accepted for this species. Nb estimates varied by a factor of 23 among 12 cohorts, from 473 to 10 999. The effective population size Ne was estimated at 10 532 (95% CI, 9312–11 752). This study also showed that genetically based demographic indices, namely Nb and allelic richness (Ar), can be used as surrogates for the abundance of breeders and recruits, which were both shown to be positively influenced by variation during high (positive) NAO phases. Thus, long‐term genetic monitoring of American glass eels at several sites along the North American Atlantic coast would represent a powerful and efficient complement to census monitoring to track demographic fluctuations and better understand their causes.

Conservation genomics of anadromous Atlantic salmon across its North American range: outlier loci identify the same patterns of population structure as neutral loci

Anadromous Atlantic salmon (Salmo salar) is a species of major conservation and management concern in North America, where population abundance has been declining over the past 30 years. Effective conservation actions require the delineation of conservation units to appropriately reflect the spatial scale of intraspecific variation and local adaptation. Towards this goal, we used the most comprehensive genetic and genomic database for Atlantic salmon to date, covering the entire North American range of the species. The database included microsatellite data from 9142 individuals from 149 sampling locations and data from a medium‐density SNP array providing genotypes for >3000 SNPs for 50 sampling locations. We used neutral and putatively selected loci to integrate adaptive information in the definition of conservation units. Bayesian clustering with the microsatellite data set and with neutral SNPs identified regional groupings largely consistent with previously published regional assessments. The use of outlier SNPs did not result in major differences in the regional groupings, suggesting that neutral markers can reflect the geographic scale of local adaptation despite not being under selection. We also performed assignment tests to compare power obtained from microsatellites, neutral SNPs and outlier SNPs. Using SNP data substantially improved power compared to microsatellites, and an assignment success of 97% to the population of origin and of 100% to the region of origin was achieved when all SNP loci were used. Using outlier SNPs only resulted in minor improvements to assignment success to the population of origin but improved regional assignment. We discuss the implications of these new genetic resources for the conservation and management of Atlantic salmon in North America.

Transcriptional responses to environmental metal exposure in wild yellow perch (Perca flavescens) collected in lakes with differing environmental metal concentrations (Cd, Cu, Ni)

To investigate the mechanisms involved in metal stress in wild fish, yellow perch (Perca flavescens) were collected in eight lakes of the Rouyn-Noranda and Sudbury regions (Canada). Due to mining and smelting activities, these two regions indeed present a broad contamination gradient in metal concentrations (Cd, Cu, Zn and Ni; water, sediment and prey) and offer a unique research opportunity to investigate relationships between metal bioaccumulation and resulting deleterious effects in indigenous biota chronically exposed to metal mixtures. The expression level of genes encoding for proteins involved in metal detoxification (metallothioneins, mts), protein protection (heat shock protein-70, hsp-70), growth (insulin-like growth factor-1, igf-1), aerobic energy metabolism (cytochrome c oxydase, cco-1) and protection against oxidative stress (Cu/Zn superoxide dismutase, sod-1) were assessed in fish liver and muscle in association with protein and enzymatic assays for cytochrome c oxidase (CCO). Bioaccumulation of both Cd and Cu increased in response to higher ambient metal concentrations, but the two metals clearly have different modes of action. For Cd, changes in gene expression levels were more marked in the liver than in the dorsal muscle, whereas for Cu the opposite trend was observed. Hepatic Cd accumulation was linked to decreased cco-1 and sod-1 gene expression, whereas Cu accumulation was associated with a decrease in CCO enzymatic activity and an increase in total protein concentration and in cco-1, mts and hsp-70 gene expression levels. For Ni, no significant correlations were observed at the transcriptional level, but increasing hepatic Ni concentrations were significantly and positively correlated with protein concentrations and CCO activity. By coupling gene expression to biochemical and physiological endpoints, this work provides new insights into the mechanisms involved in metal stress and the adaptive response of fish chronically exposed to metal mixtures.

Parallel and nonparallel genome-wide divergence among replicate population pairs of freshwater and anadromous Atlantic salmon

Little is known about the genetic basis differentiating resident and anadromous forms found in many salmonid species. Using a medium‐density SNP array, we documented genomic diversity and divergence at 2336 genetically mapped loci among three pairs of North American anadromous and freshwater Atlantic salmon populations. Our results show that across the genome, freshwater populations have lower diversity and a smaller proportion of private polymorphism relative to anadromous populations. Moreover, differentiation was more pronounced among freshwater than among anadromous populations at multiple spatial scales, suggesting a large effect of genetic drift in these isolated freshwater populations. Using nonhierarchical and hierarchical genome scans, we identified hundreds of markers spread across the genome that are potentially under divergent selection between anadromous and freshwater populations, but few outlier loci were repeatedly found in all three freshwater–anadromous comparisons. Similarly, a sliding window analysis revealed numerous regions of high divergence that were nonparallel among the three comparisons. These last results show little evidence for the parallel evolution of alleles selected for in freshwater populations, but suggest nonparallel adaptive divergence at many loci of small effects distributed through the genome. Overall, this study emphasizes the important role of genetic drift in driving genome‐wide reduction in diversity and divergence in freshwater Atlantic salmon populations and suggests a complex multigenic basis of adaptation to resident and anadromous strategies with little parallelism.

Transatlantic secondary contact in Atlantic Salmon, comparing microsatellites, a single nucleotide polymorphism array and restriction‐site associated DNA sequencing for the resolution of complex spatial structure

Identification of discrete and unique assemblages of individuals or populations is central to the management of exploited species. Advances in population genomics provide new opportunities for re‐evaluating existing conservation units but comparisons among approaches remain rare. We compare the utility of RAD‐seq, a single nucleotide polymorphism (SNP) array and a microsatellite panel to resolve spatial structuring under a scenario of possible trans‐Atlantic secondary contact in a threatened Atlantic Salmon, Salmo salar, population in southern Newfoundland. Bayesian clustering indentified two large groups subdividing the existing conservation unit and multivariate analyses indicated significant similarity in spatial structuring among the three data sets. mtDNA alleles diagnostic for European ancestry displayed increased frequency in southeastern Newfoundland and were correlated with spatial structure in all marker types. Evidence consistent with introgression among these two groups was present in both SNP data sets but not the microsatellite data. Asymmetry in the degree of introgression was also apparent in SNP data sets with evidence of gene flow towards the east or European type. This work highlights the utility of RAD‐seq based approaches for the resolution of complex spatial patterns, resolves a region of trans‐Atlantic secondary contact in Atlantic Salmon in Newfoundland and demonstrates the utility of multiple marker comparisons in identifying dynamics of introgression.

Interplay between ecological, behavioural and historical factors in shaping the genetic structure of sympatric walleye populations (Sander vitreus).

Disentangling ecological, behavioural and evolutionary factors responsible for the presence of stable population structure within wild populations has long been challenging to population geneticists. This study primarily aimed at decoding population structure of wild walleye (Sander vitreus) populations of Mistassini Lake (Québec, Canada) in order to define source populations to be used for the study of spatial partitioning using individual‐based multilocus assignment methods, and decipher the dynamics of individual dispersal and resulting patterns of spatial resource partitioning and connectivity among populations. A second objective was to elucidate the relationships between biological characteristics (sex, size, age and population of origin) and an individuals probability to migrate and/or disperse. To do so, a total of 780 spawning individuals caught on five distinct spawning sites, and 1165 postspawning individuals, captured over two sampling seasons (2002–2003) were analysed by means of eight microsatellite loci. Four temporally stable walleye populations associated with distinct reproductive grounds were detected. These populations were differentially distributed among lake sectors during their feeding migration and their spatial distribution was stable over the two sampling seasons. Dispersing individuals were identified (n = 61); these revealed asymmetrical patterns of dispersal between populations, which was also confirmed by divergent admixture proportions. Regression models underlined population of origin as the only factor explaining differential dispersal of individuals among populations. An analysis of covariance (ancova) indicated that larger individuals tended to migrate from their river of origin further away in the lake relative to smaller fish. In summary, this study underlined the relevance of using individual‐based assignment methods for deciphering dynamics of connectivity among wild populations, especially regarding behavioural mechanisms such as differential spatial partitioning and dispersal responsible for the maintenance of genetic population structure.

Range-wide parallel climate-associated genomic clines in Atlantic salmon

Clinal variation across replicated environmental gradients can reveal evidence of local adaptation, providing insight into the demographic and evolutionary processes that shape intraspecific diversity. Using 1773 genome-wide single nucleotide polymorphisms we evaluated latitudinal variation in allele frequency for 134 populations of North American and European Atlantic salmon (Salmo salar). We detected 84 (4.74%) and 195 (11%) loci showing clinal patterns in North America and Europe, respectively, with 12 clinal loci in common between continents. Clinal single nucleotide polymorphisms were evenly distributed across the salmon genome and logistic regression revealed significant associations with latitude and seasonal temperatures, particularly average spring temperature in both continents. Loci displaying parallel clines were associated with several metabolic and immune functions, suggesting a potential basis for climate-associated adaptive differentiation. These climate-based clines collectively suggest evidence of large-scale environmental associated differences on either side of the North Atlantic. Our results support patterns of parallel evolution on both sides of the North Atlantic, with evidence of both similar and divergent underlying genetic architecture. The identification of climate-associated genomic clines illuminates the role of selection and demographic processes on intraspecific diversity in this species and provides a context in which to evaluate the impacts of climate change.