Body length changes for Atlantic salmon (Salmo salar) over five decades exhibit weak spatial synchrony over a broad latitudinal gradient.

Understanding the factors that drive spatial synchrony among populations or species is important for management and recovery of populations. The range-wide declines in Atlantic salmon (Salmo salar) populations may be the result of broad-scale changes in the marine environment. Salmon undergo rapid growth in the ocean; therefore changing marine conditions may affect body size and fecundity estimates used to evaluate whether stock reference points are met. Using a dataset that spanned five decades, 172,268 individuals, and 19 rivers throughout Eastern Canada, we investigated the occurrence of spatial synchrony in changes in the body size of returning wild adult Atlantic salmon. Body size was then related to conditions in the marine environment (i.e., climate indices, thermal habitat availability, food availability, density-dependence, and fisheries exploitation rates) that may act on all populations during the ocean feeding phase of their life cycle. Body size increased during the 1980s and 1990s for salmon that returned to rivers after one (1SW) or two winters at sea (2SW); however, significant changes were only observed for 1SW and/or 2SW in some mid-latitude and northern rivers (10/13 rivers with 10 of more years of data during these decades) and not in southern rivers (0/2), suggesting weak spatial synchrony across Eastern Canada. For 1SW salmon in nine rivers, body size was longer when fisheries exploitation rates were lower. For 2SW salmon, body size was longer when suitable thermal habitat was more abundant (significant for 3/8 rivers) and the Atlantic Multidecadal Oscillation was higher (i.e., warmer sea surface temperatures; significant for 4/8 rivers). Overall, the weak spatial synchrony and variable effects of covariates on body size across rivers suggest that changes in Atlantic salmon body size may not be solely driven by shared conditions in the marine environment. Regardless, body size changes may have consequences for population management and recovery through the relationship between size and fecundity.

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.

Population genomics, life-history tactics, and mixed-stock subsistence fisheries in the northernmost American Atlantic salmon populations.

While Atlantic salmon (Salmo salar) of the northernmost American populations is alimentary, economically, and culturally important for Ungava Inuit communities (Nunavik, Canada) and might play a key role in the persistence of the species in a global warming context, many mysteries remain about those remote and atypical populations. Thus, our first aim was to document the genomic structure of the Nunavik populations. The second objective was to determine whether salmon only migrating to the estuary without reaching the sea, apparently unique to those populations, represent distinct populations from the typical anadromous salmons and subsequently explore the genetic basis of migratory life-history tactics in the species. Finally, the third goal was to quantify the contribution of each genetically distinct population and life-history tactic in the mixed-stock subsistence fishery of the Koksoak R. estuary. We used Genotyping-by-Sequencing to genotype 14,061 single nucleotide polymorphisms in the genome of 248 individuals from 8 source populations and 280 individuals from the Koksoak estuary mixed-stock fishery. Life-history tactics were identified by a visual assessment of scales. Results show a hierarchical structure mainly influenced by isolation-by-distance with 7 populations out of the 8 studied rivers. While no obvious structure was detected between marine and estuarine salmon within the population, we have identified genomic regions putatively associated with those migration tactics. Finally, all salmon captured in the Koksoak estuary originated from the Koksoak drainage and mostly from 2 tributaries, but no inter-annual variation in the contribution of these tributaries was found. Our results indicate, however, that both marine and estuarine salmon contribute substantially to estuarine fisheries and that there is inter-annual variation in this contribution. These findings provide crucial information for the conservation of salmon populations in a rapidly changing ecosystem, as well as for fishery management to improve the food security of Inuit communities.

Captive rearing effects on the methylome of Atlantic salmon after oceanic migration: Sex-specificity and intergenerational stability.

Captive rearing in salmon hatcheries can have considerable impacts on both fish phenotype and fitness within a single generation, even in the absence of genetic change. Evidence for hatchery-induced changes in DNA methylation is becoming abundant, though questions remain on the sex-specificity of these effects, their persistence until spawning and potential for transmission to future generations. Here we performed whole genome methylation sequencing of fin tissue for 16 hatchery and 16 wild Atlantic salmon (Salmo salar) returning to spawn in the Rimouski River, Québec, Canada. We identified two cohorts of hatchery-reared salmon through methylation analysis, one of which was epigenetically similar to wild fish, suggesting that supplementation efforts may be able to minimize the epigenetic effects of hatchery rearing. We found considerable sex-specific effects of hatchery rearing, with few genomic regions being affected in both males and females. We also analysed the methylome of 32 F1 offspring from four groups (pure wild, pure hatchery origin and reciprocal hybrids). We found that few epigenetic changes due to parental hatchery rearing persisted in the F1 offspring though the patterns of inheritance appear to be complex, involving nonadditive effects. Our results suggest that the epigenetic effects of hatchery rearing can be minimal in F0 . There may also be minimal epigenetic inheritance and rapid loss of epigenetic changes associated with hatchery rearing. However, due to sex-specificity and nonadditive patterns of inheritance, methylation changes due to captive rearing are rather complex and the field would benefit from further research on minimizing the epigenetic effects of captive rearing in conservation efforts.

Effects of stocking at the parr stage on the reproductive fitness and genetic diversity of a wild population of Atlantic salmon (Salmo salar L.).

Captive-breeding programs are among the most adopted conservation practices to mitigate the loss of biodiversity, including genetic diversity. However, both genetic and nongenetic changes occurring in captivity can reduce the fitness of supplemented individuals, which complicate rehabilitation efforts. In the case of Atlantic salmon, the intensity of changes that occur in captivity and their impact on fitness will vary with the stocking practice adopted. In this study, we test whether salmon stocked at the parr stage have reduced reproductive success compared with their wild conspecifics and whether they contribute to increase genetic diversity in the targeted population. To do so, we use high-throughput microsatellite sequencing of 38 loci to accurately assign 2381 offspring to a comprehensive set of possible parents from a supplemented Atlantic salmon population in Québec, Canada. Captive-bred salmon stocked at the parr stage had fewer mates than their wild conspecifics, as well as a reduced relative reproductive success (RSS) compared with their wild counterparts. Nonetheless, in comparison with previous studies, stocking at the parr stage significantly improved RSS compared with salmon stocked as smolts and they displayed a reduction in reproductive success similar to salmon stocked as fry, which spend less time in captivity than parr. Moreover, supplementation of captive-bred salmon significantly contributed to increasing genetic diversity. These results should contribute to informing resource managers in determining the best stocking practice to enhance Atlantic salmon populations.

Past, present and future contributions of evolutionary biology to wildlife forensics, management and conservation.

Successfully implementing fundamental concepts into concrete applications is challenging in any given field. It requires communication, collaboration and shared will between researchers and practitioners. We argue that evolutionary biology, through research work linked to conservation, management and forensics, had a significant impact on wildlife agencies and department practices, where new frameworks and applications have been implemented over the last decades. The Quebec government's Wildlife Department (MFFP: Ministère des Forêts, de la Faune et des Parcs) has been proactive in reducing the "research-implementation" gap, thanks to prolific collaborations with many academic researchers. Among these associations, our department's outstanding partnership with Dr. Louis Bernatchez yielded significant contributions to harvest management, stocking programmes, definition of conservation units, recovery of threatened species, management of invasive species and forensic applications. We discuss key evolutionary biology concepts and resulting concrete examples of their successful implementation that derives directly or indirectly from this successful partnership. While old and new threats to wildlife are bringing new challenges, we expect recent developments in eDNA and genomics to provide innovative solutions as long as the research-implementation bridge remains open.

Metabolic rate and climatic fluctuations shape continental wide pattern of genetic divergence and biodiversity in fishes.

Taxonomically exhaustive and continent wide patterns of genetic divergence within and between species have rarely been described and the underlying evolutionary causes shaping biodiversity distribution remain contentious. Here, we show that geographic patterns of intraspecific and interspecific genetic divergence among nearly all of the North American freshwater fish species (>750 species) support a dual role involving both the late Pliocene-Pleistocene climatic fluctuations and metabolic rate in determining latitudinal gradients of genetic divergence and very likely influencing speciation rates. Results indicate that the recurrent glacial cycles caused global reduction in intraspecific diversity, interspecific genetic divergence, and species richness at higher latitudes. At the opposite, longer geographic isolation, higher metabolic rate increasing substitution rate and possibly the rapid accumulation of genetic incompatibilities, led to an increasing biodiversity towards lower latitudes. This indicates that both intrinsic and extrinsic factors similarly affect micro and macro evolutionary processes shaping global patterns of biodiversity distribution. These results also indicate that factors favouring allopatric speciation are the main drivers underlying the diversification of North American freshwater fishes.

Glacial cycles as an allopatric speciation pump in north-eastern American freshwater fishes.

Allopatric speciation may be the principal mechanism generating new species. Yet, it remains difficult to judge the generality of this process because few studies have provided evidence that geographic isolation has triggered the development of reproductive isolation over multiple species of a regional fauna. Here, we first combine results from new empirical data sets (7 taxa) and published literature (9 taxa) to show that the eastern Great Lakes drainage represents a multispecies suture zone for glacial lineages of freshwater fishes with variable levels of genetic divergence. Second, we performed amplified fragment length polymorphism analyses among four pairs of lineages. Results indicate that lineages with relatively deep levels of mtDNA 5' COI (barcode) sequence divergence (>2%) developed strong reproductive barriers, while lineages with lower levels of divergence show weaker reproductive isolation when found in sympatry. This suggests that a threshold of 2% sequence divergence at mtDNA could be used as a first step to flag cryptic species in North American freshwater fishes. By describing different levels of divergence and reproductive isolation in different co-occurring fishes, we offer strong evidence that allopatric speciation has contributed significantly to the diversification of north-eastern American freshwater fishes and confirm that Pleistocene glacial cycles can be viewed as a 'speciation pump' that played a predominant role in generating biodiversity.

Genetic calibration of species diversity among North America's freshwater fishes.

Freshwater ecosystems are being heavily exploited and degraded by human activities all over the world, including in North America, where fishes and fisheries are strongly affected. Despite centuries of taxonomic inquiry, problems inherent to species identification continue to hamper the conservation of North American freshwater fishes. Indeed, nearly 10% of species diversity is thought to remain undescribed. To provide an independent calibration of taxonomic uncertainty and to establish a more accessible molecular identification key for its application, we generated a standard reference library of mtDNA sequences (DNA barcodes) derived from expert-identified museum specimens for 752 North American freshwater fish species. This study demonstrates that 90% of known species can be delineated using barcodes. Moreover, it reveals numerous genetic discontinuities indicative of independently evolving lineages within described species, which points to the presence of morphologically cryptic diversity. From the 752 species analyzed, our survey flagged 138 named species that represent as many as 347 candidate species, which suggests a 28% increase in species diversity. In contrast, several species of parasitic and nonparasitic lampreys lack such discontinuity and may represent alternative life history strategies within single species. Therefore, it appears that the current North American freshwater fish taxonomy at the species level significantly conceals diversity in some groups, although artificially creating diversity in others. In addition to providing an easily accessible digital identification system, this study identifies 151 fish species for which taxonomic revision is required.

Identifying Canadian freshwater fishes through DNA barcodes.

BACKGROUND: DNA barcoding aims to provide an efficient method for species-level identifications using an array of species specific molecular tags derived from the 5' region of the mitochondrial cytochrome c oxidase I (COI) gene. The efficiency of the method hinges on the degree of sequence divergence among species and species-level identifications are relatively straightforward when the average genetic distance among individuals within a species does not exceed the average genetic distance between sister species. Fishes constitute a highly diverse group of vertebrates that exhibit deep phenotypic changes during development. In this context, the identification of fish species is challenging and DNA barcoding provide new perspectives in ecology and systematics of fishes. Here we examined the degree to which DNA barcoding discriminate freshwater fish species from the well-known Canadian fauna, which currently encompasses nearly 200 species, some which are of high economic value like salmons and sturgeons. METHODOLOGY/PRINCIPAL FINDINGS: We bi-directionally sequenced the standard 652 bp "barcode" region of COI for 1360 individuals belonging to 190 of the 203 Canadian freshwater fish species (95%). Most species were represented by multiple individuals (7.6 on average), the majority of which were retained as voucher specimens. The average genetic distance was 27 fold higher between species than within species, as K2P distance estimates averaged 8.3% among congeners and only 0.3% among concpecifics. However, shared polymorphism between sister-species was detected in 15 species (8% of the cases). The distribution of K2P distance between individuals and species overlapped and identifications were only possible to species group using DNA barcodes in these cases. Conversely, deep hidden genetic divergence was revealed within two species, suggesting the presence of cryptic species. CONCLUSIONS/SIGNIFICANCE: The present study evidenced that freshwater fish species can be efficiently identified through the use of DNA barcoding, especially the species complex of small-sized species, and that the present COI library can be used for subsequent applications in ecology and systematics.