Atlantic Salmon (Salmo salar) populations are at historic lows, primarily due to poor marine survival, and knowledge gaps regarding their migration limit our ability to identify population-specific stressors. From 2021 to 2023, 3900 smolts were tagged and tracked from 32 rivers across eastern Canada to the Labrador Sea. Migration routes were generally uniform within most populations, but distinct secondary routes in others suggest adaptive flexibility and shared environmental cues across a broad spatial scale. Despite a strong latitudinal gradient in the initial timing of migration, with southern populations leaving earlier, temporal overlap increased at northern marine locations. This convergence coincided with the seasonal warming of shelf waters above 4 degrees C and a narrow 4-10 degrees C thermal niche. This overview of early post-smolt migration highlights the journey's active nature, the significance of estuarine stopover sites, and thermal limitations dictating the arrival in the Labrador Sea. Protecting this culturally and economically significant species will require population-specific management that accounts for cumulative stressors along these routes.
ABSTRACT Supportive breeding programs are widely implemented to counteract demographic collapse in threatened populations. Their long‐term success, however, depends on maintaining genetic diversity while ensuring that released individuals contribute effectively to wild populations. In Atlantic salmon ( Salmo salar ), uncertainties remain regarding the capacity of captive broodstocks to preserve genetic variation and the demographic and genetic consequences of supplementation. Here, we evaluate the outcomes of a decade‐long restoration program targeting two genetically differentiated but geographically proximate Atlantic salmon populations in the Romaine watershed (Romaine and Puyjalon population, Québec, Canada). Using microsatellite data, we performed population assignment, parentage analyses, and temporal estimates of effective number of breeders and genetic diversity. We assessed broodstock performance, the contribution of stocked individuals to wild populations, and the impact of two egg incubation treatments on fry to smolt survival. Despite sustained efforts to maintain large and representative broodstocks, the failure of wild‐caught juvenile salmon to reach maturity substantially reduced the number of breeders, representing the greatest loss of genetic potential in the hatchery broodstock. Nevertheless, partial factorial mating and kinship‐based management allowed us to avoid inbreeding and preserved levels of heterozygosity and allelic richness comparable to those observed in wild populations. Stocked individuals contributed around 25% to juvenile population size in both populations, without reducing effective population size or eroding genetic differentiation. Estimates of total effective population size consistently exceeded those of wild components alone, indicating no evidence of a Ryman–Laikre effect. Finally, egg incubation in the water of the Romaine River increased survival to smolt stage for genetically Romaine individuals but not for individuals from Puyjalon, suggesting local adaptation to early rearing conditions. These results demonstrate that, when carefully designed and genetically monitored, supportive breeding can reinforce depleted salmon populations without compromising genetic diversity and integrity.
Captive rearing is a common practice for the stocking, conservation, and supplementation of fish species worldwide, but captive-reared fish can exhibit altered phenotypes leading to reduced fitness in nature compared to wild conspecifics. In salmonids, certain studies have found limited genetic differentiation between wild and captive-reared fish. However, documented changes in gene expression in hatchery fish have led scientists to investigate epigenetic mechanisms, such as DNA methylation, as a source of these differences. In this binational collaborative piece, we synthesize the knowledge and efforts of academics and government scientists to highlight how interactions between captive rearing and the epigenome elicit parallel phenotypic changes across salmonid species. We examine the known and potential links between DNA methylation and the phenotypic effects of captive rearing including changes in behavior, color, gut microbiomes, and developmental abnormalities. We review efforts to minimize these phenotypic and epigenetic effects including attempts to modify the hatchery environment and rearing protocols. We provide a framework to integrate epigenetic considerations into hatchery rearing protocols by weighing the heritable nature of DNA methylation with the goals of different captive rearing programs and explore whether minimizing the phenotypic and epigenetic effects of captive rearing is worthwhile. We examine heritability and persistence of epigenetic effects, and we propose the exploitation of heritable bet-hedging as an epigenetic buffer to increase post-release survival. We also suggest novel applications of epigenomic biomarkers as a non-lethal method for post-release monitoring. Ultimately, collaborative multi-disciplinary research across species is needed to understand the comprehensive effects of captive rearing, reduce the ecological impacts of captive fish in the wild, and increase population resilience. Integrating epigenetics into fish hatchery management will provide new opportunities for optimizing and improving captive rearing.
Atlantic Salmon (Salmo salar) are typically anadromous; however, some individuals complete their life cycle in freshwater. A widely documented scenario suggests that this resident tactic arose independently in each river via isolation from anadromous Atlantic Salmon populations after the last ice age. Yet, origin of residency remains poorly studied in the North Shore region of the Gulf of St. Lawrence (Canada). To address this, we genotyped 189 resident and 196 anadromous individuals from five watersheds at 43 microsatellite markers. We found marked genetic differences between tactics within rivers, likely resulting from different levels of gene flow associated with geographic isolation, suggesting that residents may not have always been isolated as expected. Moreover, exploratory demographic inference analyses suggest that residents may have a common ancestral source, which does not support the strict independent development model typically expected. This pattern is rather more consistent with a two-wave colonization events and/or ancestral intracontinental gene flow. These findings bring nuances and complexity to views on the origin of residency in Atlantic Salmon, and are valuable for guiding conservation practices.
While body size is the primary driver of fecundity, other factors may contribute to variation in these relationships. Anadromous populations of Atlantic salmon (Salmo salar) have diverse life histories, and fisheries management relies on accurate fecundity estimates. We used Bayesian hierarchical models to determine the relationship between fecundity and fork length, and other life-history characteristics, for 25 spawning populations throughout Eastern Canada. Fecundity was best modeled at the river level, increased with body size and condition, and decreased with mean egg diameter. Fecundity was higher for individuals that spent fewer years in freshwater as juveniles, and for consecutive repeat spawners compared with first-time (or maiden) spawners that spent 1 year in the ocean. Lastly, there was interannual variability in the fecundity-body size relationship. These relationships should be used in conjunction with data on recent changes in body size and/or life-history traits of populations to inform stock management.
Change in the mean size of individuals within populations or species is a common response to shifts in maturation schedules, size-selective mortality, and/or size of individuals at different ages. This can be indicative of a decreased resilience to environmental variation, particularly when body size changes co-occur with changes in the population age structure or life-history diversity. For species where age and life history of mature adults are linked with size, declines in mean body size may reflect a simplification in age structure or loss of life-history diversity. We examined temporal and spatial patterns in body size, age, and diversity of anadromous of Atlantic salmon (Salmo salar). Our dataset included 12 wild and two hatchery populations (hereafter river/origin groups) spanning most of the extant range of Atlantic salmon in North America over five decades (1969-2018). Of these 14 river/origin groups, six (five wild and one hatchery) exhibited temporal changes in mean fork length that co-occurred with changes in age and/or diversity of life histories. There was river-specific variability in the trends but overall, changes in mean fork length for anadromous salmon returns were closely associated with similar directional changes in age structure and life-history strategies. For example, three river/origin groups had increases in fork length, age, and diversity associated with an increase in repeat spawner abundance during part of the timeseries. However, three river/origin groups of highest conservation concern had declines in fork length, age, and/or diversity associated with earlier maturation and a decline in repeat spawner abundance. Reductions in body size with fewer age classes and life-history strategies may affect the resilience and recovery of at-risk populations through the reduced brood-year overlap among returns and lower fecundity.
Salmon populations exhibit a variety of migratory behaviours, generally residing in fresh water or migrating to the sea. It is important for the management and conservation of salmon populations that migratory behaviour is well understood, particularly in the context of climate change and exploitation. Scalimetry of Atlantic salmon (Salmo salar) at the northern edge of its North American range has revealed unusual migratory patterns. In the Ungava Bay region, some salmon described as estuary-growth spend summers in estuaries and winters in fresh water, whereas others from the same river exhibit typical marine anadromy or fresh-water residency. This study aimed to confirm and estimate the occurrence of estuary-growth Atlantic salmon using scalimetry and otolith chemistry. We compared scalimetry and otolith chemical transects of 86 salmon, 21 collected from the Koksoak River hydrographic network in Nunavik and 65 salmons from 12 hydrographic networks in southern Quebec. Otolith concentrations of Zn, Mg, Sr, and Ba detected the age and migrations of individual Atlantic salmon throughout their lifetime. The life history inferred by both methods matched very well (98.8% matching), confirming the effectiveness and reliability of scalimetry. This information strengthens the relevance of using this non-lethal and accessible method to monitor this iconic species. Additionally, our study confirmed the occurrence of salmon making estuarine migrations in the Ungava Bay region. This atypical migratory behaviour accounted for 22% and 74% of the Atlantic salmon sampled in the aux Mélèzes River in 2018 and the du Gué River in 2019, respectively.
Effective monitoring strategies are key for aquatic species conservation, but traditional methods often require significant resources, especially in large aquatic systems. The emergence of quantitative environmental DNA (eDNA) is a promising alternative. Yet, few studies have evaluated the possibility of quantifying Atlantic salmon abundance with eDNA when individuals are at low abundance and occur in large river systems. In this study, we tested the efficacy of eDNA to monitor and quantify daily variation in smolt counts during their downstream migration in a large river system with low abundance of smolts. During the 2021 and 2022 downstream migrations, trap nets were used to conduct a daily census of smolts in the Romaine and Puyjalon rivers (Qu & eacute;bec, Canada) while eDNA samples were collected daily over a transect perpendicular to the riverbank. Using quantitative real-time qPCR, we showed that discharge-corrected eDNA concentrations were positively correlated with daily smolt counts for both years. In addition, we found that controlling for temperature and precipitation improved model transferability between years, showing the importance of considering environmental correlates when using eDNA for abundance quantification. Finally, smolt counts were correlated with eDNA concentrations on the same day, but not with eDNA concentrations 1 or 2 days prior, highlighting the capacity of the model to track daily fluctuations in smolt abundance. Our results underscore the potential of using eDNA to monitor Atlantic salmon in large river systems with low smolt abundance when the river hydrology and environmental conditions are documented.
Resolving the migratory behaviour and population dynamics of Atlantic salmon (Salmo salar Linnaeus, 1758) in the Nastapoka River, a unique northern population located along the eastern shore of Hudson Bay (Quebec), is critical for population conservation. This study used otolith chemistry to elucidate the migration patterns and natal origins of salmon captured in this isolated system. The Nastapoka River has a 35 m waterfall that separates upstream landlocked salmon from downstream specimens whose migratory behavior remains unresolved. We identified two migratory groups; one exhibited short movements to brackish or marine environments, and the second group exhibited strictly freshwater residence. Migratory individuals had increased growth and Fulton condition compared to resident specimens. Our analyses also revealed two groups related to natal origin: upstream and downstream of the waterfall. Certain specimens captured downstream exhibited signatures indicative of upstream origin, suggesting potential population connectivity via occasional downstream drifting. This study highlights the coexistence of partial migration strategies within this population driven by environmental constraints and resource optimization. It also suggests that the population structure in Nastapoka River is still unresolved and requires more extensive studies to optimize its conservation, aiming at preserving this unusual unit of Atlantic salmon species in Northern Canada.
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.
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.
AbstractComplex 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.
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.
Catch- and-release fishing is a common conservation practice in recreational fisheries for Atlantic Salmon, although the effects on the reproductive success of caught- and-released fish are poorly understood. Herein, we compared the relative reproductive success of caught- and-released to non-caught salmon and tested the effect of temperature at release on reproductive success in the Rimouski River, Québec, Canada. At least 83% of caught- and-released salmon that moved upstream of a dam successfully reproduced, including fish that have been released in water above 20°C. However, the reproductive success of caught- and-released female salmon was only 73% of the reproductive success of non-caught salmon. Moreover, the increasing temperature did not affect the reproductive success of released fish that entered a trap, but fish caught at warmer temperatures were less likely to enter the trap. Our findings should be useful for evaluating the risks and benefits of catch- and-release, and for optimising conservation practices used for the preservation of Atlantic salmon populations.
Abstract 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.
Environmental DNA (eDNA) is a very promising approach to facilitate and improve the aquatic species monitoring, which is crucial for their management and conservation. In comparison with the plethora of monitoring studies in the fields, relatively few studies have focused on experimentally investigating the “ecology” of eDNA, in particular pertaining to processes influencing the detection of eDNA. The paucity of knowledge about its ecology hampers the use of eDNA analysis to its full potential. In this study, we experimentally evaluated the impact of several biotic and abiotic factors on the rate of production and degradation of eDNA. Individuals of three freshwater fish species (brown bullhead, tench, and yellow perch) with distinct ecology were placed in two types of water from the St. Lawrence River (Québec, Canada) with very distinct physicochemical characteristics and at three different temperatures. Water samples were then filtered at predetermined time intervals, and quantitative PCR was used to quantify the eDNA in each sample. We found that temperature, species, water types, and some interactions between these factors had a strong effect on the production and degradation of eDNA. The results of this study enhance our knowledge about the ecology of eDNA, thus improving eDNA data interpretation.
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 SNP array and low coverage whole genome re-sequencing 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 large-effect loci ( vgll3, six6) previously identified in European populations, indicating genetic parallelism, but found that this pattern varied based on both sex and geographic region. We also identified largely non-repeated sweep signatures and sets of highly predictive loci associated with sea age among populations and sexes within North America, indicating polygenicity and low rates of repeated 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. 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.
Captive-breeding programs as well as and catch-and-release are among the most commonly adopted conservation practices in recreational fisheries. However, risks and benefits associated with their implementation are rarely evaluated. In the case of Atlantic Salmon, while previous studies revealed that captive-bred fish show reduced fitness compared to their wild counterparts in nature. Yet, few examined the extent and causes of their reduced reproductive success or directly compared their contribution to enhance genetic diversity to that of wild fish, including mature male parr. Furthermore, only one study specifically measured the reproductive success of caught and released Atlantic salmon in natural settings, and no study to date evaluated if released salmon are able to reproduce when released at temperature above 20°C which is known to increase post-release mortality. Here, we use high-throughput microsatellite sequencing of 38 loci to accurately assign 2500 offspring to a comprehensive set of possible parents from a supplemented Atlantic salmon population in Québec, Canada. The resolved molecular pedigree provided informative insight on the reproductive pattern of both captive-bred salmon and caught-and-released salmon. Captive-bred salmon had fewer partners than their wild conspecifics which lead to a significant reduction of reproductive success relative to that of their wild counterparts. Supplementation of captive-bred salmon significantly contributed to increase genetic diversity but mature male parr did so to an even greater extent and significantly inflated the number of alleles found among offspring. Moreover, our results showed that that at least 83% of caught-and-released salmon did successfully reproduced although caught-and-released female salmon have a significantly reduced reproductive success, averaging 73% of the reproductive output of non-caught salmon. Reproductive success of released salmon was not influenced by water temperature over 20°C which suggests either that the studied population is locally adapted to warm waters or that they behaviorally regulated body temperature by accessing nearby thermal refugia. Our results should help refining managers’ ability to analyze the risks and benefits associated with captive-breeding and catch-and-release, and thus, optimize conservation practices used for the preservation of Atlantic salmon populations.