Eric Verspoor

A critical review of adaptive genetic variation in Atlantic salmon: implications for conservation

Here we critically review the scale and extent of adaptive genetic variation in Atlantic salmon (Salmo salar L.), an important model system in evolutionary and conservation biology that provides fundamental insights into population persistence, adaptive response and the effects of anthropogenic change. We consider the process of adaptation as the end product of natural selection, one that can best be viewed as the degree of matching between phenotype and environment. We recognise three potential sources of adaptive variation: heritable variation in phenotypic traits related to fitness, variation at the molecular level in genes influenced by selection, and variation in the way genes interact with the environment to produce phenotypes of varying plasticity. Of all phenotypic traits examined, variation in body size (or in correlated characters such as growth rates, age of seaward migration or age at sexual maturity) generally shows the highest heritability, as well as a strong effect on fitness. Thus, body size in Atlantic salmon tends to be positively correlated with freshwater and marine survival, as well as with fecundity, egg size, reproductive success, and offspring survival. By contrast, the fitness implications of variation in behavioural traits such as aggression, sheltering behaviour, or timing of migration are largely unkown. The adaptive significance of molecular variation in salmonids is also scant and largely circumstantial, despite extensive molecular screening on these species. Adaptive variation can result in local adaptations (LA) when, among other necessary conditions, populations live in patchy environments, exchange few or no migrants, and are subjected to differential selective pressures. Evidence for LA in Atlantic salmon is indirect and comes mostly from ecological correlates in fitness‐related traits, the failure of many translocations, the poor performance of domesticated stocks, results of a few common‐garden experiments (where different populations were raised in a common environment in an attempt to dissociate heritable from environmentally induced phenotypic variation), and the pattern of inherited resistance to some parasites and diseases. Genotype × environment interactions occurr for many fitness traits, suggesting that LA might be important. However, the scale and extent of adaptive variation remains poorly understood and probably varies, depending on habitat heterogeneity, environmental stability and the relative roles of selection and drift. As maladaptation often results from phenotype‐environment mismatch, we argue that acting as if populations are not locally adapted carries a much greater risk of mismanagement than acting under the assumption for local adaptations when there are none. As such, an evolutionary approach to salmon conservation is required, aimed at maintaining the conditions necessary for natural selection to operate most efficiently and unhindered. This may require minimising alterations to native genotypes and habitats to which populations have likely become adapted, but also allowing for population size to reach or extend beyond carrying capacity to encourage competition and other sources of natural mortality.

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.

Mitochondrial DNA variation in Pleistocene and modern Atlantic salmon from the Iberian glacial refugium

Current understanding of the postglacial colonization of Nearctic and Palearctic species relies heavily on inferences drawn from the phylogeographic analysis of contemporary generic variants. Modern postglacial populations are supposed to be representative of their Pleistocene ancestors, and their current distribution is assumed to reflect the different colonization success and dispersal patterns of refugial lineages. Yet, testing of phylogeographic models against ancestral genomes from glacial refugia has rarely been possible. Here we compare ND1 mitochondrial DNA variation in late Pleistocene (16 000–40 000 years before present), historical and contemporary Atlantic salmon (Salmo salar) populations from northern Spain and other regions of western Europe. Our study demonstrates the presence of Atlantic salmon in the Iberian glacial refugium during the last 40 000 years and points to the Iberian Peninsula as the likely source of the most common haplotype within the Atlantic lineage in Europe. However, our findings also suggest that there may have been significant changes in the genetic structure of the Iberian refugial stock since the last ice age, and question whether modern populations in refugial areas are representative of ice age populations. A common haplotype that persisted in the Iberian Peninsula during the Pleistocene last glacial maximum is now extremely rare or absent from European rivers, highlighting the need for caution when making phylogeographic inferences about the origin and distribution of modern genetic types.

Asymmetric gene flow and the evolutionary maintenance of genetic diversity in small, peripheral Atlantic salmon populations

Small populations may be expected to harbour less genetic variation than large populations, but the relation between census size (N), effective population size (Ne), and genetic diversity is not well understood. We compared microsatellite variation in four small peripheral Atlantic salmon populations from the Iberian peninsula and three larger populations from Scotland to test whether genetic diversity was related to population size. We also examined the historical decline of one Iberian population over a 50-year period using archival scales in order to test whether a marked reduction in abundance was accompanied by a decrease in genetic diversity. Estimates of effective population size (Ne) calculated by three temporal methods were consistently low in Iberian populations, ranging from 12 to 31 individuals per generation considering migration, and from 38 to 175 individuals per generation if they were regarded as closed populations. Corresponding Ne/N ratios varied from 0.02 to 0.04 assuming migration (mean=0.03) and from 0.04 to 0.18 (mean=0.10) assuming closed populations. Population bottlenecks, inferred from the excess of heterozygosity in relation to allelic diversity, were detected in all four Iberian populations, particularly in those year classes derived from a smaller number of returning adults. However, despite their small size and declining status, Iberian populations continue to display relatively high levels of heterozygosity and allelic richness, similar to those found in larger Scottish populations. Furthermore, in the R. Asón no evidence was found for a historical loss of genetic diversity despite a marked decline in abundance during the last five decades. Thus, our results point to two familiar paradigms in salmonid conservation: (1)␣endangered populations can maintain relatively high levels of genetic variation despite their small size, and (2) marked population declines may not necessarily result in a significant loss of genetic diversity. Although there are several explanations for such results, microsatellite data and physical tagging suggest that high levels of dispersal and asymmetric gene flow have probably helped to maintain genetic diversity in these peripheral populations, and thus to avoid the negative consequences of inbreeding.

Management of salmonid fisheries in the British Isles: towards a practical approach based on population genetics

The evidence for structuring of Atlantic salmon (Salmo salar) and brown trout (Salmo trutta) into distinct reproductive populations and for genetic differentiation and local adaptation is compelling. The effect of genetic variation among populations is demonstrably a factor determining the economic value of salmonid fisheries in the British Isles. Genetic considerations are, therefore, a matter of self-interest for fisheries managers and a shared interest with those advocating more general approaches to the conservation of diversity and variation. The local population is the basic unit of production and, therefore, the preferred unit of management. However, salmonid populations are numerous and many are small. These factors limit practical possibilities for management at the population level. We suggest that this difficulty can be addressed by combining populations in fisheries-biased management units that comprise interchangeable, nested groupings of populations that are both genetically and biologically meaningful. This population-based approach addresses the necessity of managing the fisheries in ways that are consistent with the conservation of adaptive potential in relation to the dynamic aspects of populations, their capacity to respond to changing environmental conditions, and the likelihood that salmonids will remain a worthwhile resource for the future.

Unravelling first-generation pedigrees in wild endangered salmon populations using molecular genetic markers

There is increasing interest in the use of molecular genetic data to infer genealogical relationships among individuals in the absence of parental information. Such analyses can provide insight into mating systems and estimations of heritability in the wild. In addition, accurate pedigree reconstruction among the founders of endangered populations being reared in captivity would be invaluable. Many breeding programs for endangered species attempt to minimize loss of genetic variation and inbreeding through strategies designed to minimize global co‐ancestry, but they assume a lack of relatedness among the founders. Yet populations that are the target of such programs are generally in serious demographic decline, and many of the available founders may be closely related. Here we demonstrate determination of full and half‐sib relationships among the wild founders of a captive breeding program involving two endangered Atlantic salmon populations using two different approaches and associated software, pedigree and colony. A large portion of the juveniles collected in these two rivers appear to be derived from surprisingly few females mating with a large number of males, probably small precocious parr. Another group of potential founders, obtained from a local hatchery, clearly originated from a small number of full‐sib crosses. These results allowed us to prioritize individuals on the basis of conservation value, and are expected to help minimize loss of genetic variation through time. In addition, insight is provided into the number of contributing parents and the mating systems that produced this last generation of endangered wild Atlantic salmon.

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.

Patterns of natural selection acting on the mitochondrial genome of a locally adapted fish species

BackgroundMitochondrial DNA (mtDNA) is frequently used in population genetic studies and is usually considered as a neutral marker. However, given the functional importance of the proteins encoded by the mitochondrial genome, and the prominent role of mitochondria in cellular energy production, the assumption of neutrality is increasingly being questioned.ResultsWe tested for evidence of selection on the mitochondrial genome of the Atlantic salmon, which is a locally adapted and widely farmed species and is distributed across a large latitudinal cline. We analysed 20 independent regions of the salmon mtDNA that represented nine genes (ND1, ND2, ND3, COX1, COX2, ATP6, ND4, ND5, and CYTB). These 20 mtDNA regions were sequenced using a 454 approach from samples collected across the entire European range of this species. We found evidence of positive selection at the ND1, ND3 and ND4 genes, which is supported by at least two different codon-based methods and also by differences in the chemical properties of the amino acids involved. The geographical distribution of some of the mutations indicated to be under selection was not random, and some mutations were private to artic populations. We discuss the possibility that selection acting on the Atlantic salmon mtDNA genome might be related to the need for increased metabolic efficiency at low temperatures.ConclusionsThe analysis of sequences representing nine mitochondrial genes that are involved in the OXPHOS pathway revealed signatures of positive selection in the mitochondrial genome of the Atlantic salmon. The properties of the amino acids involved suggest that some of the mutations that were identified to be under positive selection might have functional implications, possibly in relation to metabolic efficiency. Experimental evidence, and better understanding of regional phylogeographic structuring, are needed to clarify the potential role of selection acting on the mitochondrial genome of Atlantic salmon and other locally adapted fishes.

Accuracy of Assignment of Atlantic Salmon (Salmo salar L.) to Rivers and Regions in Scotland and Northeast England Based on Single Nucleotide Polymorphism (SNP) Markers.

Understanding the habitat use patterns of migratory fish, such as Atlantic salmon (Salmo salar L.), and the natural and anthropogenic impacts on them, is aided by the ability to identify individuals to their stock of origin. Presented here are the results of an analysis of informative single nucleotide polymorphic (SNP) markers for detecting genetic structuring in Atlantic salmon in Scotland and NE England and their ability to allow accurate genetic stock identification. 3,787 fish from 147 sites covering 27 rivers were screened at 5,568 SNP markers. In order to identify a cost-effective subset of SNPs, they were ranked according to their ability to differentiate between fish from different rivers. A panel of 288 SNPs was used to examine both individual assignments and mixed stock fisheries and eighteen assignment units were defined. The results improved greatly on previously available methods and, for the first time, fish caught in the marine environment can be confidently assigned to geographically coherent units within Scotland and NE England, including individual rivers. As such, this SNP panel has the potential to aid understanding of the various influences acting upon Atlantic salmon on their marine migrations, be they natural environmental variations and/or anthropogenic impacts, such as mixed stock fisheries and interactions with marine power generation installations.

Conservation of the vendace (Coregonus albula), the U.K.'s rarest freshwater fish

Although also formerly present in two lochs in South West Scotland, populations of vendace (Coregonus albula) were until recently believed to persist in only two U.K. lakes, i.e., Bassenthwaite Lake and Derwent Water in North West England. However, although Derwent Water has retained its natural mesotrophic conditions and the status of its vendace population is acceptable, monitoring at Bassenthwaite Lake has failed to record any specimens since 2000 and the species has recently been declared locally extinct. Bassenthwaite Lake has experienced increasing problems from eutrophication, sedimentation and the introduction of fi sh species including roach (Rutilus rutilus) and ruffe (Gymnocephalus cernuus), both of which have more recently also been introduced to Derwent Water and give concern over possible food competition and egg predation. In addition to monitoring, considerable efforts have been made in recent years to conserve vendace through the protection and improvement of their habitats and the establishment of refuge populations. The latter has resulted in the establishment of a population originating from Bassenthwaite Lake in Loch Skeen of South West Scotland, with further attempts still in progress at two other sites. Public awareness of the conservation of this species, which is the U.K.s rarest freshwater fish, has also been actively promoted.