Fine-scale genetic structure of Atlantic salmon ( Salmo salar ) using microsatellite markers: effects of restocking and natural recolonization (original) (raw)
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The restoration and maintenance of habitat connectivity are major challenges in conservation biology. These aims are especially critical for migratory species using corridors that can be obstructed by anthropogenic barriers. Here, we explored the origins and genetic diversity of Atlantic salmon (Salmo salar) recolonizing upstream areas of the largest South European Atlantic salmon population (Adour drainage, France) following restoration of connectivity and stocking. We genotyped 1,009 juvenile individuals, sampled either in continuously inhabited downstream sites or in recently reconnected and recolonized upstream locations, at 12 microsatellite loci. We found significant fine scale genetic structure, with three main genetic clusters corresponding to the Nive, Nivelle and Gaves rivers. Within each of these clusters, samples collected in continuously inhabited and recently recolonized sites had comparable allelic richness and effective population sizes and were only weakly differentiated. Genetic structure among basins was also similar among continuously inhabited and recently recolonized sites. The majority of the individuals sampled from recently recolonized sites were assigned to neighboring continuously inhabited downstream sites, but noticeable proportions of fish were assigned to samples collected in more distant sites or identified as putative hybrids. Overall, this study suggests that the restoration of accessibility to upstream areas can allow for the recolonization and effective reproduction of Atlantic salmon from proximate downstream refugia, which does not decrease local diversity or disrupt existing genetic structure.
Fishes
Atlantic salmon Salmo salar supports highly valuable commercial and recreational fisheries in Europe, but its stocks are currently overexploited and threatened by climate change. Its southernmost populations (in northern Spain) play a key role in conserving the species’ original genetic diversity, which is endangered due to decades-long (1970s to 1990s) massive stocking with non-native stocks. Their decline is well documented, but the effect of stock transfer and conservation efforts is unclear. Nine microsatellite loci were amplified from archival samples (scales from 1958–1959) from eight Spanish rivers to analyse the species’ natural genetic dynamics before its decline started. Allelic richness was high in the historical populations (the 1950s) and above most contemporary estimates. Private alleles were found in most rivers, indicating high local uniqueness and relative isolation among river basins. Some alleles are regional markers since they are rare or absent from contemporary...
Molecular Ecology, 2001
Atlantic salmon (n = 1682) from 27 anadromous river populations and two nonanadromous strains ranging from south-central Maine, USA to northern Spain were genotyped at 12 microsatellite DNA loci. This suite of moderate to highly polymorphic loci revealed 266 alleles (5 -37/locus) range-wide. Statistically significant allelic and genotypic heterogeneity was observed across loci between all but one pairwise comparison. Significant isolation by distance was found within and between North American and European populations, indicating reduced gene flow at all geographical scales examined. North American Atlantic salmon populations had fewer alleles, fewer unique alleles (though at a higher frequency) and a shallower phylogenetic structure than European Atlantic salmon populations. We believe these characteristics result from the differing glacial histories of the two continents, as the North American range of Atlantic salmon was glaciated more recently and more uniformly than the European range. Genotypic assignment tests based on maximum-likelihood provided 100% correct classification to continent of origin and averaged nearly 83% correct classification to province of origin across continents. This multilocus method, which may be enhanced with additional polymorphic loci, provides fishery managers the highest degree of correct assignment to management unit of any technique currently available.
Evolution, 2003
An understanding of the relative roles of historical and contemporary factors in structuring genetic variation is a fundamental, but understudied aspect of geographic variation. We examined geographic variation in microsatellite DNA allele frequencies in bull trout (Salvelinus confluentus, Salmonidae) to test hypotheses concerning the relative roles of postglacial dispersal (historical) and current landscape features (contemporary) in structuring genetic variability and population differentiation. Bull trout exhibit relatively low intrapopulation microsatellite variation (average of 1.9 alleles per locus, average H e ϭ 0.24), but high levels of interpopulation divergence (F ST ϭ 0.39). We found evidence of historical influences on microsatellite variation in the form of a decrease in the number of alleles and heterozygosities in populations on the periphery of the range relative to populations closer to putative glacial refugia. In addition, one region of British Columbia that was colonized later during deglaciation and by more indirect watershed connections showed less developed and more variable patterns of isolation by distance than a similar region colonized earlier and more directly from refugia. Current spatial and drainage interconnectedness among sites and the presence of migration barriers (falls and cascades) within individual streams were found to be important contemporary factors influencing historical patterns of genetic variability and interpopulation divergence. Our work illustrates the limited utility of equilibrium models to delineate population structure and patterns of genetic diversity in recently founded populations or those inhabiting highly heterogeneous environments, and it highlights the need for approaches incorporating a landscape context for population divergence. Substantial microsatellite DNA divergence among bull trout populations may also signal divergence in traits important to population persistence in specific environments.
Fisheries Management and Ecology, 2011
Population genetic studies can be useful for informing conservation and management. In Atlantic salmon, Salmo salar L., population structuring frequently occurs between river systems, but contrasting patterns occur within rivers, highlighting the need for catchment-specific studies to inform management. Here, population structure of Atlantic salmon was examined in the River Tamar, United Kingdom, using 12 microsatellite loci. Gene diversity and allelic richness ranged from 0.80 to 0.84 and from 8.96 to 10.24, respectively. Some evidence of genetic structure was found, including significant genetic differentiation between samples in different subcatchments (pairwise h and tests of genic differentiation), results from assignment tests and a pattern of isolation by distance. Conversely, STRUCTURE revealed only one population cluster, and an analysis of molecular variance showed no significant variation between subcatchments. Evidence of population bottlenecks depended on the mutation model assumed and is discussed with reference to catchment-specific studies of stock abundance. Implications for implementing management actions are considered.
Ecology and evolution, 2013
While the stocking of captive-bred fish has been occurring for decades and has had substantial immediate genetic and evolutionary impacts on wild populations, its long-term consequences have only been weakly investigated. Here, we conducted a spatiotemporal analysis of 1428 Atlantic salmon sampled from 1965 to 2006 in 25 populations throughout France to investigate the influence of stocking on the neutral genetic structure in wild Atlantic salmon (Salmo salar) populations. On the basis of the analysis of 11 microsatellite loci, we found that the overall genetic structure among populations dramatically decreased over the period studied. Admixture rates among populations were highly variable, ranging from a nearly undetectable contribution from donor stocks to total replacement of the native gene pool, suggesting extremely variable impacts of stocking. Depending on population, admixture rates either increased, remained stable, or decreased in samples collected between 1998 and 2006 compared to samples from 1965 to 1987, suggesting either rising, long-lasting or short-term impacts of stocking. We discuss the potential mechanisms contributing to this variability, including the reduced fitness of stocked fish and persistence of wild locally adapted individuals.
The river-resident Salmo salar ("sm ablank") has been isolated from other Atlantic salmon populations for 9,500 years in upper River Namsen, Norway. This is the only European Atlantic salmon population accomplishing its entire life cycle in a river. Hydropower development during the last six decades has introduced movement barriers and changed more than 50% of the river habitat to lentic conditions. Based on microsatellites and SNPs, genetic variation within sm ablank was only about 50% of that in the anadromous Atlantic salmon within the same river. The genetic differentiation (F ST ) between sm ablank and the anadromous population was 0.24. This is similar to the differentiation between anadromous Atlantic salmon in Europe and North America. Microsatellite analyses identified three genetic subpopulations within sm ablank, each with an effective population size N e of a few hundred individuals. There was no evidence of reduced heterozygosity and allelic richness in contemporary samples (2005)(2006)(2007)(2008) compared with historical samples (1955-56 and 1978-79). However, there was a reduction in genetic differentiation between sampling localities over time. SNP data supported the differentiation of sm ablank into subpopulations and revealed downstream asymmetric gene flow between subpopulations. In spite of this, genetic variation was not higher in the lower than in the upper areas. The meta-population structure of sm ablank probably maintains genetic variation better than one panmictic population would do, as long as gene flow among subpopulations is maintained. Sm ablank is a unique endemic island population of Atlantic salmon. It is in a precarious situation due to a variety of anthropogenic impacts on its restricted habitat area. Thus, maintaining population size and avoiding further habitat fragmentation are important.
Rivers in Asturias (northern Spain) constitute the southern limit of the distribution of Atlantic salmon (Salmo salar L.) in Europe, a biological resource facing one of the more serious challenges for conservation today. In this work, eight microsatellite loci have been used to analyse samples collected in 1993 and 1999 from four Asturian rivers (Esva, Narcea, Sella, and Cares), obtaining information about the temporal and the spatial genetic variation in these populations and, in addition, estimations of their effective population sizes. The temporal analysis revealed a general decrease in all the estimated genetic variability parameters when samples from 1993 (mean A(1993) = 6.47, mean HO(1993) = 0.472, mean HE(1993) = 0.530) were compared with those obtained in 1999 (mean A(1999) = 6.16, mean HO(1999) = 0.460, mean HE(1999) = 0.490). This reduction was particularly notable for the case of the Esva river. Our results pointed to a pattern of spatial genetic differentiation inside the Asturian region (FST (1993) = 0.016 P\0.01; FST (1999) = 0.023 P\0.01). Using the standard Temporal Method we found estimates of Ne ^ (Esva) = 75.1 (33.2–267.2); Ne ^ (Cares) = 96.6 (40.0–507.5), Ne ^ (Sella) = 106.5 (39.1–9396.4) and Ne ^ (Narcea) = 113.9 (42.0–3693.3). The use of likelihood-based methods for the Ne ^ estimations improved the results (smaller CIs) for the Esva and Cares rivers (Ne ^ (Esva) = 63.9 (32.3–165.3); Ne ^ (Cares) = 76.4 (38.8–202.0) using a Maximum likelihood approach) and suggested the presence of larger populations for the Sella and Narcea rivers (Ne ^&200). These results showed that the Asturian Atlantic salmon populations (in particular Esva and Cares river populations) could be close to the conservation genetic borderline for avoiding inbreeding depression although we discuss some implications of the analysis of temporal genetic change in populations with overlapping generations.
Molecular ecology, 2011
Disentangling the effects of natural environmental features and anthropogenic factors on the genetic structure of endangered populations is an important challenge for conservation biology. Here, we investigated the combined influences of major environmental features and stocking with non-native fish on the genetic structure and local adaptation of Atlantic salmon (Salmo salar) populations. We used 17 microsatellite loci to genotype 975 individuals originating from 34 French rivers. Bayesian analyses revealed a hierarchical genetic structure into five geographically distinct clusters. Coastal distance, geological substrate and river length were strong predictors of population structure. Gene flow was higher among rivers with similar geologies, suggesting local adaptation to geological substrate. The effect of river length was mainly owing to one highly differentiated population that has the farthest spawning grounds off the river mouth (up to 900 km) and the largest fish, suggesting local adaptation to river length. We detected high levels of admixture in stocked populations but also in neighbouring ones, implying large-scale impacts of stocking through dispersal of non-native individuals. However, we found relatively few admixed individuals suggesting a lower fitness of stocked fish and/or some reproductive isolation between wild and stocked individuals. When excluding stocked populations, genetic structure increased as did its correlation with environmental factors. This study overall indicates that geological substrate and river length are major environmental factors influencing gene flow and potential local adaptation among Atlantic salmon populations but that stocking with non-native individuals may ultimately disrupt these natural patterns of gene flow among locally adapted populations.
ICES Journal of Marine Science, 2006
The populations of Atlantic salmon in the Ulla and Lérez rivers, located in Galicia in northwestern Spain, were close to extinction early in the 1990s. A restoration programme involving supportive breeding has been conducted since 1995, using a mixture of salmon populations from several Galician rivers. The programme utilizes progeny of adults returning to the rivers and wild parr reared in fresh water until maturity. Five microsatellite loci were used to compare genetic variability in the restored populations with that in populations before their collapse in the 1950s. DNA samples were obtained from scale collections (old samples) and from tissue samples of live fish caught in the rivers (modern samples). Average heterozygosities and allelic richness are very similar in modern and old samples. Populations inhabiting the Ulla and Lérez rivers today are more similar than they were in the past, possibly because they originated in the same stock mixture.