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ICES Journal of Marine Science: Journal du Conseil 2006 63(7):1269-1273; doi:10.1016/j.icesjms.2006.03.023
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© 2006 International Council for the Exploration of the Sea

Loss of regional population structure in Atlantic salmon, Salmo salar L., following stocking

Fernando Ayllon, Jose L. Martinez and Eva Garcia-Vazquez*

Departamento de Biologia Funcional, Facultad de Medicina, Universidad de Oviedo 33006 Oviedo, Spain

*Correspondence to E. Garcia-Vazquez: tel: +34 985 102726; fax: +34 985 103534. e-mail: egv{at}fq.uniovi.es.

Many wild Atlantic salmon populations have been stocked with cultured fish during the past century. To evaluate the degree and the direction of the resulting genetic changes in wild southern European populations of Atlantic salmon, the variation at microsatellite loci was examined in historical and modern scale samples from five Spanish and two French rivers. Significant genetic differentiation between neighbouring rivers, which is typical of Atlantic salmon and which existed before stocking, appears to have been lost after only a decade of stocking with fish of foreign origin. Apparent introgression of foreign-origin genes into local gene pools was detected in the populations studied. These results indicate that stocking risks the loss of genetic diversity in wild salmon populations.

Keywords: Atlantic salmon, genetic variation, microsatellite loci, population structure, regional diversity, stocking

Received 2 November 2005; accepted 30 March 2006.


   Introduction
Top
 Introduction
Material and methods
 Results and discussion
 References
 
Because Atlantic salmon, Salmo salar L., exhibit a high degree of homing and fidelity to their natal river (Ryman and Utter, 1987), gene flow between local populations is minimal, and salmon inhabiting neighbouring rivers are reproductively isolated (Elo, 1993). This substantial isolation has facilitated genetic differentiation among wild Atlantic salmon populations, observed at neutral genetic loci in surveys of variation at allozyme loci (Davidson et al., 1989; Jordan et al., 1992; Moran et al., 1994a; Sanchez et al., 1996; Bourke et al., 1997), minisatellite loci (Galvin et al., 1995, 1996), microsatellite loci (Sanchez et al., 1996; McConnell et al., 1997; Nielsen et al., 1997; Beacham and Dempson, 1998), and in mitochondrial DNA (Tessier et al., 1997). As a consequence, Atlantic salmon populations exhibit high spatial differentiation at every geographic level examined, from continents to rivers within a region (King et al., 2001).

In recent years, many salmon populations have declined and some populations, particularly at the southern limit of the range of the species in Europe and North America, are close to extinction (Parrish et al., 1998) as a result of, inter alia, habitat modifications and low at-sea survival (Parrish et al., 1998; Friedland et al., 2003). However, small population size has not severely affected genetic variability in some southern European rivers (Moran and Garcia-Vazquez, 1998). The spawning of mature male parr may increase the effective population size, thus at least partially compensating for low returns of sea-run adults (Garant et al., 2000; Martinez et al., 2000). Another factor that might theoretically increase genetic variability is high gene flow, which may have occurred as a result of the stocking of northern European salmon stocks in southern European rivers during the period 1981–1991 (Baglinière et al., 1990; Dumas and Barrière, 1991; Vazquez et al., 1993). Often a single donor stock was used to supplement a number of rivers in a region (Vazquez et al., 1993; Moran et al., 2005). Thus, there is a risk of genetic homogenization caused by the reduction in the spatial component of population variation (Vasemägi et al., 2005), posing a threat of disruption to local adaptations (Allendorf et al., 2001; Utter, 2001). However, the effect of stocking on regional genetic diversity remains unclear (Verspoor, 1997).

In Spanish salmon rivers, stocking of foreign-origin fish has contributed differentially to the current genetic structure of salmon populations (Moran et al., 2005). In some rivers, the negligible proportions of foreign genomes suggest that the foreign-origin stocked fish were not successful (Garcia-Vazquez et al., 1991; Moran et al., 1998, 2005; Blanco et al., 2005), while in the heavily stocked Nivelle River population in the south of France, the low proportion of foreign introgressed genomes was explained by greater reproductive success of native individuals (Martinez et al., 2001).

This study aims to quantify the changes in salmon population differentiation following intense stocking with hatchery-reared salmon in seven rivers located at the southern limit of the European range of Atlantic salmon (Moran et al., 2005). Hypervariable microsatellite loci and mitochondrial RFLP DNA variation were used as genetic markers.


   Material and methods
Top
 Introduction
 Material and methods
Results and discussion
 References
 
Samples
The locations of the study rivers are shown in Figure 1. These rivers were all stocked with foreign-origin Atlantic salmon, mainly from Scotland, from 1981 to 1991 (Table 1).


Figure 1
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  		Figure 1 The location of the seven rivers studied.

 


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  		Table 1 The cumulative number of foreign fish stocked and the cumulative number of adult salmon caught (1981–1996) in the seven study rivers.

 
DNA was extracted from scales collected from adult salmon caught by anglers in five Spanish rivers (Eo, Esva, Narcea, Sella, and Cares) during 1980–1985 (old samples) and during 1999–2000 (modern samples), before and after the peak of foreign stocking, respectively. Two or three scales were obtained from each fish. From the Sella River, only modern scale samples were available. Additional samples from two French rivers (Nivelle and Nive) for 2000 and a sample (n = 44) of Scottish hatchery juveniles stocked in southern European rivers in the 1980s were provided by the staff of the Institute National de la Recherche Agronomique (INRA), St Pée sur Nivelle, France. Details of the number of samples analysed from each river appear in Table 2.


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  		Table 2 Genetic variation at five microsatellite loci in the samples analysed. n, Number of samples analysed; Mean Na, mean number of alleles per locus; Mean He, mean heterozygosity expected across loci; Mean Ho, mean heterozygosity observed; HWE p-value, p-values of tests for conformity with Hardy–Weinberg equilibrium for each population.

 
Genetic analyses
Total DNA extraction was based on Chelex methodology (Estoup et al., 1996). Five loci were amplified: SSOSL85, SSOSL311, SSOSL417 (Slettan et al., 1995), SSA197 (O'Reilly et al., 1996), and SS4 (Martinez et al., 1999). Polymerase Chain Reaction (PCR) amplifications and determination of allele sizes were performed as described in Ayllon et al. (2004).

Statistical analyses
Scoring errors, allele drop-out, and null alleles were checked with the program MICROCHECKER (van Oosterhout et al., 2004). Observed and expected heterozygosity and mean number of alleles per locus were determined employing the GENETIX computer package (GENETIX, 2000). Exact p-values for testing conformation of genotypes to Hardy–Weinberg proportions and linkage disequilibrium were estimated by the Markov Chain Method (1000 dememorization steps, 1000 batches, 1000 iterations per batch). Sequential Bonferroni correction was applied when pertinent (Rice, 1989). Statistical differences among groups of samples (before and after stocking) were estimated employing the program FSTAT (Goudet, 2001) with 10 000 permutations. Allele frequencies and paired theta values (FST of Weir and Cockerham, 1984), indicating differences in allele frequencies between populations, were calculated using the GENETIX package (GENETIX, 2000). Mantel tests (with 1000 permutations) to estimate possible associations between genetic and geographic distances between populations were performed with the program MANTEL within the package GENETIX.

The Monte-Carlo simulation based IMMANC5 computer program (Rannala and Mountain, 1997) was employed for identifying individuals of foreign origin, based on their microsatellite genotypes (with 10 000 replications).


   Results and discussion
Top
 Introduction
 Material and methods
 Results and discussion
References
 
No evidence of null alleles, large allele drop-out, and stuttering were found in the studied populations after checking their microsatellite genotypes with the program MICROCHECKER. Heterozygosity values and allele numbers per locus found for the seven populations studied (Table 2) were similar to those described at microsatellite loci for other Atlantic salmon populations, both in Europe and North America (Sanchez et al., 1996; McConnell et al., 1997; Garant et al., 2000; King et al., 2001; Letcher and King, 2001). Some tests for linkage disequilibrium between loci were significant after correction for multiple tests, owing to different pairs of loci (3 out of 70 tests). These associations were probably the result of the population mixture, as is also indicated by deviations from Hardy–Weinberg equilibrium (Table 2), which are always the result of an excess of homozygotes. Although Atlantic salmon populations typically exhibit genetic isolation between neighbouring rivers (Elo, 1993), natural gene flow cannot be excluded in this area; it might have caused significant deviation from Hardy–Weinberg equilibrium, especially in old samples for which gene introgression resulting from foreign stocking could be excluded.

In this study, lack of regional population structure was indicated by a non-significant Mantel test (r = 0.520) of association between genetic and geographical distances between populations in modern samples. Significant increases of both allelic richness and heterozygosity were found after stocking in the Spanish region (Table 3), suggesting introgression between native and non-native stocked salmon may have occurred. A significant reduction in regional between-population differentiation (FST) in modern samples indicates a loss of regional population structure following stocking. The correlation coefficient between paired theta values and geographical distances between pairs of samples decreased by one-half in modern samples (r = 0.246) compared with the old samples (r = 0.498; Figure 2), illustrating the effect of introgression of hatchery-reared stocks into these southern European salmon populations. In all, 24 individuals were identified as belonging to the Scottish hatchery stock, representing 4.5–8.3% introgression in the seven study rivers (Table 4). These values are close to those reported by other authors for rivers in this area (Moran et al., 1998, 2005; Martinez et al., 2001).


Figure 2
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  		Figure 2 A plot of theta values (estimates of differences in allele frequencies) against geographic distances between paired populations. Old samples, triangles (linear trend as a dotted line); modern samples, squares (linear trend as a solid line).

 


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  		Table 3 Parameters of genetic variability in old and modern Spanish samples; p-value of the statistical difference between the two groups; AR, mean allelic richness; Ho, mean heterozygosity observed; He, mean heterozygosity expected; FIS and FST indicate within- and between-sample genetic differentiation, respectively.

 


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  		Table 4 Number and percentage of Scottish-origin hatchery fish identified in modern samples for the seven study rivers considered. n, Number of samples analysed in each river; Ns, number of foreign stocked individuals identified in each river employing the IMMANC program; %, percentage of Scottish-origin stocked individuals.

 
The mechanisms of gene transfer can be related to the reproduction of large anadromous salmon of foreign origin in the rivers into which they were stocked as juveniles, although their success appears less in southern European rivers (Verspoor and Garcia de Leaniz, 1997; Martinez et al., 2001). Straying of hatchery-origin fish returning to rivers to spawn may also contribute to the loss of regional genetic differentiation as reported for other European regions (Vasemägi et al., 2005). Additionally, the reproduction of foreign-origin mature male salmon parr may also account for some introgression of foreign genomes, as suggested by Moran et al. (1994b) because mature parr can fertilize a large proportion of eggs in southern European rivers (Moran et al., 1996; Thomaz et al., 1997; Martinez et al., 2000).

Gene flow between the river systems in this study probably resulted from the widespread transfer of hatchery stocks among European rivers, a common practice for other fish species (e.g. Weiss et al., 2001). Translocations should, therefore, be avoided if population conservation is a priority (Lodge and Shrader-Frechette, 2003; Sanders et al., 2003). This study indicates that regional genetic diversity can be lost through stocking of foreign-origin salmon, a serious threat to salmonid populations which are characterized by strong local adaptations (Taylor, 1991).


   Acknowledgements
 
We are grateful to Ivan G. Pola for help with laboratory analyses. Edward Beall and Jacques Dumas (INRA, France) kindly provided the French and Scottish samples. Peter Hutchinson kindly revised the manuscript and improved it considerably. This study was funded by the Spanish Grant MCYT REN2003-00303.


   References
Top
 Introduction
 Material and methods
 Results and discussion
 References
 

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