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Stocking may increase mitochondrial DNA diversity but fails to halt the decline of endangered Atlantic salmon populations

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Abstract

Over the last 50 years, Spanish Atlantic salmon (Salmo salar) populations have been in decline. In order to bolster these populations, rivers were stocked with fish of northern European origin during the period 1974–1996, probably also introducing the furunculosis-inducing pathogen, Aeromonas salmonicida. Here we assess the relative importance of processes influencing mitochondrial (mt)DNA variability in these populations from 1948 to 2002. Genetic material collected over this period from four rivers in northern Spain (Cantabria) was used to detect variability at the mtDNA ND1 gene. Before stocking, a single haplotype was found at high frequency (0.980). Following stocking, haplotype diversity (h) increased in all rivers (mean h before stocking was 0.041, and 0.245 afterwards). These increases were due principally to the dramatic increase in frequency of a previously very low frequency haplotype, reported at higher frequencies in northern European populations proximate to those used to stock Cantabrian rivers. Genetic structuring increased after stocking: among-river differentiation was low before stocking (1950s/1960s Φ ST = –0.00296–0.00284), increasing considerably at the height of stocking (1980s Φ ST = 0.18932) and decreasing post-stocking (1990s/2002 Φ ST = 0.04934–0.03852). Gene flow from stocked fish therefore seems to have had a substantial role in increasing mtDNA variability. Additionally, we found significant differentiation between individuals that had probably died from infectious disease and apparently healthy, angled fish, suggesting a possible role for pathogen-driven selection of mtDNA variation. Our results suggest that stocking with non-native fish may increase genetic diversity in the short term, but may not reverse population declines.

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References

  • Aprahamian MW, Smith KM, Mcginnity P, Mckelvey S, Taylor J (2003) Restocking of salmonids—opportunities and limitations. Fish Res 62:211–227

    Article  Google Scholar 

  • Ballard JWO, Rand DM (2005) The population biology of mitochondrial DNA and its phylogenetic implications. Ann Rev Ecol Evol Syst 36:621–642

    Article  Google Scholar 

  • Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744

    Article  PubMed  Google Scholar 

  • Britt A, Welch C, Katz A, Iambana B, Porton I, Junge R, Crawford G, Williams C, Haring D (2004) The re-stocking of captive-bred ruffed lemurs (Varecia variegata variegata) into the Betampona Reserve, Madagascar: methodology and recommendations. Biodivers Conserv 13:635–657

    Article  Google Scholar 

  • Buckmeier DL, Schlechte JW, Betsill RK (2003) Stocking fingerling largemouth bass to alter genetic composition: efficacy and efficiency of three stocking rates. North Am J Fish Manage 23:523–529

    Article  Google Scholar 

  • Consuegra S, García De Leániz C, Serdio A, Morales MG, Straus LG, Knox D, Verspoor E (2002) Mitochondrial DNA variation in Pleistocene and modern Atlantic salmon from the Iberian glacial refugium. Mol Ecol 11:2037–2048

    Article  PubMed  CAS  Google Scholar 

  • Consuegra S, García De Leániz C, Serdio A, Verspoor E (2005a) Selective exploitation of early running fish may induce genetic and phenotypic changes in Atlantic salmon. J Fish Biol 67:129–145

    Article  Google Scholar 

  • Consuegra S, Verspoor E, Knox D, García De Leániz C (2005b) Asymmetric gene flow and the evolutionary maintenance of genetic diversity in small, peripheral Atlantic salmon populations. Conserv Genet 1–20

  • Cronin MA, Spearman WJ, Wilmot RL, Patton JC, Bickham JW (1993) Mitochondrial-DNA variation in Chinook (Oncorhynchus–Tshawytscha) and Chum Salmon (O Keta) detected by restriction enzyme analysis of polymerase chain-reaction (PCR) Products. Can J Fish Aquat Sci 50:708–715

    Article  CAS  Google Scholar 

  • Danielsdottir AK, Marteinsdottir G, Arnason F, Gudjonsson S (1997) Genetic structure of wild and reared Atlantic salmon (Salmo salar L.) populations in Iceland. ICES J Mar Sci 54:986–997

    Google Scholar 

  • Einum S, Fleming IA (1997) Genetic divergence and interactions in the wild among native, farmed and hybrid Atlantic salmon. J Fish Biol 50:634–651

    Article  Google Scholar 

  • Englbrecht CC, Schliewen U, Tautz D (2002) The impact of stocking on the genetic integrity of Arctic charr (Salvelinus) populations from the Alpine region. Mol Ecol 11:1017–1027

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinfo Online 1:47–50

    CAS  Google Scholar 

  • Excoffier L, Smouse PE (1994) Using allele frequencies and geographic subdivision to reconstruct gene trees within a species—molecular variance parsimony. Genetics 136:343–359

    PubMed  CAS  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes—application to human mitochondrial-DNA restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • Felsenstein J (1994) PHYLIP (Phlyogency Inference Package) version 3.572c. Department of Genetics, University of Washington, Seattle

    Google Scholar 

  • Fleming IA (1998) Pattern and variability in the breeding system of Atlantic salmon (Salmo salar), with comparisons to other salmonids. Can J Fish Aquat Sci 55:59–76

    Article  Google Scholar 

  • García De Leániz C, Serdio A, Consuegra S (2001) Present status of Atlantic salmon in Cantabria. In: García De Leaníz C, Serdio A, Consuegra S (eds) El Salmón, Joya de nuestros ríos. Santander, Gobierno de Cantabria, Consejería de Ganadería, Agricultura y Pesca

  • García De Leániz C, Verspoor E, Hawkins AD (1989) Genetic determination of the contribution of stocked and wild Atlantic salmon, Salmo-salar L., to the angling fisheries in two spanish rivers. J Fish Biol 35:261–270

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hampe A, Arroyo J, Jordano P, Petit RJ (2003) Rangewide phylogeography of a bird-dispersed Eurasian shrub: contrasting Mediterranean and temperate glacial refugia. Mol Ecol 12:3415–3426

    Article  PubMed  CAS  Google Scholar 

  • Hindar K, Ryman N, Utter F (1991) Genetic-effects of cultured fish on natural fish populations. Can J Fish Aquat Sci 48:945–957

    Google Scholar 

  • Hurst CD, Bartlett SE, Davidson WS, Bruce IJ (1999) The complete mitochondrial DNA sequence of the Atlantic salmon, Salmo salar. Gene 239:237–242

    Article  PubMed  CAS  Google Scholar 

  • Hutchinson WF, Carvalho GR, Rogers SI (1999) A nondestructive technique for the recovery of DNA from dried fish otoliths for subsequent molecular genetic analysis. Mol Ecol 8:893–894

    CAS  Google Scholar 

  • Jaarola M, Searle JB (2002) Phylogeography of field voles (Microtus agrestis) in Eurasia inferred from mitochondrial DNA sequences. Mol Ecol 11:2613–2621

    Article  PubMed  CAS  Google Scholar 

  • Jordan WC, Verspoor E, Youngson AF (1997) The effect of natural selection on estimates of genetic divergence among populations of the Atlantic salmon. J Fish Biol 51:546–560

    Google Scholar 

  • King TL, Kalinowski ST, Schill WB, Spidle AP, Lubinski BA (2001) Population structure of Atlantic salmon (Salmo salar L.): a range-wide perspective from microsatellite DNA variation. Mol Ecol 10:807–821

    Article  PubMed  CAS  Google Scholar 

  • Kirby DM, Mcfarland R, Ohtake A, Dunning C, Ryan MT, Wilson C, Ketteridge D, Turnbull DM, Thorburn DR, Taylor RW (2004) Mutations of the mitochondrial ND1 gene as a cause of MELAS. J Med Gen 41:784–789

    Article  CAS  Google Scholar 

  • McGinnity P, Prodohl P, Maoileidigh NO, Hynes R, Cotter D, Baker N, O’Hea B, Ferguson A (2004) Differential lifetime success an performance of native and non-native Atlantic salmon examined under communal natural conditions. J Fish Biol 65:173–187

    Article  Google Scholar 

  • Martinez JL, Dumas J, Beall E, García-Vazquez E (2001) Assessing introgression of foreign strains in wild Atlantic salmon populations: variation in microsatellites assessed in historic scale collections. Freshw Biol 46:835–844

    Article  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. 2. Gene-frequency data. J Mol Evol 19:153–170

    Article  PubMed  CAS  Google Scholar 

  • Nielsen EE, Hansen MM, Loeschcke V (1996) Genetic structure of European populations of Salmo salar L. (Atlantic salmon) inferred from mitochondrial DNA. Heredity 77:351–358

    CAS  Google Scholar 

  • Nielsen EE, Hansen MM, Loeschcke V (1997) Analysis of microsatellite DNA from old scale samples of Atlantic salmon Salmo salar: a comparison of genetic composition over 60 years. Mol Ecol 6:487–492

    Article  CAS  Google Scholar 

  • Nielsen EE, Hansen MM, Loeschcke V (1999a) Analysis of DNA from old scale samples: technical aspects, applications and perspectives for conservation. Hereditas 130:265–276

    Article  CAS  Google Scholar 

  • Nielsen EE, Hansen MM, Loeschcke V (1999b) Genetic variation in time and space: Microsatellite analysis of extinct and extant populations of Atlantic salmon. Evolution 53:261–268

    Article  Google Scholar 

  • Nilsson J (1997) MtDNA and microsatellite variation in Baltic Atlantic salmon. ICES J Mar Sci 54:1173–1176

    Google Scholar 

  • Nilsson J, Gross R, Asplund T, Dove O, Jansson H, Kelloniemi J, Kohlmann K, Löytynoja A, Nielsen EE, Paaver T, Primmer CR, Titov S, Vasemägi A, Veselov A, Öst T, Lumme J (2001) Matrilinear phylogeography of Atlantic salmon (Salmo salar L.) in Europe and postglacial colonization of the Baltic Sea area. Mol Ecol 10:89–102

    Article  PubMed  CAS  Google Scholar 

  • Ota T (1993) DISPAN: genetic distance and phylogenetic analysis. Pensylvannia State University, University Park, PA

    Google Scholar 

  • Palumbi SR (1996) Nucleic acids II: the polymerase chain reaction. In: Hillis DMMC, Mable BM (eds) Molecular systematics. 2nd edn. Sinauer Associates, Sunderland, Massachusetts

    Google Scholar 

  • Parrish DL, Behnke RJ, Gephard SR, Mccormick SD, Reeves GH (1998) Why aren’t there more Atlantic salmon (Salmo salar)?. Can J Fish Aquat Sci 55:281–287

    Article  Google Scholar 

  • Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109

    Article  Google Scholar 

  • Rozas J, Sanchez-Delbarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Smith JS, Sumner JW, Roumillat LF, Baer GM, Winkler WG (1984) Antigenic characteristics of isolates associated with a new epizootic of raccoon rabies in the United-States. J Infect Diseases 149:769–774

    CAS  Google Scholar 

  • Taylor EB (1991) A review of local adaptation in salmonidae, with particular reference to Pacific and Atlantic Salmon. Aquaculture 98:185–207

    Article  Google Scholar 

  • Valentino ML, Barboni P, Ghelli A, Bucchi L, Rengo C, Achilli A, Torroni A, Lugaresi A, Lodi R, Barbiroli B, Dotti MT, Federico A, Baruzzi A, Carelli V (2004) The ND1 gene of complex I is a mutational hot spot for Leber’s hereditary optic neuropathy. Ann Neurol 56:631–641

    Article  PubMed  CAS  Google Scholar 

  • Vasemagi A, Gross R, Paaver T, Kangur M, Nilsson J, Eriksson LO (2001) Identification of the origin of Atlantic salmon (Salmo salar L.) population in a recently recolonized river in the Baltic Sea. Mol Ecol 10:2877–2882

    Article  PubMed  CAS  Google Scholar 

  • Verspoor E (1997) Genetic diversity among Atlantic salmon (Salmo salar L.) populations. ICES J Mar Sci 54:965–973

    Google Scholar 

  • Verspoor E, García De Leániz C (1997) Stocking success of Scottish Atlantic salmon in two Spanish rivers. J Fish Biol 51:1265–1269

    Article  Google Scholar 

  • Verspoor E, Jordan WC (1989) Genetic-Variation at the Me-2 Locus in the Atlantic Salmon within and between Rivers—Evidence for its selective maintenance. J Fish Biol 35:205–213

    Article  Google Scholar 

  • Verspoor E, Mccarthy EM, Knox D (1999) The phylogeography of European Atlantic salmon (Salmo salar L.) based on RFLP analysis of the ND1/16sRNA region of the mtDNA. Biol J Linnean Soc 68:129–146

    Article  Google Scholar 

  • Wang J, Ryman N (2001) Genetic effects of multiple generations of supportive breeding. Conserv Biol 15

  • WWF (2001) The status of wild Atlantic salmon: a river by river assessment. AGMV Marquis, Québec, Canada

    Google Scholar 

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Authors and Affiliations

  1. Institute of Zoology, Zoological Society of London, Regent’s Park, London, NW1 4RY, UK

    K. L. Ciborowski, J. Wang & W. C. Jordan

  2. School of Biological Sciences, University of Wales Swansea, Swansea, SA2 8PP, UK

    S. Consuegra & C. García de Leániz

  3. School of Animal and Microbial Sciences, University of Reading, Whiteknights, P.O. Box 228, Reading, RG6 6AJ, UK

    M. A. Beaumont

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  1. K. L. Ciborowski
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  2. S. Consuegra
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  3. C. García de Leániz
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  4. J. Wang
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  5. M. A. Beaumont
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  6. W. C. Jordan
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Correspondence to K. L. Ciborowski.

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Ciborowski, K.L., Consuegra, S., García de Leániz, C. et al. Stocking may increase mitochondrial DNA diversity but fails to halt the decline of endangered Atlantic salmon populations. Conserv Genet 8, 1355–1367 (2007). https://doi.org/10.1007/s10592-007-9286-2

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