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Spatial and temporal variation of genetic diversity and estimation of effective population sizes in Atlantic salmon (Salmo salar, L.) populations from Asturias (Northern Spain) using microsatellites

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Abstract

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 H O(1993) = 0.472, mean H E(1993) = 0.530) were compared with those obtained in 1999 (mean A (1999) = 6.16, mean H O(1999) = 0.460, mean H E(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 (F ST (1993) = 0.016 P < 0.01; F ST (1999) = 0.023 P < 0.01). Using the standard Temporal Method we found estimates of N ^e (Esva) = 75.1 (33.2–267.2); N ^e (Cares) = 96.6 (40.0–507.5), N ^e (Sella) = 106.5 (39.1–9396.4) and N ^e (Narcea) = 113.9 (42.0–3693.3). The use of likelihood-based methods for the N ^e estimations improved the results (smaller CIs) for the Esva and Cares rivers (N ^e (Esva) = 63.9 (32.3–165.3); N ^e (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 (N ^e ≈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.

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References

  • Berthier P, Beamount MA, Cornuet JM, Luikart G (2002) Likelihood-based estimation of the effective population size using temporal changes in allele frequencies: a genealogical approach. Genetics 160:741–751

    PubMed  CAS  Google Scholar 

  • Blanco G, Sánchez JA, Vázquez E, Rubio J, Utter FM (1992) Genetic differentiation among natural European populations of Atlantic salmon, Salmo salar L., from drainages of the Atlantic Ocean. Anim Genet 23:11–18

    PubMed  CAS  Google Scholar 

  • Blanco G, Ramos MD, Vázquez E, Sánchez JA (2005) Assessing temporal and spatial variation in wild populations of Atlantic salmon with particular reference to Asturias (Northern Spain) rivers. J Fish Biol 67(A):169–184

    Article  CAS  Google Scholar 

  • Borrell YJ, Pineda H, McCarthy I, vázquez E, Sánchez JA, Blanco GB (2004) Correlations between fitness and heterozygosity at allozyme and microsatellite loci in the Atlantic salmon, Salmo salar L. Heredity 92:585–593

    Article  PubMed  CAS  Google Scholar 

  • Braña A, Nicieza Ag, Garrido R, Vauclin V (1995) Caracterización de las poblaciones actuales y análisis de las tendencias de variación. In: ICONA: Biología y conservación del Salmón Atlántico (Salmo salar) en los ríos de la región cantábrica (eds. Ministerio de Agricultura, Pesca y Alimentación), pp 27–66. Madrid

  • Caballero P, Garcia Rego M, Garcia de Leaniz C (2001) Estrategias migradoras y reproductivas del salmón atlántico y la trucha común en la cuenca del río Ulla (Galicia): implicaciones para la conservación de las poblaciones. In: García de Leaniz C, Serdio A, Consuegra S (eds) El salmón, Joya de nuestros ríos. Gobierno de Cantabria, Consejeria de Ganaderia, Agricultura y Pesca, Santander, Spain, pp 155–172

    Google Scholar 

  • Consuegra S, Verspoor E, Knox D, García de Leaniz C. (2005) Asymmetric gene flow and the evolutionary maintenance of genetic diversity in small, peripheral Atlantic salmon populations. Conserv Genetics 6:823–842

    Article  CAS  Google Scholar 

  • Cornuet JM, Luikart G. (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed  CAS  Google Scholar 

  • De la Hoz R (1999) Resultados de los programas de repoblación y marcaje de Salmón Atlántico en Asturias (España). In: El salmón atlántico en la Península Ibérica: Un reto del siglo XXI (eds KRK), pp 225–230 Oviedo, Spain

  • De la Hoz R (2001) Present status of Atlantic salmon in Asturias (Spain). In: García de Leaniz C, Serdio A, Consuegra S (eds) El salmón, Joya de nuestros ríos. Gobierno de Cantabria, Consejeria de Ganaderia, Agricultura y Pesca, Santander, Spain, pp 39–53

    Google Scholar 

  • Estoup A, Presa P, Krieg F, Vaiamn D, Guyomard R (1993) (CT)n and (GT)n microsatellites: a new class of genetic markes for Salmo trutta L. (Brown trout) Heredity 71:488–496

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Smouse P, Quattro J (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 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online (submitted)

  • Ferguson A, Verspoor E, Cross T, García Vázquez E, McGuinnity P, García de Leániz C (1996) An assessment of the genetic consequences of the deliberate or inadvertent introduction of non-native atlantic salmon into natural populations. Final Report. 1993–1996

  • Franklin LR (1980) Evolutionary changes in small populations. In: Soulé ME (eds) Conservation biology: an evolutionary-ecological perspective. Sinauer Associates, Sunderland Massachusetts, pp 135–149

    Google Scholar 

  • García de Leániz C, Verspoor E, Hawkins D (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(suppl A):261–270

    Google Scholar 

  • García-Vázquez E, Moran P, Martínez JL, Pérez J, Gaudermar B, Beall E (2001) Alternative mating strategies in Atlantic salmon and brown trout. J Hered 92(2):146–149

    Article  PubMed  Google Scholar 

  • Goudet J (1995) FSTAT (vers. 1.2): a computer program to calculate F-statistics. J Heredity 86:485–486

    Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from: http://www.unil.ch/izea/softwares/fstat.html

  • Hauser L, Ward RD (1998) Population identification in pelagic fish: the limits of molecular markers. In: Carvalho GR (ed) Advances in molecular ecology 191–216. ISO Press

  • Hedrick PW (1999) Highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318

    Article  Google Scholar 

  • Kalinowski ST, Waples RS (2002) Relationship of effective to census size in fluctuating populations. Cons Biol 16(1):129–136

    Article  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 microsatellites DNA variation. Mol Ecol 10:807–821

    Article  PubMed  CAS  Google Scholar 

  • Krimbas CB, Tsakas S (1971) The genetics of Dacus oleae V. Changes of esterase polymorphism in natural population following insecticide control-selection or drift? Evolution 25:454–460

    Article  Google Scholar 

  • La Hood ES, Moran P, Olsen J, Grant S, Park LK (2002) Microsatellite allele ladders in two species of Pacific salmon: preparation and field-test results. Mol Ecol Notes 2:187–190

    Article  CAS  Google Scholar 

  • Leberg PL (2002) Estimating allelic richness: effects of simple size and bottlenecks. Mol Ecol 11:2445–2449

    Article  PubMed  CAS  Google Scholar 

  • Luikart G, Cornuet JM (1997) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12(1):228–237 [Feb. 1998]

    Article  Google Scholar 

  • Machado-Schiaffino G, Dopico E, Garcia-Vazquez E (2007) Genetic variation losses in Atlantic salmon stocks created for supportive breeding. Aquaculture 264:59–65

    Article  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    PubMed  CAS  Google Scholar 

  • Martínez JL, Morán P, Pérez J, de Gaudemar B, Beall E, García-Vázquez E (2000) Multiple paternity increases effective size of southern Atlantic salmon populations. Mol Ecol 9:293–298

    Article  PubMed  Google Scholar 

  • Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142:1061–1064

    PubMed  CAS  Google Scholar 

  • Morán P, Pendás AM, García-Vázquez E, Izquierdo JL (1994) Genetic variation among Atlantic salmon in six Spanish rivers. J Fish Biol 45:831–837

    Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    PubMed  CAS  Google Scholar 

  • Nei M, Tajima F (1981) Genetic drift and estimation of effective population size. Genetics 98(3):625–640

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Nicieza AG, Toledo MM, Braña F (1990) Capturas de salmón atlántico (Salmo salar L.) en los ríos asturianos en el periodo 1953–1989. Variaciones en abundancia y estructura de edades de mar. Biodatos básicos Suplemento de Biología de la Universidad Oviedo 4:1–91

    Google Scholar 

  • Pemberton JM, Slate J, Bancroft DR, Barrett JA (1995) Nonamplifying alleles at microsatellite loci: a caution for parentage and population studies. Mol Ecol 4:249–252

    Article  PubMed  CAS  Google Scholar 

  • Pongsomboon S, Whan V, Moore SS, Tassanakajon A (2000) Characterization of tri-and tetranucleotide microsatellites in the black tiger prawn Penaeus monodon. Sci Asia 26:1–8

    Article  CAS  Google Scholar 

  • Rice WR (1989) Analysing tables of statistical test. Evolution 43:223–225

    Article  Google Scholar 

  • Sánchez JA, Blanco G, Vázquez E, García E, Rubio J (1991) Allozyme variation in natural populations of Atlantic salmon in Asturias (norther Spain). Aquaculture 93:291–298

    Article  Google Scholar 

  • Sánchez JA, Clabby C, Ramos D, Blanco G, Flavin F, Vázquez E, Powell R (1996) Protein and microsatellite single locus variability in Salmo salar L (Atlantic salmon) Heredity 77:423–432

    Article  PubMed  Google Scholar 

  • Sánchez JA, Ramos MD, Pineda H, Borrell Y, Vázquez E, Blanco G (2000) The application of genetic variation at microsatellite loci in Atlantic salmon (Salmo salar) stock identification. ICES CM 2000/Y:06, 8 pages

  • Shrimpton JM, Heath DD (2003) Census vs. effective population size in chinook salmon: large- and small-scale environmental perturbations effects. Mol Ecol 12:2571–2583

    Article  PubMed  CAS  Google Scholar 

  • Slettan A, Olsaker I, Lie O (1993) Isolation and characterization of variable (GT)n repetitive sequences from Atlantic salmon, Salmo salar L. Anim Genet 24:195–197

    Article  CAS  Google Scholar 

  • Slettan A, Olsaker I, Lie O (1995) Atlantic salmon, Salmo salar L, microsatelllites at the SSOSL311, SSOSL417, SSOSL85, SSOSL25 loci. Anim Genet 26:277–285

    Google Scholar 

  • Swofford DL, Selander B (1981) BIOSYS-1: a FORTRAN program for the comprehensive analysis of electrophoretic data in population genetics and systematics. J Hered 72:282–302

    Google Scholar 

  • Tajima F (1992) Statistical method for estimating the effective population size in Pacific salmon. J Hered 83:309–311

    Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4(3):535–538

    Article  CAS  Google Scholar 

  • Vázquez E, Presa P, Sánchez JA, Blanco G, Utter F (1993) Genetic characterization of introduced populations of Atlantic salmon, Salmo salar, in Asturias (Northern Spain). Hereditas 119:47–51

    Article  Google Scholar 

  • Verspoor E, García de Leaniz C (1997) Stocking success of Scottish Atlantic Salmon in two Spanish rivers. J Fish Biology 51:1265–1269

    Article  Google Scholar 

  • Verspoor E, Beardmore JA, Consuegra S, García de Leániz C, Hindar K, Jordan WC, Koljonen ML, Mahkrov AA, Paaver T, Sánchez JA, Skaala Ø, Titov S, Cross TF (2005) Population structure in the Atlantic salmon: insights from 40 years of research into genetic protein variation. J Fish Biol 67(A):3–54

    Article  CAS  Google Scholar 

  • Wang J (2001) A pseudo-likelihood method for estimating effective population size from temporal spaced samples. Genet Res 78:243–257

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Whitlock MC (2003) Estimating effective population size and migration rates from genetic samples over space and time. Genetics 163:429–446

    PubMed  CAS  Google Scholar 

  • Waples RS (1989) A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics 121:379–391

    PubMed  CAS  Google Scholar 

  • Waples RS (1998) Separating the wheat from the chaff: Patterns of genetic differentiation in high gene flow species. J Hered 89(5):438–450

    Article  Google Scholar 

  • Waples RS (2002) Effective size of fluctuating salmon populations. Genetics 161:783–791

    PubMed  Google Scholar 

  • Waples RS, Yokota M (2007) Temporal estimates of effective population size in species with overlapping generations. Genetics 175(1):219–233

    Article  PubMed  Google Scholar 

  • Waples RS, Masuda M, Pella J (2007) SALMONNb: a program for computing cohort-specific effective population sizes (N ^ b ) in Pacific salmon and other semelparous species using the temporal method. Mol Ecol Notes 7:21–24

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1538–1370

    Article  Google Scholar 

  • Wright S (1931) Evolution in Mendelian populations. Genetics 16:96–159

    Google Scholar 

  • WWF (2001) The status of wild Atlantic salmon: a river by river assessment. WWF, May 2001. Available at: http://www.panda.org/news_facts/publications/general/index.cfm

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Acknowledgements

The authors wish to acknowledge the “Consejería de Medio Rural y Pesca de Asturias” for supplying biological samples and the “Ministerio de Educación, Cultura y Deporte de España” for the FPU Grant awarded to David Bernardo. Authors thanks to R. Waples (in particular) and to others anonymous reviewers for their comments and help.

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  1. Departamento de Biología Funcional. Laboratorio de Genética Acuícola. IUBA, Universidad de Oviedo, c/Julián Clavería s/n. 33071, Oviedo, Asturias, Spain

    Yaisel Juan Borrell, David Bernardo, Gloria Blanco, Emilia Vázquez & José Antonio Sánchez

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  1. Yaisel Juan Borrell
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  2. David Bernardo
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  3. Gloria Blanco
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Correspondence to José Antonio Sánchez.

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Borrell, Y.J., Bernardo, D., Blanco, G. et al. Spatial and temporal variation of genetic diversity and estimation of effective population sizes in Atlantic salmon (Salmo salar, L.) populations from Asturias (Northern Spain) using microsatellites. Conserv Genet 9, 807–819 (2008). https://doi.org/10.1007/s10592-007-9400-5

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