Conservation Genetics

, Volume 7, Issue 4, pp 515–530 | Cite as

Genetic variation at MHC, mitochondrial and microsatellite loci in isolated populations of Brown trout (Salmo  trutta)

Article

Abstract

We have studied levels and distribution of genetic variation in nine isolated populations of Brown trout in NW Spain. In the present study, we have tried to test the importance of preservation of genetic variability for the survival of a set of isolated Brown trout (Salmo trutta) populations from the same river drainage. We screened genetic variation in three different markers, mitochondrial, microsatellites and Major Histocompatibility Complex (MHC), presumed to be under different selective pressures. Overall, genetic diversity varied considerably across populations and the distribution of genetic variation was similar at MHC and microsatellites; highly polymorphic populations at the microsatellite loci were also highly polymorphic at the MHC. We also observed high levels of differentiation among populations. Although we found evidence suggesting that balancing selection has influenced the long term evolution of the MHC, genetic drift seems to have eroded the effect of selection, becoming the predominant evolutionary force shaping genetic variation in some of the smaller populations. Despite current lack of variation at the MHC, these small populations seem to have remained viable for a long time.

Keywords

MHC Brown trout Salmo trutta balancing selection ND1 microsatellite 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

We are very grateful to José Manuel Cano, David Alvarez and Alfredo González Nicieza for generously providing the samples used here, and for supplying concrete details about the rivers studied. We appreciate comments on the manuscript from Armando Caballero, Antonio Carvajal-Rodríguez, Humberto Quesada and Emilio Rolán. Pilar Alvariño and Nieves Santamaria assisted with technical support. We are thankful for the help provided by José Luis Martínez and Eva García-Vázquez’s lab. Jose L Campos is supported by a grant from Xunta de Galicia.

References

  1. Aguilar A, Roemer G, Debenham S, Binns M, Garcelon D, Wayne RK (2004) High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc. Natl. Acad. Sci. USA 101:3490–3494PubMedGoogle Scholar
  2. Anisimova M, Nielsen R, Yang Z (2003) Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 164:1229–1236PubMedGoogle Scholar
  3. Antunes A, Faria R, Weiss S, Alexandrino P (2001) Complex evolutionary history in the brown trout: Insights on the recognition of conservation units. Conserv. Genet. 2:337–347Google Scholar
  4. Apostolidis A, Karakousis Y, Triantaphyllidis C (1996) Genetic divergence and phylogenetic relationships among Salmo trutta L. (Brown trout) populations from Greece and other European countries. Heredity 76:551–560Google Scholar
  5. Arkush KD, Giese AR, Mendonca HL, McBride AM, Marty GD, Hedrick PW (2002) Resistance to three pathogens in the endangered winter-run Chinook salmon (Oncorhynchus tshawytscha): effects of inbreeding and major histocompatibility complex genotypes. Can. J. Fish. Aquat. Sci. 59:966–975Google Scholar
  6. Beerli P, Felsenstein J (1999) Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152:763–773PubMedGoogle Scholar
  7. Belkhir K, Borsa P, Goudet J, Chikhi L, Bonhomme F (1998) GENETIX, logiciel sous Windows TM pour la genetique des populations. Laboratoire Genome et Populations, CNRS UPR 9060. Universite de Montpellier II, MontpellierGoogle Scholar
  8. Bergstrom TF, Josefsson A, Erlich HA, Gyllensten U (1998) Recent origin of HLA-DRB1 alleles and implications for human evolution. Nature Genet. 18:237–242PubMedGoogle Scholar
  9. Bernatchez L (2001) The evolutionary history of Brown trout (Salmo trutta L.) inferred from phylogeographic, nested clade, and mismatch analyses of mitochondrial DNA variation. Evolution 55:351–379PubMedGoogle Scholar
  10. Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years. Mol. Ecol. 16:363–377Google Scholar
  11. Blanco JC, González JL (1992) Libro rojo de los vertebrados de España. Colección Técnica. ICONA, MadridGoogle Scholar
  12. Bouza C, Arias J, Castro J, Sanchez L, Martínez P (1999) Genetic structure of Brown trout, Salmo trutta L., at the southern limit of the distribution range of the anadromous form. Mol. Ecol. 8:1991–2001PubMedGoogle Scholar
  13. Brown JH, Jardtzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC (1993) 3-Dimensional structure of the human class-II histocompatibility antigen HLA-DR1. Nature 364:33–39PubMedGoogle Scholar
  14. Cano JM (2002) Diferenciación de poblaciones de trucha común (Salmo trutta L.). PhD thesis, Universidad de Oviedo, SpainGoogle Scholar
  15. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9:1657–1659PubMedGoogle Scholar
  16. Cortey M, García-Marín JL (2002) Evidence for phylogeographically informative sequence variation in the mitochondrial control region of Atlantic Brown trout. J. Fish Biol. 60:1058–1063Google Scholar
  17. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol. Evol. 15:290–295PubMedGoogle Scholar
  18. Crozier WW, Ferguson A (1986) Electrophoretic examination of the population structure of Brown trout, Salmo trutta L, from the Lough Neagh catchment, Northern-Ireland. J. Fish Biol. 28:459–477Google Scholar
  19. DiRienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc. Natl. Acad. Sci. USA 91:3166–3170Google Scholar
  20. Doiron S, Bernatchez L, Blier PU (2002) A comparative mitogenomic analysis of the potential adaptive value of arctic charr mtDNA introgression in brook charr populations (Salvelinus fontinalis Mitchill). Mol. Biol. Evol.19:1902–1909PubMedGoogle Scholar
  21. Ellegren H, Hartman G, Johansson M, Andersson L (1993) Major histocompatibility complex monomorphism and low levels of DNA fingerprinting variability in a reintroduced and rapidly expanding population of beavers. Proc. Natl. Acad. Sci. USA 90:8150–8153PubMedGoogle Scholar
  22. Elvira B (1996) Endangered freshwater fish of Spain. In: Kirchofer A, Hefti D (eds). Conservation of Endangered Freshwater Fish in Europe. Birkhäuser Verlag, Basel, pp. 55–61Google Scholar
  23. Erlandsson J, Rolán-Alvarez E, Johannesson K (1998) Migratory differences between ecotypes of the snail Littorina saxatilis on Galician rocky shores. Evol. Ecol. 12:913–924Google Scholar
  24. Estoup A, Largiader CR, Perrot E, Chourrout D (1996) Rapid one tube DNA extraction for reliable PCR detection of fish polymorphic markers and transgenes. Mol. Mar. Biol. Biotechnol. 5:295–298Google Scholar
  25. Fearnhead P, Donnelly PJ (2001) Estimating recombination rates from population genetic data. Genetics 159:1299–1318PubMedGoogle Scholar
  26. Felsenstein J (1984) Distance methods for inferring phylogenies: a justification. Evolution 38:16–24Google Scholar
  27. Ferguson A (1989) Genetic differences among Brown trout, Salmo trutta, stocks and their importance for the conservation and management of the species. Freshw. Biol. 21:35–46Google Scholar
  28. Frankel OH, Soulé ME (1981) Conservation and Evolution. Cambridge University Press, CambridgeGoogle Scholar
  29. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to Conservation Genetics. Cambridge University Press, CambridgeGoogle Scholar
  30. Franklin LR (1980) Evolutionary changes in small populations. In: Soulé ME (eds), Conservation Biology: An evolutionary-ecological perspective. Sinauer Associates, Sunderland, pp. 135–149Google Scholar
  31. García-Marín JL, Jorde PE, Ryman N, Utter F, Pla C (1991). Management implications of genetic differentiation between native and hatchery populations of Brown trout (Salmo trutta) in Spain. Aquaculture 95:235–249Google Scholar
  32. García-Marín JL, Sanz N, Pla C (1998) Proportions of native and introduced Brown trout in adjacent fished and unfished Spanish rivers. Conserv. Biol. 2:313–319Google Scholar
  33. García-Marín JL, Utter FM, Pla C (1999) Postglacial colonization of Brown trout in Europe based on distribution of allozyme variants. Heredity 82:46–56Google Scholar
  34. Garrigan D, Hedrick PW (2003) Detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 57:1707–1722PubMedGoogle Scholar
  35. Giuffra E, Bernatchez L, Guyomard R (1994) Mitochondrial control region and protein-coding genes sequence variation among phenotypic forms of Brown trout (Salmo trutta) from northern Italy. Mol. Ecol. 3:161–171PubMedGoogle Scholar
  36. Hansen MM, Loeschcke V (1996) Genetic differentiation among Danish Brown trout populations, as detected by RFLP analysis of PCR amplified mitochondrial DNA segments. J. Fish Biol. 48:422–436Google Scholar
  37. Heath DD, Busch C, Kelly J, Atagi DY (2002) Temporal change in genetic structure and effective population size in steelhead trout (Oncorhynchus mykiss). Mol. Ecol. 11:197–214PubMedGoogle Scholar
  38. Hedrick PW (1994) Evolutionary genetics of the Major Histocompatibility Complex. Am. Nat. 143:945–964Google Scholar
  39. Hedrick PW (2005) Genetics of populations. Jones and Bartlett, SudburyGoogle Scholar
  40. Hedrick PW, Hedgecock D, Hamelberg S (1995) Effective population size in winter-run chinook salmon. Conserv. Biol. 9:615–624Google Scholar
  41. Hedrick PW, Lee RN, Garrigan D (2002) Major histocompatibility complex variation in red wolves: evidence for common ancestry with coyotes and balancing selection. Mol. Ecol. 11:1905–1913PubMedGoogle Scholar
  42. Hedrick PW, Parker KM, Gutiérrez-Espeleta GA, Rattink A, Lievers K (2000) Major histocompatibility complex variation in the Arabian Oryx. Evolution 5:2145–2151Google Scholar
  43. Hedrick PW, Parker KM, Lee RN (2001) Using microsatellite and MHC variation to identify species, ESUs, and MUs in the endangered Sonoran topminnow. Mol. Ecol. 10:1399–1412PubMedGoogle Scholar
  44. Hedrick PW, Thomson G (1983) Evidence for balancing selection at HLA. Genetics 104: 449–456PubMedGoogle Scholar
  45. Hochberg Y (1989) A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75:800–802Google Scholar
  46. Hordvik I, Grimholt U, Fosse VM, Lie O, Endressen C (1993) Cloning and sequence analysis of cDNAs encoding the MHC class II beta chain in Atlantic salmon (Salmo salar). Immunogenetics 37:437–441PubMedGoogle Scholar
  47. Hudson RR (2001) Two-locus sampling distributions and their application. Genetics 159:1805–1817PubMedGoogle Scholar
  48. Hughes AL (1991) MHC polymorphism and the design of captive breeding programs. Conserv. Biol. 5:249–251Google Scholar
  49. Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex Class-I loci reveals overdominant selection. Nature 335:167–170PubMedGoogle Scholar
  50. Hughes AL, Nei M (1989) Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc. Natl. Acad. Sci. USA 86:958–962PubMedGoogle Scholar
  51. Hurst CD, Bartlett SE, Davidson WS, Bruce IJ (1999) The complete mitochondrial DNA sequence of the Atlantic salmon, Salmo salar. Gene 239:237–242PubMedGoogle Scholar
  52. Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: Inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53:1898–1914Google Scholar
  53. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed), Mammalian Protein Metabolism. Academic Press, New York, pp. 21–132Google Scholar
  54. Knox D, Lehmann K, Reddin DG, Verspoor E (2002) Genotyping of archival Atlantic salmon scales from northern Quebec and West Greenland using novel PCR primers for degraded mtDNA. J. Fish Biol. 60:266–270Google Scholar
  55. Koskinen MT, Haugen TO, Primmer CR (2002) Contemporary fisherian life-history evolution in small salmonid populations. Nature 419:826–830PubMedGoogle Scholar
  56. Kumar S, Tamura K, Jakobsen I, Nei M (2000) MEGA: Molecular Evolutionary Genetics Analysis Version 2.0. Pennsylvania State University, University Park, PAGoogle Scholar
  57. Laikre L, Antunes A, Apostolidis A, Berrebi P, Duguid A, Ferguson A, García-Marín JL, Guyomard R, Hansen MM, Hindar K, Koljonen ML, Largiader C, Martínez P, Nielsen E, Palm S, Ruzzante D, Ryman N, Triantaphyllidis C (1999) Conservation Genetic Management of Brown Trout (Salmo trutta) in Europe. Report by the Concerted action on identification, management and exploitation of genetic resources in the Brown trout (Salmo trutta) (“TROUTCONCERT”; EU FAIR CT97–3882).Google Scholar
  58. Laikre L, Ryman N (1996) Effects on intraspecific biodiversity from harvesting and enhancing natural populations. Ambio 25:504–509Google Scholar
  59. Landry C, Bernatchez L (2001) Comparative analysis of population structure across environments and geographical scales at major histocompatibility complex and microsatellite loci in Atlantic salmon (Salmo salar). Mol. Ecol. 10:2525–2539PubMedGoogle Scholar
  60. Langefors A, Lohm J, Grahn M, Andersen O, von Schantz T (2001a) Association between major histocompatibility complex class II B alleles and resistance to Aeromonas salmonicida in Atlantic salmon. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 268:479–485Google Scholar
  61. Langefors A, Lohm J, von Schantz T (2001b) Allelic polymorphism in MHC class II B in four populations of Atlantic salmon (Salmo salar). Immunogenetics 53:329–336Google Scholar
  62. Machordom A, García-Marín JL, Sanz N, Almodóvar A, Pla C (1999) Allozyme diversity in Brown trout (Salmo trutta) from Central Spain: Genetic consequences of restocking. Freshw. Biol. 41:707–717Google Scholar
  63. Machordom A, Suárez J, Almodóvar A, Bautista JM (2000) Mitochondrial haplotype variation and phylogeography of Iberian Brown trout populations. Mol. Ecol. 9:1325–1338Google Scholar
  64. Martinez JL, Moran P, Garcia-Vazquez E (1999) Dinucleotide repeat polymorphism at the SS4, SS6 and SS11 loci in Atlantic salmon (Salmo salar). Anim. Genet. 30:464–465PubMedGoogle Scholar
  65. Martinsohn JT, Sousa AB, Guethlein LA, Howard JC (1999) The gene conversion hypothesis of MHC evolution: a review. Immunogenetics 50:168–200PubMedGoogle Scholar
  66. McDonald JH, Kreitman M (1991) Adaptive protein evolution at the ADH locus in drosophila. Nature 351:652–654PubMedGoogle Scholar
  67. McVean G, Awadalla P, Fearnhead P (2002) A coalescent based method for detecting and estimating recombination from gene sequences. Genetics 160:1231–1241PubMedGoogle Scholar
  68. Miller HC, Lambert DM (2004a) Genetic drift outweighs balancing selection in shaping post-bottleneck major histocompatibility complex variation in New Zealand robins (Petroicidae). Mol. Ecol. 13:3709–3721Google Scholar
  69. Miller HC, Lambert DM (2004b) Gene duplication and gene conversion in class II MHC genes of New Zealand robins (Petroicidae). Immunogenetics 56:178–191Google Scholar
  70. Miller KM, Kaukinen KH, Beachman TD, Withler RE (2001) Geographic heterogeneity in natural selection on an MHC locus. Genetica 111:237–257PubMedGoogle Scholar
  71. Miller PS, Hedrick PW (1991) MHC polymorphism and the design of captive breeding programs: Simple solutions are not the answer. Conserv. Biol. 5:556–558Google Scholar
  72. Moritz C (1994) Defining “Evolutionarily significant units” for conservation. Trends Ecol. Evol. 9:373–375Google Scholar
  73. Moritz C (1999) Conservation units and translocations: strategies for conserving evolutionary processes. Hereditas 130:217–228Google Scholar
  74. Moritz C (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst. Biol. 51:238–254PubMedGoogle Scholar
  75. Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New YorkGoogle Scholar
  76. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3:418–426PubMedGoogle Scholar
  77. 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. 10:89–102PubMedGoogle Scholar
  78. O’Brien SJ, Roelke ME, Marker L, Newman A, Winkler CA, Meltzer D, Colly L, Evermann JF, Bush M, Wildt DE (1985) Genetic basis for species vulnerability in the cheetah. Science 227:1428–1434PubMedGoogle Scholar
  79. Ojanguren AF (2000) Efectos de factores ambientales y del tamaño de huevo sobre eficacia bioló gica en trucha común (Salmo trutta L.). PhD thesis, Universidad de Oviedo, SpainGoogle Scholar
  80. Olsen KH, Grahn M, Lohm J, Langefors A (1998) MHC and kin discrimination in juvenile Arctic charr, Salvelinus alpinus (L.). Anim. Behav. 56:319–327PubMedGoogle Scholar
  81. Orita M, Iwahana H, Kanazawa H, Hayashi K, Sekiya T (1989) Detection of polymorphisms of human DNA by gel electrophoresis as single-strand conformation polymorphisms. Proc. Natl. Acad. Sci. USA 86:2766–2770PubMedGoogle Scholar
  82. Paterson S, Wilson K, Pemberton JM (1998) Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.). Proc. Natl. Acad. Sci. USA 95:3714–3719PubMedGoogle Scholar
  83. Posada D, Crandall KA (2002) The effect of recombination on the accuracy of phylogeny estimation. J. Mol. Evol. 54:396–402PubMedGoogle Scholar
  84. Posada D, Crandall KA, Templeton AR (2000) GeoDis: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol. Ecol. 9:487–488PubMedGoogle Scholar
  85. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol. Biol. Evol. 19:2092–2100PubMedGoogle Scholar
  86. Raymond M, Rousset F (1995) GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86:248–249Google Scholar
  87. Reyes-Gavilán FG, Garrido R, Nicieza AG, Toledo M, Braña F (1995) Variability in growth, density and age structure of Brown trout populations under contrasting environmental and managerial conditions. In: Harper DM, Ferguson ADJ (eds). The ecological basis for river management. John Wiley & Sons Ltd., New YorkGoogle Scholar
  88. Richman AD, Herrera LG, Nash D (2003a) Evolution of MHC class II E beta diversity within the genus Peromyscus. Genetics164:289–297CrossRefGoogle Scholar
  89. Richman AD, Herrera LG, Nash D, Schierup MH (2003b) Relative roles of mutation and recombination in generating allelic polymorphism at an MHC class II locus in Peromyseus maniculatus. Genet. Res. 82:89–99Google Scholar
  90. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedGoogle Scholar
  91. Ryman N (1983) Patterns of distribution of biochemical genetic variation in salmonids: differences between species. Aquaculture 33:1–21Google Scholar
  92. Schierup MH, Hein J (2000) Consequences of recombination on traditional phylogenetic analysis. Genetics 156:879–891PubMedGoogle Scholar
  93. Schneider S, Roessli D, Excoffier L (2000) Arlequin version 2.000: A software for population genetics data analysis. Genetic and Biomedical Laboratory, University of Geneva, GenevaGoogle Scholar
  94. Seddon JM, Baverstock PR (1999) Variation on islands: major histocompatibility complex (Mhc) polymorphism in populations of the Australian bush rat. Mol. Ecol. 8:2071–2079PubMedGoogle Scholar
  95. Shrimpton JM, Heath DD (2003) Census vs. effective population size in chinook salmon: large- and small-scale environmental perturbation effects. Mol. Ecol. 12:2571–2583PubMedGoogle Scholar
  96. Shriner D, Nickle DC, Jensen MA, Mullins JI (2003) Potential impact of recombination on sitewise approaches for detecting positive natural selection. Genet. Res. 81:115–121PubMedGoogle Scholar
  97. Shum BP, Guethlein L, Flodin LR, Adkison MA, Hedrick RP, Nehring RB, Stet RJM, Secombes C, Parham P (2001) Modes of salmonid MHC class I and II evolution differ from the primate paradigm. J. Immunol. 66:3297–3308Google Scholar
  98. Slade RW (1992) Limited MHC polymorphism in the southern elephant seal: implications for MHC evolution and marine mammal population biology. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 249:163–171Google Scholar
  99. Slettan A, Olsaker I, Lie O (1995) Atlantic salmon, Salmo salar, microsatellites at the SSOSL25, SSOSL85, SSOSL311, SSOSL417 loci. Anim. Genet. 26:281–282PubMedGoogle Scholar
  100. Smulders MJM, Snoek LB, Booy G, Vosman B (2003) Complete loss of MHC genetic diversity in the Common Hamster (Cricetus cricetus) population in The Netherlands. Consequences for conservation strategies. Conserv. Genet. 4:441–451Google Scholar
  101. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  102. Takahata N, Satta Y (1998) Footprints of intragenic recombination at HLA loci. Immunogenetics 47:430–441PubMedGoogle Scholar
  103. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data.III. Cladogram estimation. Genetics 132:619–633PubMedGoogle Scholar
  104. Templeton AR, Routman E, Phillips CA (1995) Separating population structure from population history: a cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the tiger salamander, Ambystoma tigrinum. Genetics 140:767–782PubMedGoogle Scholar
  105. Templeton AR, Sing CF (1993) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. IV. Nested analyses with cladogram uncertainty and recombination. Genetics 134:659–669PubMedGoogle Scholar
  106. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24:4876–4882Google Scholar
  107. Vrijenhoek RC, Leberg PL (1991) Let’s not throw the baby out with the bathwater: a comment on management for MHC diversity in captive populations. Conserv. Biol. 5:252–254Google Scholar
  108. Waldick RC, Kraus SS, Brown M, White BN (2002) Evaluating the effects of historic bottleneck events: an assessment of microsatellite variability in the endangered, North Atlantic right whale. Mol. Ecol. 11:2241–2250PubMedGoogle Scholar
  109. Waples RS (1991) Pacific salmon, Oncorhyncus spp., and the definition of “species” under the endangered species act. Mar. Fish. Rev. 53:11–22Google Scholar
  110. Weber DS, Stewart BS, Schienman J, Lehman N (2004) Major histocompatibility complex variation at three class II loci in the northern elephant seal. Mol. Ecol. 13: 711–718PubMedGoogle Scholar
  111. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  1. 1.Departamento de Bioquímica, Genética e Inmunología, Facultad de BiologíaUniversidad de VigoVigoSpain
  2. 2.Area de Genética, Edificio de Ciencias ExperimentalesCampus UniversitarioVigoSpain

Personalised recommendations