, Volume 707, Issue 1, pp 29–45 | Cite as

Identification and conservation of remnant genetic resources of brown trout in relict populations from Western Mediterranean streams

  • M. Vera
  • J. L. Garcia-Marin
  • P. Martinez
  • R. M. Araguas
  • C. Bouza
Primary Research Paper


Brown trout is a cold-adapted freshwater species with restricted distribution to headwater streams in rivers of the South European peninsulas, where populations are highly vulnerable because Mediterranean regions are highly sensitive to the global climatic warming. Moreover, these populations are endangered due to the introgressive hybridization with cultured stocks. Individuals from six remnant populations in Western Mediterranean rivers were sequenced for the complete mitochondrial DNA control region and genotyped for 11 nuclear markers. Three different brown trout lineages were present in the studied region. Significant genetic divergence was observed among locations and a strong effect of genetic drift was suggested. An important stocking impact (close to 25%) was detected in the zone. Significant correlations between mitochondrial-based rates of hatchery introgression and water flow variation suggested a higher impact of stocked females in unstable habitats. In spite of hatchery introgression, all populations remained highly differentiated, suggesting that native genetic resources are still abundant. However, climatic predictions indicated that suitable habitats for the species in these rivers will be reduced and hence trout populations are highly endangered and vulnerable. Thus, management policies should take into account these predictions to design upstream refuge areas to protect remnant native trout in the region.


Mediterranean brown trout Environmental change Introgression Genetic variability Stocking impact Relict populations 


  1. Allendorf, F. W., R. F. Leary, P. Spruell & J. K. Wenburg, 2001. The problems with hybrids: setting conservation guidelines. Trends in Ecology & Evolution 16: 613–622.CrossRefGoogle Scholar
  2. Allendorf, F. W., R. F. Leary, N. P. Hitt, K. L. Knudsen, L. L. Lundquist & P. Spruell, 2004. Intercrosses and the US Endangered Species Act: should hybridized populations be included as Westslope cutthroat trout? Conservation Biology 18: 1203–1213.CrossRefGoogle Scholar
  3. Almodovar, A., G. G. Nicola, B. Elvira & J. L. Garcia-Marin, 2006. Introgression variability among Iberian brown trout evolutionary significant units: the influence of local management and environmental features. Freshwater Biology 51: 1175–1187.CrossRefGoogle Scholar
  4. Almodovar, A., G. G. Nicola, D. Ayllon & B. Elvira, 2012. Global warming threatens the persistence of Mediterranean brown trout. Global Change Biology 18: 1549–1560.CrossRefGoogle Scholar
  5. Alonso, C., D. Garcia De Jalon, J. Alvarez & J. Gortazar, 2011. A large-scale approach can help detect general processes driving the dynamics of brown trout populations in extensive areas. Ecology of Freshwater Fish 20: 449–460.CrossRefGoogle Scholar
  6. Antunes, A., A. R. Templeton, R. Guyomard & P. Alexandrino, 2002. The role of nuclear genes in intraspecific evolutionary inference: genealogy of the transferrin gene in the brown trout. Molecular Biology and Evolution 19: 1272–1287.PubMedCrossRefGoogle Scholar
  7. Aparicio, E., E. Garcia-Berthou, R. M. Araguas, P. Martinez & J. L. Garcia-Marin, 2005. Body pigmentation pattern to assess introgression by hatchery stocks in native Salmo trutta from Mediterranean streams. Journal of Fish Biology 67: 931–949.CrossRefGoogle Scholar
  8. Apostolidis, A. P., M. J. Madeira, M. M. Hansen & A. Machordom, 2008. Genetic structure and demographic history of brown trout (Salmo trutta) populations from the southern Balkans. Freshwater Biology 53: 1555–1566.CrossRefGoogle Scholar
  9. Araguas, R. M., N. Sanz, R. Fernandez, F. M. Utter, C. Pla & J. L. Garcia-Marin, 2008. Genetic refuges for a self-sustained fishery: experience in wild brown trout populations in the eastern Pyrenees. Ecology of Freshwater Fish 17: 610–616.CrossRefGoogle Scholar
  10. Araguas, R. M., N. Sanz, R. Fernandez, F. M. Utter, C. Pla & J. L. Garcia-Marin, 2009. Role of genetic refuges in the restoration of native gene pools of brown trout. Conservation Biology 23: 871–878.PubMedCrossRefGoogle Scholar
  11. Araujo, M. B., W. Thuiller & R. G. Pearson, 2006. Climate warming and the decline of amphibians and reptiles in Europe. Journal of Biogeography 33: 1712–1728.CrossRefGoogle Scholar
  12. Arias, J., L. Sanchez & P. Martinez, 1995. Low stocking incidence in brown trout populations from northwestern Spain monitored by LDH-5* diagnostic marker. Journal of Fish Biology 47: 170–176.CrossRefGoogle Scholar
  13. Baric, S., A. Riedl, A. Meraner, N. Medgyesy, R. Lackner, B. Pelster & J. Dalla-Via, 2010. Alpine headwater streams as reservoirs of remnant populations of the Danubian clade brown trout. Freshwater biology 55: 866–880.CrossRefGoogle Scholar
  14. Beaugrand, G., P. C. Reid, F. Ibanez, J. A. Lindley & M. Edwards, 2002. Reorganization of North Atlantic marine copepod biodiversity and climate. Science 296: 1692.PubMedCrossRefGoogle Scholar
  15. 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: 351–379.PubMedGoogle Scholar
  16. Berrebi, P., C. Poteaux, M. Fissier & G. Cattaneo-Berrebi, 2000. Stocking impact and allozyme diversity in brown trout from Mediterranean southern France. Journal of Fish Biology 56: 949–960.CrossRefGoogle Scholar
  17. Borgstrom, R. & J. Museth, 2005. Accumulated snow and summer temperature—critical factors for recruitment to high mountain populations of brown trout (Salmo trutta L.). Ecology of Freshwater Fish 14: 375–384.CrossRefGoogle Scholar
  18. Bouza, C., J. Arias, J. Castro, L. Sanchez & P. Martinez, 1999. Genetic structure of brown trout, Salmo trutta L., at the southern limit of the distribution range of the anadromous form. Molecular Ecology 8: 1991–2001.PubMedCrossRefGoogle Scholar
  19. Bouza, C., J. Castro, L. Sanchez & P. Martinez, 2001. Allozymic evidence of parapatric differentiation of brown trout (Salmo trutta L.) within an Atlantic river basin of the Iberian Peninsula. Molecular Ecology 10: 1455–1469.PubMedCrossRefGoogle Scholar
  20. Buisson, L., W. Thuiller, S. Lek, P. Lim & G. Grenouillet, 2008. Climate change hastens the turnover of stream fish assemblages. Global Change Biology 14: 2232–2248.CrossRefGoogle Scholar
  21. Caballero, A. & S. T. Rodriguez-Ramilo, 2010. A new method for the partition of allelic diversity within and between subpopulations. Conservation Genetics 11: 2219–2229.CrossRefGoogle Scholar
  22. Corander, J. & P. Marttinen, 2006. Bayesian identification of admixture events using multilocus molecular markers. Molecular Ecology 15: 2833–2843.PubMedCrossRefGoogle Scholar
  23. Cortey, M. & J. L. Garcia-Marin, 2002. Evidence for phylogeographically informative sequence variation in the mitochondrial control region of Atlantic brown trout. Journal of Fish Biology 60: 1058–1063.CrossRefGoogle Scholar
  24. Cortey, M., C. Pla & J. L. Garcia-Marin, 2004. Historical biogeography of Mediterranean trout. Molecular Phylogenetics and Evolution 33: 831–844.PubMedCrossRefGoogle Scholar
  25. Cortey, M., M. Vera, C. Pla & J. L. Garcia-Marin, 2009. Northern and southern expansions of Atlantic brown trout (Salmo trutta) populations during the Pleistocene. Biological Journal of the Linnean Society 97: 904–917.CrossRefGoogle Scholar
  26. Daufresne, M., M. C. Roger, H. Capra & N. Lamouroux, 2004. Long-term changes within the invertebrate and fish communities of the Upper Rhone River: effects of climatic factors. Global Change Biology 10: 124–140.CrossRefGoogle Scholar
  27. De Luis, M., J. C. Gonzalez-Hidalgo, L. A. Longares & P. Stepanek, 2009. Seasonal precipitation trends in the Mediterranean Iberian Peninsula in second half of 20th century. International Journal of Climatology 29: 1312–1323.CrossRefGoogle Scholar
  28. Durance, I. & S. J. Ormerod, 2009. Trends in water quality and discharge confound long-term warming effects on river macroinvertebrates. Freshwater Biology 54: 388–405.CrossRefGoogle Scholar
  29. Elmousadik, A. & R. J. Petit, 1996. High level of genetic differentiation for allelic richness among populations of the argan tree Argania spinosa (L) Skeels endemic to Morocco. Theoretical and Applied Genetics 92: 832–839.CrossRefGoogle Scholar
  30. Estoup, A., P. Presa, F. Krieg, D. Vaiman & R. Guyomard, 1993. CT)(n) and (GT)(n) microsatellites: a new class of genetic markers for Salmo trutta L (brown trout). Heredity 71: 488–496.PubMedCrossRefGoogle Scholar
  31. Excoffier, L., P. E. Smouse & J. M. Quattro, 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479–491.PubMedGoogle Scholar
  32. Frankham, R., 2005. Genetics and extinction. Biological Conservation 126: 131–140.CrossRefGoogle Scholar
  33. Frankham, R., J. D. Ballou & D. A. Briscoe, 2002. Introduction to conservation genetics. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  34. Fumagalli, L., A. Snoj, D. Jesensek, F. Balloux, T. Jug, O. Duron, F. Brossier, A. J. Crivelli & P. Berrebi, 2002. Extreme genetic differentiation among the remnant populations of marble trout (Salmo marmoratus) in Slovenia. Molecular Ecology 11: 2711–2716.PubMedCrossRefGoogle Scholar
  35. Garcia-Marin, J. L. & C. Pla, 1996. Origins and relationships of native populations of Salmo trutta (brown trout) in Spain. Heredity 77: 313–323.CrossRefGoogle Scholar
  36. Garcia-Marin, J. L., P. E. Jorde, N. Ryman, F. Utter & C. Pla, 1991. Management implications of genetic differentiation between native and hatchery populations of brown trout (Salmo trutta) in Spain. Aquaculture 95: 235–249.CrossRefGoogle Scholar
  37. Garcia-Marin, J. L., N. Sanz & C. Pla, 1998. Proportions of native and introduced brown trout in adjacent fished and unfished Spanish rivers. Conservation Biology 12: 313–319.CrossRefGoogle Scholar
  38. Garcia-Marin, J. L., F. M. Utter & C. Pla, 1999a. Postglacial colonization of brown trout in Europe based on distribution of allozyme variants. Heredity 82: 46–56.CrossRefGoogle Scholar
  39. Garcia-Marin, J. L., N. Sanz & C. Pla, 1999b. Erosion of the native genetic resources of brown trout in Spain. Ecology of Freshwater Fish 8: 151–158.CrossRefGoogle Scholar
  40. Gibelin, A. L. & M. Deque, 2003. Anthropogenic climate change over the Mediterranean region simulated by a global variable resolution model. Climate Dynamics 20: 327–339.Google Scholar
  41. Goudet, J., 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3) [available on internet at http://www.unil.ch/izea/softwares/fstat.html].
  42. Grant, E. H. C., W. H. Lowe & W. F. Fagan, 2007. Living in the branches: population dynamics and ecological processes in dendritic networks. Ecology Letters 10: 165–175.CrossRefGoogle Scholar
  43. Hansen, M. M., 2002. Estimating the long-term effects of stocking domesticated trout into wild brown trout (Salmo trutta) populations: an approach using microsatellite DNA analysis of historical and contemporary samples. Molecular Ecology 11: 1003–1015.PubMedCrossRefGoogle Scholar
  44. Hansen, M. M., D. Bekkevold, L. F. Jensen, K. L. D. Mensberg & E. E. Nielsen, 2006. Genetic restoration of a stocked brown trout Salmo trutta population using microsatellite DNA analysis of historical and contemporary samples. Journal of Applied Ecology 43: 669–679.CrossRefGoogle Scholar
  45. Hari, R. E., D. M. Livingstone, R. Siber, P. Burkhardt-Holm & H. Guttinger, 2006. Consequences of climatic change for water temperature and brown trout populations in Alpine rivers and streams. Global Change Biology 12: 10–26.CrossRefGoogle Scholar
  46. Hijmans, R. J., S. E. Cameron, J. L. Parra, P. G. Jones & A. Jarvis, 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25: 1965–1978.CrossRefGoogle Scholar
  47. Hurt, C. & P. Hedrick, 2004. Conservation genetics in aquatic species: general approaches and case studies in fishes and springsnails of arid lands. Aquatic Sciences 66: 402–413.CrossRefGoogle Scholar
  48. Jensen, L. F., M. M. Hansen, J. Carlsson, V. Loeschcke & K. L. D. Mensberg, 2005. Spatial and temporal genetic differentiation and effective population size of brown trout (Salmo trutta, L.) in small Danish rivers. Conservation Genetics 6: 615–621.CrossRefGoogle Scholar
  49. Jug, T., P. Berrebi & A. Snoj, 2005. Distribution of non-native trout in Slovenia and their introgression with native trout populations as observed through microsatellite DNA analysis. Biological Conservation 123: 381–388.CrossRefGoogle Scholar
  50. Laikre, L., A. Antunes, A. Apostolidis,P. Berrebi, A. Duguid, A. Ferguson, J. L. Garcia-Marin, R. Guyomard, M.M. Hansen, K. Hindar, M. L. Koljonen, C. Largiader, P. Martinez, E. E. Nielsen, S. Palm, D. Ruzzante, N. Ryman & C. Triantaphyllidis, 1999. Conservation Genetic Management of Brown trout (Salmo trutta L.) 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). ISBN 87-987732-0-8 1999.Google Scholar
  51. Langan, S. J., L. Johnston, M. J. Donaghy, A. F. Youngson, D. W. Hay & C. Soulsby, 2001. Variation in river water temperatures in an upland stream over a 30-year period. Science of the Total Environment 265: 195–207.PubMedCrossRefGoogle Scholar
  52. Langella, O., 2002. POPULATIONS 1.2.26. Logiciel de Génétique de populations.Laboratoire populations, génétique et évolution. CNRS UPR 9034.Gif-sur-Yvette. France [available on internet at http://www.bioinformatics.org/project/?group_id=84].
  53. Lobon-Cervia, J. & E. Mortensen, 2005. Population size in stream-living juveniles of lake-migratory brown trout Salmo trutta L.: the importance of stream discharge and temperature. Ecology of Freshwater Fish 14: 394–401.CrossRefGoogle Scholar
  54. Lobon-Cervia, J. & P. A. Rincon, 2004. Environmental determinants of recruitment and their influence on the population dynamics of stream-living brown trout Salmo trutta. Oikos 105: 641–646.CrossRefGoogle Scholar
  55. Luikart, G., F. W. Allendorf, J. M. Cornuet & W. B. Sherwin, 1998. Distortion of allele frequency distributions provides a test for recent population bottlenecks. Journal of Heredity 89: 238–247.PubMedCrossRefGoogle Scholar
  56. Machordom, A., J. Suarez, A. Almodovar & J. M. Bautista, 2000. Mitochondrial haplotype variation and phylogeography of Iberian brown trout populations. Molecular Ecology 9: 1325–1338.CrossRefGoogle Scholar
  57. Martinez, P., J. Arias, J. Castro & L. Sanchez, 1993. Differential stocking incidence in brown trout (Salmo trutta) populations from Northwestern Spain. Aquaculture 114: 203–216.CrossRefGoogle Scholar
  58. Martinez, P., C. Bouza, J. Castro, M. Hermida, B. G. Pardo & L. Sanchez, 2007. Analysis of a secondary contact between divergent lineages of brown trout Salmo trutta L. from Duero basin using microsatellites and mtDNA RFLPs. Journal of Fish Biology 71: 195–213.CrossRefGoogle Scholar
  59. McMeel, O. M., E. M. Hoey & A. Ferguson, 2001. Partial nucleotide sequences, and routine typing by polymerase chain reaction-restriction fragment length polymorphism, of the brown trout (Salmo trutta) lactate dehydrogenase, LDH-C1*90 and *100 alleles. Molecular Ecology 10: 29–34.PubMedCrossRefGoogle Scholar
  60. Meldgaard, T., A. J. Crivelli, D. Jesensek, G. Poizat, J. F. Rubin & P. Berrebi, 2007. Hybridization mechanisms between the endangered marble trout (Salmo marmoratus) and the brown trout (Salmo trutta) as revealed by in-stream experiments. Biological Conservation 136: 602–611.CrossRefGoogle Scholar
  61. Mezzera, M. & C. R. Largiader, 2001. Evidence for selective angling of introduced trout and their hybrids in a stocked brown trout population. Journal of Fish Biology 59: 287–301.CrossRefGoogle Scholar
  62. Nei, M., 1978. Estimation of average heterozigosity and genetic distance from a small number of individuals. Genetics 89: 583–590Google Scholar
  63. Nei, M., 1987. Molecular evolutionary genetics. Columbia University Press, New York.Google Scholar
  64. Nei, M. & F. Tajima, 1981. DNA polymorphism detectable by restriction endonucleases. Genetics 97: 145–163.PubMedGoogle Scholar
  65. Nicola, G. G. & A. Almodovar, 2002. Reproductive traits of stream-dwelling brown trout Salmo trutta in contrasting neighbouring rivers of central Spain. Freshwater Biology 47: 1353–1365.CrossRefGoogle Scholar
  66. Nicola, G. G., A. Almodovar, B. Jonsson & B. Elvira, 2008. Recruitment variability of resident brown trout in peripheral populations from southern Europe. Freshwater Biology 53: 2364–2374.CrossRefGoogle Scholar
  67. Ordeix, C., C. Sola, M. Bardina, A. Cassamitjana & A. Munne, 2010. Els peixos dels rius i zones humides de Catalunya. Agencia Catalana de l’Aigua. Departament de Medi Ambient i Habitatge, Generalitat de Catalunya.Google Scholar
  68. Ormerod, S., 2009. Climate change, river conservation and the adaptation challenge. Aquatic Conservation: Marine and Freshwater Ecosystems 19: 609–613.CrossRefGoogle Scholar
  69. Ostergaard, S., M. M. Hansen, V. Loeschcke & E. E. Nielsen, 2003. Long-term temporal changes of genetic composition in brown trout (Salmo trutta L.) populations inhabiting an unstable environment. Molecular Ecology 12: 3123–3135.PubMedCrossRefGoogle Scholar
  70. Page, R. D. M., 1996. TreeView: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12: 357–358.PubMedGoogle Scholar
  71. Parmesan, C., 2007. Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Global Change Biology 13: 1860–1872.CrossRefGoogle Scholar
  72. Perez-Figueroa, A., M. Saura, J. Fernandez, M. A. Toro & A. Caballero, 2009. METAPOP-A software for the management and analysis of subdivided populations in conservation programs. Conservation Genetics 10: 1097–1099.CrossRefGoogle Scholar
  73. Perry, A. L., P. J. Low, J. R. Ellis & J. D. Reynolds, 2005. Climate change and distribution shifts in marine fishes. Science 308: 1912.PubMedCrossRefGoogle Scholar
  74. Piry, S., G. Luikart & J. M. Cornuet, 1999. BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity 90: 502–503.CrossRefGoogle Scholar
  75. Poteaux, C., P. Berrebi & F. Bonhomme, 2001. Allozymes, mtDNA and microsatellites study introgression in a stocked trout population in France. Reviews in Fish Biology and Fisheries 10: 281–292.CrossRefGoogle Scholar
  76. Presa, P. & R. Guyomard, 1996. Conservation of microsatellites in three species of salmonids. Journal of Fish Biology 49: 1326–1329.Google Scholar
  77. Presa, P., B. G. Pardo, P. Martinez & L. Bernatchez, 2002. Phylogeographic congruence between mtDNA and rDNA ITS markers in brown trout. Molecular Biology and Evolution 19: 2161–2175.PubMedCrossRefGoogle Scholar
  78. Pritchard, J. K., M. Stephens & P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.PubMedGoogle Scholar
  79. Pujolar, J. M., S. Vincenzi, L. Zane, D. Jesensek, G. A. De Leo & A. J. Crivelli, 2011. The effect of recurrent floods on genetic composition of marble trout populations. PLoS ONE 6: e23822.PubMedCrossRefGoogle Scholar
  80. Ragab, R. & C. Prudhomme, 2002. SW–Soil and Water* 1: climate change and water resources management in arid and semi-arid regions: prospective and challenges for the 21st century. Biosystems Engineering 81: 3–34.CrossRefGoogle Scholar
  81. Rijnsdorp, A. D., M. A. Peck, G. H. Engelhard, C. Mollmann & J. K. Pinnegar, 2009. Resolving the effect of climate change on fish populations. ICES Journal of Marine Science 66: 1570.CrossRefGoogle Scholar
  82. Rohlf, F., 1993. NTSYS-pc. Numerical taxonomy and multivariate analysis system, Version 2.1. Setauket, New York.Google Scholar
  83. Rousset, F., 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145: 1219–1228.PubMedGoogle Scholar
  84. Rousset, F., 2008. GENEPOP ‘ 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources 8: 103–106.PubMedCrossRefGoogle Scholar
  85. Ruzzante, D. E., M. M. Hansen & D. Meldrup, 2001. Distribution of individual inbreeding coefficients, relatedness and influence of stocking on native anadromous brown trout (Salmo trutta) population structure. Molecular Ecology 10: 2107–2128.PubMedCrossRefGoogle Scholar
  86. Ruzzante, D. E., M. M. Hansen, D. Meldrup & K. M. Ebert, 2004. Stocking impact and migration pattern in an anadromous brown trout (Salmo trutta) complex: where have all the stocked spawning sea trout gone? Molecular Ecology 13: 1433–1445.PubMedCrossRefGoogle Scholar
  87. Sambrook, J., E. F. Fritsch & T. Maniatis, 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, New York.Google Scholar
  88. Sanz, N., R. Fernandez-Cebrian, F. Casals, R. M. Araguas & J. L. Garcia-Marin, 2011. Dispersal and demography of brown trout, Salmo trutta, inferred from population and family structure in unstable Mediterranean streams. Hydrobiologia. doi:10.1007/s10750-011-0708-2.
  89. Sanz, N., J. L. Garcia-Marin & C. Pla, 2000. Divergence of brown trout (Salmo trutta) within glacial refugia. Canadian Journal of Fisheries and Aquatic Sciences 57: 2201–2210.CrossRefGoogle Scholar
  90. Sanz, N., J. L. Garcia-Marin & C. Pla, 2002. Managing fish populations under mosaic relationships. The case of brown trout (Salmo trutta) in peripheral Mediterranean populations. Conservation Genetics 3: 385–400.CrossRefGoogle Scholar
  91. Sanz, N., M. Cortey, C. Pla & J. L. Garcia-Marin, 2006. Hatchery introgression blurs ancient hybridization between brown trout (Salmo trutta) lineages as indicated by complementary allozymes and mtDNA markers. Biological Conservation 130: 278–289.CrossRefGoogle Scholar
  92. Sanz, N., R. M. Araguas, R. Fernandez, M. Vera & J. L. Garcia-Marin, 2009. Efficiency of markers and methods for detecting hybrids and introgression in stocked populations. Conservation Genetics 10: 225–236.CrossRefGoogle Scholar
  93. Schneider, S., D. Roessli & L. Excoffier, 2000. Arlequin, Version 2.000: a software for population genetics data analysis. G.A.B. Laboratory. University of Geneva, Switzerland, Geneva.Google Scholar
  94. Snoj, A., E. Melki, S. Susnik, S. Muhamedagi & P. Dov, 2002. DNA phylogeny supports revised classification of Salmothymus obtusirostris. Biological Journal of the Linnean Society 77: 399–411.CrossRefGoogle Scholar
  95. Snoj, A., I. Bogut & S. Susnik, 2008. Evidence of a genetically distinct population of Vrljika softmouth trout Salmo obtusirostris Heckel evolved by vicariance. Journal of Fish Biology 72: 1945–1959.CrossRefGoogle Scholar
  96. Sonstebo, J. H., R. Borgstrom & M. Heun, 2008. High genetic introgression in alpine brown trout (Salmo trutta L.) populations from Hardangervidda, Norway. Ecology of Freshwater Fish 17: 174–183.CrossRefGoogle Scholar
  97. Suarez, J., J. M. Bautista, A. Almodovar & A. Machordom, 2001. Evolution of the mitochondrial control region in Palaearctic brown trout (Salmo trutta) populations: the biogeographical role of the Iberian Peninsula. Heredity 87: 198–206.PubMedCrossRefGoogle Scholar
  98. Sumner, G. N., R. Romero, V. Homar, C. Ramis, S. Alonso & E. Zorita, 2003. An estimate of the effects of climate change on the rainfall of Mediterranean Spain by the late twenty first century. Climate Dynamics 20: 789–805.Google Scholar
  99. Susnik, S., A. Snoj, I. F. Wilson, D. Mrdak & S. Weiss, 2007. Historical demography of brown trout (Salmo trutta) in the Adriatic drainage including the putative S. letnica endemic to Lake Ohrid. Molecular Phylogenetics and Evolution 44: 63–76.PubMedCrossRefGoogle Scholar
  100. Tamura, K., J. Dudley, M. Nei & S. Kumar, 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596–1599.PubMedCrossRefGoogle Scholar
  101. Thibault, I, R. D. Hedger, H. Crepeau, C. Audet & J. J. Dodson, 2010. Abiotic variables accounting for presence of the exotic rainbow trout (Oncorhynchus mykiss) in Eastern Quebec Rivers. Knowledge and Management of Aquatic Ecosystems 398: 5(16 pp).Google Scholar
  102. Trigo, R. M., D. Pozo-Vazquez, T. J. Osborn, Y. Castro-Diez, S. Gamiz-Fortis & M. J. Esteban-Parra, 2004. North Atlantic Oscillation influence on precipitation, river flow and water resources in the Iberian Peninsula. International Journal of Climatology 24: 925–944.CrossRefGoogle Scholar
  103. Van Vuuren, D. P., M. Meinshausen, G. K. Plattner, F. Joos, K. M. Strassmann, S. J. Smith, T. M. L. Wigley, S. C. B. Raper, K. Riahi, F. de la Chesnaye, M. G. J. den Elzen, J. Fujino, K. Jiang, N. Nakicenovic, S. Paltsev & J. M. Reilly, 2008. Temperature increase of 21st century mitigation scenarios. Proceedings of the National Academy of Sciences of the United States of America 105: 15258–15262.PubMedCrossRefGoogle Scholar
  104. Vera, M., M. Cortey, N. Sanz & J. L. Garcia-Marin, 2010a. Maintenance of an endemic lineage of brown trout (Salmo trutta) within the Duero river basin. Journal of Zoological Systematics and Evolutionary Research 48: 181–187.CrossRefGoogle Scholar
  105. Vera, M., N. Sanz, M. M. Hansen, A. Almodovar & J. L. Garcia-Marin, 2010b. Population and family structure of brown trout, Salmo trutta, in a Mediterranean stream. Marine and Freshwater Research 61: 672–681.CrossRefGoogle Scholar
  106. Vera, M., I. Sourinejad, C. Bouza, R. Vilas, A. Pino-Querido, M. R. Kalbassi & P. Marinez, 2011. Phylogeography, genetic structure and conservation of the endangered Caspian brown trout, Salmo trutta caspius (Kessler, 1877), from Iran. Hydrobiologia 664: 51–67.CrossRefGoogle Scholar
  107. Vilas, R., C. Bouza, J. Castro, A. López & P. Martinez, 2010. Management units of brown trout from Galicia (NW: Spain) based on spatial genetic structure analysis. Conservation Genetics 11: 897–906.CrossRefGoogle Scholar
  108. Vollestad, L. A. & E. M. Olsen, 2008. Non-additive effects of density-dependent and density-independent factors on brown trout vital rates. Oikos 117: 1752–1760.CrossRefGoogle Scholar
  109. Walsh, P. S., D. A. Metzger & R. Higuchi, 1991. Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10: 506–513.PubMedGoogle Scholar
  110. Weiss, S. & S. Schmutz, 1999. Performance of hatchery-reared brown trout and their effects on wild fish in two small Austrian streams. Transactions of the American Fisheries Society 128: 302–316.CrossRefGoogle Scholar
  111. Wigley, T. M. L. & S. C. B. Raper, 2001. Interpretation of high projections for global-mean warming. Science 293: 451–454.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • M. Vera
    • 1
    • 2
  • J. L. Garcia-Marin
    • 2
  • P. Martinez
    • 1
  • R. M. Araguas
    • 2
  • C. Bouza
    • 1
  1. 1.Departamento de Genética, Facultad de VeterinariaUniversidad de Santiago de CompostelaLugoSpain
  2. 2.Laboratori d’Ictiologia Genètica, Departament of Biology, Faculty of SciencesUniversity of GironaGironaSpain

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