, Volume 826, Issue 1, pp 209–231 | Cite as

Brown trout (Salmo trutta L.) high genetic diversity around the Tyrrhenian Sea as revealed by nuclear and mitochondrial markers

  • P. BerrebiEmail author
  • V. Caputo Barucchi
  • A. Splendiani
  • S. Muracciole
  • A. Sabatini
  • F. Palmas
  • C. Tougard
  • M. Arculeo
  • S. Marić
Primary Research Paper


The brown trout (Salmo trutta L.) is widely distributed all around Europe but its natural diversity is threatened by massive stocking with Atlantic domestic strains. Describing the remaining natural genetic diversity and the proportion of domestic hatchery strains in rivers is a prerequisite for smart conservation. The high genetic diversity of brown trout populations around the Tyrrhenian Sea is well known. Use of twelve microsatellites has allowed description of the natural genetic structure of populations and detection of the consequences of stocking. Mitochondrial DNA control region sequences and the LDH-C1* gene enabled placement of each population into one of the six mitochondrial and two allozymic known evolutionary lineages. The Corsican populations showed low intra-population genetic diversity but an exceptionally high level of inter-population differentiation. More southern Tyrrhenian regions exhibited opposite pattern of diversity, partly due to the Atlantic domestic introgression. Globally, the natural structure outlines two north–south clines: high inter-population differentiation and predominance of the Adriatic lineage in the north, but lower inter-population differentiation and the presence of the natural Atlantic lineage in the south. In addition, the Tyrrhenian region is the contact zone between the widespread Adriatic lineage and a local natural Atlantic lineage probably coming from North Africa through the Strait of Gibraltar.


Microsatellites mtDNA control region LDH-C1* Tyrrhenian brown trout Conservation 



The authors thank Bernard Lasserre, Sophie Dubois, Yuki Minegishi, and Zhaojun Shao for laboratory technical help, Pietro Armenia, Giuseppe Pisani, and Andrea Belluscio for field help, and David Schikorski (of the private company Labofarm-Genindexe—France) for genotyping most of the considered trouts. Thank you to Martin Laporte and Séverine Roques who participated to statistical solving. Some of the samples were constituted by the French anglers’ Federations of Alpes Maritimes and Corsica and the Genesalm project (CIPA). They are warmly thanked. Sicilian samples were collected with permission from the Regional Province of Syracuse and the professional assistance of Pietro Armena. In Calabria and Lazio (Rome), corresponding managers (Giuseppe Pisani in Calabria and Andrea Belluscio in Lazio) linked us with professional fishermen for sampling. We thank them for their irreplaceable assistance. The authors would also like to acknowledge OSU-OREME and Juliette Fabre for their help in database construction and mapping. Saša Marić was supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia (Grant No. 173045).

Supplementary material

10750_2018_3734_MOESM1_ESM.docx (35 kb)
Table S1: Accession numbers of all haplotypes positioned in Fig. 2 (* = new), completed with their geographic distribution according to twenty main publications. Supplementary material 1 (DOCX 34 kb)
10750_2018_3734_MOESM2_ESM.docx (33 kb)
Table S2: Hierarchical steps in estimating K (the number of genetic clusters) from STRUCTURE runs using the ΔK method. L(K) - posterior probability of K; stdev - standard deviation of L(K) from seven independent runs; ΔK - an ad hoc quantity, predictor of the real number of clusters (Evanno et al., 2005), best ΔK are highlighted. Supplementary material 2 (DOCX 33 kb)
10750_2018_3734_MOESM3_ESM.docx (38 kb)
Table S3: Detection of full-sibs in Corsican and Sardinian samples. Supplementary material 3 (DOCX 38 kb)
10750_2018_3734_MOESM4_ESM.docx (150 kb)
Fig. S4: New projection of the FCA analysis presented in Fig. 3a according to axes 1 and 3. In this new perspective, Sardinian samples and E Maghine Corsican one, together with the Corsican samples Lataga and Aqua d’Acelli, which seemed similar in Fig. 3a, are in fact clearly different (red arrows) while Corsican samples Pozzi and Val d’Ese confirm their similarity. Supplementary material 4 (DOCX 150 kb)
10750_2018_3734_MOESM5_ESM.jpg (132 kb)
Fig. S5: Estimation of the number of genetic clusters (K) for the first level, from STRUCTURE runs using the ΔK method. Supplementary material 5 (JPEG 132 kb)
10750_2018_3734_MOESM6_ESM.jpg (660 kb)
Fig. S6. Estimated population structure as inferred by STRUCTURE analysis of microsatellite marker DNA data. White lines separate sampling sites, the most probable K = 19 is based on maximizing the mean estimated ln probability of data (Pritchard et al., 2000). Names and codes of sampling sites/clusters are reported in Tables 1 and 4 and Fig. 4. Supplementary material 6 (JPEG 660 kb)


  1. Almodóvar, A., G. G. Nicola, B. Elvira & J. L. García-Marín, 2006. Introgression variability among Iberian brown trout evolutionary significant units: the influence of local management and environmental features. Freshwater Biology 51: 1175–1187.Google Scholar
  2. Angers, B., L. Bernatchez, A. Angers & L. Desgroseillers, 1995. Specific microsatellite loci for brook charr (Salvelinus fontinalis Mitchill) reveal strong population subdivision on a microgeographic scale. Journal of Fish Biology 48: 177–185.Google Scholar
  3. Araguas, R. M., M. Vera, E. Aparicio, N. Sanz, R. Fernandez-Cebrian, C. Marchante & J. L. García-Marín, 2017. Current status of the brown trout (Salmo trutta) populations within eastern Pyrenees genetic refuges. Ecology of Freshwater Fish 26: 120–132.Google Scholar
  4. Aurelle, D. & P. Berrebi, 2001. Genetic structure of brown trout (Salmo trutta, L.) populations from south-western France: data from mitochondrial control region variability. Molecular Ecology 10: 1551–1561.PubMedGoogle Scholar
  5. Aurelle, D. & P. Berrebi, 2002. Natural and artificial secondary contact in brown trout (Salmo trutta, L.) in the French western Pyrenees assessed by allozymes and microsatellites. Heredity 89: 171–183.PubMedGoogle Scholar
  6. Avise, J. C., 2000. Phylogeography—the history and formation of species. Harvard University Press, Cambridge.Google Scholar
  7. Bardakci, F., N. Degerli, O. Ozdemir & H. H. Basibuyuk, 2006. Phylogeography of the Turkish brown trout Salmo trutta L.: mitochondrial DNA PCR-RFLP variation. Journal of Fish Biology 68: 36–55.Google Scholar
  8. Behnke, R. J., 1972. The systematics of salmonid fishes of recently glaciated lakes. Journal of the Fisheries Research Board of Canada 29: 639–671.Google Scholar
  9. Behnke, R. J., 1986. Brown trout. Trout 27: 42–47.Google Scholar
  10. Belkhir, K., P. Borsa, J. Goudet & F. Bonhomme, 2004. GENETIX 4.05: logiciel sous Windows pour la génétique des populations. Laboratoire Génome et Population, CNRS-UPR, Université de Montpellier II, Montpellier, France.Google Scholar
  11. Benzécri, J.-P., 1973. L’analyse des données. Dunod, Paris.Google Scholar
  12. 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
  13. Bernatchez, L. & A. Osinov, 1995. Genetic diversity of trout (genus Salmo) from its most eastern native range based on mitochondrial DNA and nuclear gene variation. Molecular Ecology 4: 285–297.PubMedGoogle Scholar
  14. Bernatchez, L., R. Guyomard & F. Bonhomme, 1992. DNA sequence variation of the mitochondrial control region among geographically and morphologically remote European brown trout Salmo trutta populations. Molecular Ecology 1: 161–173.PubMedGoogle Scholar
  15. Berrebi, P., 2015. Three brown trout Salmo trutta lineages in Corsica described through allozyme variation. Journal of Fish Biology 86: 60–73.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.Google Scholar
  17. Berrebi, P., C. Tougard, S. Dubois, Z. Shao, I. Koutseri, S. Petkovski & A. J. Crivelli, 2013. Genetic diversity and conservation of the Prespa trout in the Balkans. International Journal of Molecular Sciences 14: 23454–23470.PubMedPubMedCentralGoogle Scholar
  18. Bianco, P. G., 2014. An update on the status of native and exotic freshwater fishes of Italy. Journal of Applied Ichthyology 30: 62–77.Google Scholar
  19. Bohling, J., P. Haffray & P. Berrebi, 2016. Genetic diversity and population structure of domestic brown trout (Salmo trutta) in France. Aquaculture 462: 1–9.Google Scholar
  20. Boulenger, G. A., 1901. On the occurrence of Salmo macrostigma in Sardinia. Annals and Magazine of Natural History 8(43): 14.Google Scholar
  21. Buroker, N. E., J. R. Brown, T. A. Gilbert, P. J. O’Hara, A. T. Beckenbach, W. K. Thomas & M. J. Smith, 1990. Length heteroplasmy of sturgeon mitochondrial DNA, an illegitimate elongation model. Genetics 124: 157–163.PubMedPubMedCentralGoogle Scholar
  22. Charles, K., R. Guyomard, B. Hoyheim, D. Ombredane & J.-L. Baglinière, 2005. Lack of genetic differentiation between anadromous and resident sympatric brown trout (Salmo trutta) in a Normandy population. Aquatic Living Resources 18: 65–69.Google Scholar
  23. Clement, M., D. Posada & K. A. Crandall, 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1660.PubMedPubMedCentralGoogle Scholar
  24. Cortey, M. & J. L. García-Marín, 2002. Evidence for phylogeographically informative sequence variation in the mitochondrial control region of Atlantic brown trout. Journal of Fish Biology 60: 1058–1063.Google Scholar
  25. Cortey, M., C. Pla & J. L. García-Marín, 2004. Historical biogeography of Mediterranean trout. Molecular Phylogenetics and Evolution 33: 831–844.PubMedGoogle Scholar
  26. Cortey, M., M. Vera, C. Pla & J. L. García-Marín, 2009. Northern and Southern expansions of Atlantic brown trout (Salmo trutta) populations during the Pleistocene. Biological Journal of the Linnean Society 97: 904–917.Google Scholar
  27. De Moor, I. J. & M. N. Bruton, 1988. Atlas of alien and translocated indigenous aquatic animals in southern Africa. National Scientific Programmes Unit: CSIR, SANSP Report 144: 317.Google Scholar
  28. Delling, B., 2010. Diversity of western and southern Balkan trouts, with the description of a new species from the Louros River, Greece (Teleostei: Salmonidae). Ichthyological Exploration of Freshwaters 21: 331–344.Google Scholar
  29. Delling, B. & I. Doadrio, 2005. Systematics of the trouts endemic to Moroccan lakes, with description of a new species (Teleostei: Salmonidae). Ichthyological Exploration of Freshwaters 16: 49–64.Google Scholar
  30. Doadrio, I., S. Perea & A. Yahyaoui, 2015. Two new species of Atlantic trout (Actinopterygii, Salmonidae) from Morocco. Graellsia 71(2): e031.Google Scholar
  31. Duchi, A., 2011. Fecundity, egg and alevin size in the River Irminio population of the threatened Salmo cettii Rafinesque-Schmaltz, 1810 (Sicily, Italy). Journal of Applied Ichthyology 27: 868–872.Google Scholar
  32. Duchi, A., 2018. Flank spot number and its significance for systematics, taxonomy and conservation of the near-threatened Mediterranean trout Salmo cettii: evidence from a genetically pure population. Journal of Fish Biology 92: 254–260.PubMedGoogle Scholar
  33. Estoup, A., C. R. Largiader, E. Perrot & D. Chourrout, 1996. Rapid one-tube DNA extraction for reliable PCR detection of fish polymorphic markers and transgenes. Molecular Marine Biology and Biotechnology 5: 295–298.Google Scholar
  34. Evanno, G., S. Regnaut & J. Goudet, 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620.PubMedGoogle Scholar
  35. Fabiani, A., P. Gratton, I. A. Zappes, M. Seminara, A. D’Orsi, V. Sbordoni & G. Allegrucci, 2018. Investigating the genetic structure of trout from the Garden of Ninfa (central Italy): suggestions for conservation and management. Fisheries Management and Ecology 25: 1–11.Google Scholar
  36. Fruciano, C., A. M. Pappalardo, C. Tigano & V. Ferrito, 2014. Phylogeographical relationships of Sicilian brown trout and the effects of genetic introgression on morphospace occupation. Biological Journal of Linnean Society 112: 387–398.Google Scholar
  37. Gandolfi, G., S. Zerunian, P. Torricelli & A. Marconato, 1991. I Pesci delle acque interne italiane. Ministero dell’Ambiente, Instituto Poligrafico e Zecca dello Stato, Rome. pp. 616.Google Scholar
  38. García-Marín, J.-L., F. M. Utter & C. Pla, 1999. Postglacial colonization of brown trout in Europe based on distribution of allozyme variants. Heredity 82: 46–56.Google Scholar
  39. Garnett, S. T. & L. Christidis, 2017. Taxonomy anarchy hampers conservation—the classification of complex organisms is in chaos. Nature 546: 25–27.PubMedGoogle Scholar
  40. Gauthier, A. & P. Berrebi, 2007. La colonisation de l’île par différentes souches de truite. Guide de gestion de la truite macrostigma. pp 4–10.Google Scholar
  41. Giuffra, E., L. Bernatchez & R. Guyomard, 1994. Mitochondrial control region and protein coding genes sequence variation among phenotypic forms of brown trout Salmo trutta from northern Italy. Molecular Ecology 3: 161–171.PubMedGoogle Scholar
  42. Giuffra, E., R. Guyomard & G. Forneris, 1996. Phylogenetic relationships and introgression patterns between incipient parapatric species of Italian brown trout (Salmo trutta L. complex). Molecular Ecology 5: 207–220.Google Scholar
  43. Gratton, P., G. Allegrucci, V. Sbordoni & A. Gandolfi, 2014. The evolutionary jigsaw puzzle of the surviving trout (Salmo trutta L. complex) diversity in the Italian region. A multilocus Bayesian approach. Molecular Phylogenetics and Evolution 79: 292–304.PubMedGoogle Scholar
  44. Guyomard, R., 1989. Diversité génétique de la truite commune. Bulletin Français de Pêche et de Pisciculture 314: 118–135.Google Scholar
  45. Hamilton, K. E., A. Ferguson, J. B. Taggart, T. Tomasson, A. Walker & E. Fahy, 1989. Post-glacial colonisation of brown trout, Salmo trutta L.: Ldh-5 as a phylogeographic marker locus. Journal of Fish Biology 35: 651–664.Google Scholar
  46. Hebert, P. D. N., A. Cywinska, S. L. Ball & J. R. DeWaard, 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society Series B, Biological Sciences 270: 313–321.Google Scholar
  47. Holm, L. E. & C. Bendixen, 2000. Oncorhynchus mykiss clone TAA72-13, sequence tagged site [available on internet at]. Accession number AF239038.
  48. Isaac, N. J. B., J. Mallet & G. M. Mace, 2004. Taxonomic inflation: its influence on macroecology and conservation. Trends in Ecology and Evolution 19: 464–469.PubMedGoogle Scholar
  49. Jones, O. R. & J. I. Wang, 2010. COLONY: a program for parentage and sibship inference from multilocus genotype data. Molecular Ecology Resources 10: 551–555.PubMedGoogle Scholar
  50. Knowles, L. L. & B. C. Carstens, 2007. Delimiting species without monophyletic gene trees. Systematic Biology 56(6): 887–895.PubMedGoogle Scholar
  51. Kottelat, M., 1997. European freshwater fishes. An heuristic checklist of the freshwater fishes of Europe (exclusive of former USSR), with an introduction for non-systematists and comments on nomenclature and conservation. Biologia, Bratislava 52 (supplement 5): 1–271.Google Scholar
  52. Kottelat, M. & J. Freyhof, 2007. Handbook of European Freshwater Fishes. Publications Kottelat, Cornol, CH, xiv + 646 pp.Google Scholar
  53. Largiadèr, C. R. & A. Scholl, 1996. Genetic introgression between native and introduced brown trout (Salmo trutta L.) populations in the Rhone River Basin. Molecular Ecology 5: 417–426.Google Scholar
  54. Lucentini, L., A. Palomba, L. Gigliarelli, H. Lancioni, P. Viali & F. Panara, 2006. Genetic characterization of a putative indigenous brown trout (Salmo trutta fario) population in a secondary stream of the Nera River Basin (Central Italy) assessed by means of three molecular markers. Italian Journal of Zoology 73: 263–273.Google Scholar
  55. Marić, S., S. Sušnik Bajec, J. Schöffmann, V. Kostov & A. Snoj, 2017. Phylogeography of stream-dwelling trout in the Republic of Macedonia and a molecular genetic basis for revision of the taxonomy proposed by S. Karaman. Hydrobiologia 785: 249–260.Google Scholar
  56. Massidda, P., 1995. Salmo (trutta) macrostigma in Sardegna. Biologia Ambientale 5: 40–43.Google Scholar
  57. 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.PubMedGoogle Scholar
  58. 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.Google Scholar
  59. Miró, A. & M. Ventura, 2013. Historical use, fishing management and lake characteristics explain the presence of non-native trout in Pyrenean lakes: Implications for conservation. Biological Conservation 167: 17–24.Google Scholar
  60. Mola, P., 1928. Facies della fauna e della flora delle acque interne. Contributo alla idrobiologia della Sardegna. Internationale Revue der gesamten Hydrobiologie und Hydrographie 20: 117–173.Google Scholar
  61. Moritz, C., 1994. Defining evolutionarily significant units for conservation. Trends in Ecology and Evolution 9: 373–375.PubMedGoogle Scholar
  62. Nei, M., 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583–590.PubMedPubMedCentralGoogle Scholar
  63. Ninua, L., D. Tarkhnishvili & E. Gvazava, 2018. Phylogeography and taxonomic status of trout and salmon from the Ponto-Caspian drainages, with inferences on European brown trout evolution and taxonomy. Ecology and Evolution. Scholar
  64. Nonnis Marzano, F., N. Corradi, R. Papa, J. Tagliavini & G. Gandolfi, 2003. Molecular evidence for introgression and loss of genetic variability in Salmo (trutta) macrostigma as a result of massive restocking of Apennine populations (Northern and Central Italy). Environmental Biology of Fishes 68: 349–356.Google Scholar
  65. Olsson, K., P. Stenroth, P. Nyström, N. Holmqvist, A. R. McIntosh & M. J. Winterbourn, 2006. Does natural acidity mediate interactions between introduced brown trout, native fish, crayfish and other invertebrates in West Coast New Zealand streams? Biological Conservation 130: 255–267.Google Scholar
  66. O’Reilly, P. T., L. C. Hamilton, S. K. McConnell & J. M. Wright, 1996. Rapid analysis of genetic variation in Atlantic salmon (Salmo salar) by PCR multiplexing of dinucleotide and tetranucleotide microsatellites. Canadian Journal of Fisheries and Aquatic Sciences 53: 2292–2298.Google Scholar
  67. Orrù, F., A. M. Deiana & A. Cau, 2010. Introduction and distribution of alien freshwater fishes on the island of Sardinia (Italy): an assessment on the basis of existing data sources. Journal of Applied Ichthyology 26(2): 46–52.Google Scholar
  68. Patarnello, T., L. Bargelloni, F. Caldara & L. Colombo, 1994. Cytochrome b and 16S rRNA sequence variation in the Salmo trutta (Salmonidae, Teleostei) species complex. Molecular Phylogenetics and Evolution 3: 69–74.PubMedGoogle Scholar
  69. Phillimore, A. B. & I. P. F. Owens, 2006. Are subspecies useful in evolutionary and conservation biology? Proceedings of the Royal Society of London, Series B, Biological Sciences 273: 1049–1053.Google Scholar
  70. Pomini, F. P., 1940. Ricerche sul Salmo macrostigma Dum. Bollettino di Pesca, Piscicoltura e Idrobiologia 16(3): 12–63.Google Scholar
  71. Popa, G.-O., A. Curtean-Bănăduc, D. Bănăduc, I. E. Florescu, A. Burcea, A. Dudu, S. E. Georgescu & M. Costache, 2016. Molecular markers reveal reduced genetic diversity in Romanian populations of brown trout, Salmo trutta L., 1758 (Salmonidae). Acta Zoologica Bulgarica 68: 399–406.Google Scholar
  72. Presa, P. & R. Guyomard, 1996. Conservation of microsatellites in three species of salmonids. Journal of Fish Biology 49: 1326–1329.Google Scholar
  73. Presa, P., F. Krieg, A. Estoup & R. Guyomard, 1994. Diversité et gestion génétique de la truite commune: apport de l’étude du polymorphisme des locus protéiques et microsatellites. Genetics Selection Evolution 26(suppl. 1): 183–202.Google Scholar
  74. 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(12): 2161–2175.PubMedGoogle Scholar
  75. Pritchard, J. K., M. Stephens & P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.PubMedPubMedCentralGoogle Scholar
  76. Rexroad III, C. E., R. L. Coleman, W. K. Hershberger & J. Killefer, 2002. Thirty-eight polymorphic microsatellite markers for mapping in rainbow trout. Journal of Animal Science 80: 541–542.PubMedGoogle Scholar
  77. Rice, W. R., 1989. Analyzing tables of statistical tests. Evolution 43: 223–225.Google Scholar
  78. Roule, L., 1933. Le peuplement des cours d’eau de la Corse en poissons. Bulletin Français de Pisciculture 63: 61–62.Google Scholar
  79. Sabatini, A., F. Orrù, R. Cannas, P. Serra & P. Cau, 2006. Conservation and management of Salmo (trutta) macrostigma in Sardinian freshwaters: first results of genetic characterization. Quaderni ETP 34: 335–340.Google Scholar
  80. Sabatini, A., R. Cannas, M. C. Follesa, F. Palmas, A. Manunza, G. Matta, A. A. Pendugiu, P. Serra & A. Cau, 2011. Genetic characterization and artificial reproduction attempt of endemic Sardinian trout Salmo trutta L., 1758 (Osteichthyes, Salmonidae): Experiences in captivity. Italian Journal of Zoology 78(1): 20–26.Google Scholar
  81. Sabatini, A., C. Podda, G. Frau, M. V. Cani, A. Musu, M. Serra & F. Palmas, 2018. Restoration of native Mediterranean trout Salmo cetti Rafinesque, 1810 (Actinopterygii, Salmonidae) populations using an electric barrier as mitigation tool. The European Zoological Journal. Scholar
  82. Sanz, N., 2018. Phylogeographic history of brown trout: a review. In Lobon-Cervia, J. & N. Sanz (eds), Brown trout: biology, ecology and management. Wiley, Hoboken, NJ: 17–63.Google Scholar
  83. Schöffmann, J., S. Sušnik & A. Snoj, 2007. Phylogenetic origin of Salmo trutta L 1758 from Sicily, based on mitochondrial and nuclear DNA analyses. Hydrobiologia 575: 51–55.Google Scholar
  84. Scribner, K. T., J. R. Gust & R. L. Fields, 1996. Isolation and characterization of novel salmon microsatellite loci: cross-species amplification and population genetic applications. Canadian Journal of Fisheries and Aquatic Sciences 53: 833–841.Google Scholar
  85. She, J. X., M. Autem, G. Kotoulas, N. Pasteur & F. Bonhomme, 1987. Multivariate analysis of genetic exchanges between Solea aegyptiaca and Solea senegalensis (Teleosts, Soleidae). Biological Journal of the Linnean Society 32: 357–371.Google Scholar
  86. Sites, J. W. & J. C. Marshall, 2004. Empirical criteria for delimiting species. Annual Review of Ecology, Evolution, and Systematics 35: 199–227.Google Scholar
  87. Slettan, A., I. Olsaker & Ø. Lie, 1995. Atlantic salmon, Salmo salar, microsatellites at the SSOSL25, SSOSL85, SSOSL311, SSOSL417 loci. Animal Genetics 26: 277–285.Google Scholar
  88. Slettan, A., I. Olsaker & Ø. Lie, 1996. Polymorphic Atlantic salmon, Salmo salar, microsatellites at the SSOSL438, SSOSL439 and SSOSL444 loci. Animal Genetics 27: 57–64.PubMedGoogle Scholar
  89. Snoj, A., E. Melkic, S. Sušnik, S. Muhamedagic & P. Dovc, 2002. DNA phylogeny supports revised classification of Salmothymus obtusirostris. Biological Journal of the Linnean Society 77: 397–411.Google Scholar
  90. Snoj, A., S. Marić, P. Berrebi, A. J. Crivelli, S. Shumka & S. Sušnik, 2009. Genetic architecture of trout from Albania as revealed by mtDNA control region variation. Genetics Selection Evolution 41: 22.Google Scholar
  91. Snoj, A., B. Glamuzina, A. Razpet, J. Zablocki, I. Bogut, E. Lerceteau-Kohler, N. Pojskic & S. Sušnik, 2010. Resolving taxonomic uncertainties using molecular systematics: Salmo dentex and the Balkan trout community. Hydrobiologia 651: 199–212.Google Scholar
  92. Snoj, A., S. Marić, S. Sušnik Bajec, P. Berrebi, S. Janjani & J. Schöffmann, 2011. Phylogeographic structure and demographic patterns of brown trout in North-West Africa. Molecular Phylogenetics and Evolution 61: 203–211.PubMedGoogle Scholar
  93. Splendiani, A., T. Fioravanti, M. Giovannotti, A. Negri, P. Ruggeri, L. Olivieri, P. Nisi Cerioni, M. Lorenzoni & V. Caputo Barucchi, 2016. The effects of paleoclimatic events on Mediterranean trout: preliminary evidences from ancient DNA. PLoS ONE 11(6): e0157975.PubMedPubMedCentralGoogle Scholar
  94. Splendiani, A., T. Fioravanti, M. Giovannotti, L. Olivieri, P. Ruggeri, P. Nisi Cerioni, S. Vanni, F. Enrichetti & V. Caputo Barucchi, 2017. Museum samples could help to reconstruct the original distribution of Salmo trutta complex in Italy. Journal of Fish Biology 90: 2443–2451.PubMedGoogle Scholar
  95. Stelkens, R. B., G. Jaffuel, M. Escher & C. Wedekind, 2012. Genetic and phenotypic population divergence on a microgeographic scale in brown trout. Molecular Ecology 21: 2896–2915.PubMedGoogle Scholar
  96. Suárez, J., J. M. Bautista, A. Almodóvar & A. Machordom, 2001. Evolution of the mitochondrial control region in Paleartic brown trout (Salmo trutta) populations: the biogeographical role of the Iberian Peninsula. Heredity 87: 198–206.PubMedGoogle Scholar
  97. Sušnik, S., J. Schöffmann & A. Snoj, 2004. Phylogenetic position of Salmo (Platysalmo) platycephalus Behnke 1968 from south-central Turkey, evidenced by genetic data. Journal of Fish Biology 64: 947–960.Google Scholar
  98. Sušnik, S., I. Knizhin, A. Snoj & S. Weiss, 2006. Genetic and morphological characterization of a Lake Ohrid endemic, Salmo (Acantholingua) ohridanus with a comparison to sympatric Salmo trutta. Journal of Fish Biology 68: 2–23.Google Scholar
  99. Sušnik, 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.PubMedGoogle Scholar
  100. Tamura, K., G. Stecher, D. Peterson, A. Filipski & S. Kumar, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.PubMedPubMedCentralGoogle Scholar
  101. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin & D. G. Higgins, 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25: 4876–4882.PubMedPubMedCentralGoogle Scholar
  102. Turan, D., M. Kottelat & S. Engin, 2009. Two new species of trouts, resident and migratory, sympatric in streams of northern Anatolia (Salmoniformes: Salmonidae). Ichthyological Exploration of Freshwaters 20: 333–364.Google Scholar
  103. Turan, D., M. Kottelat & S. Engin, 2010. Two new species of trouts, resident and migratory, sympatric in streams of northern Anatolia (Salmoniformes: Salmonidae). Ichthyological Exploration of Freshwaters 20: 289–384.Google Scholar
  104. Turan, D., M. Kottelat & Y. Bektas, 2011. Salmo tigridis, a new species of trout from the Tigris River, Turkey (Teleostei: Salmonidae). Zootaxa 2993: 23–33.Google Scholar
  105. Turan, D., M. Kottelat & S. Engin, 2012. The trouts of the Mediterranean drainages of southern Anatolia, Turkey, with description of three new species (Teleostei: Salmonidae). Ichthyological Exploration of Freshwaters 23: 219–236.Google Scholar
  106. Turan, D., E. Doğan, C. Kaya & M. Kanyılmaz, 2014a. Salmo kottelati, a new species of trout from Alakır Stream, draining to the Mediterranean in southern Anatolia, Turkey (Teleostei, Salmonidae). ZooKeys 462: 135–151.Google Scholar
  107. Turan, D., M. Kottelat & S. Engin, 2014b. Two new species of trouts from the Euphrates drainage, Turkey (Teleostei: Salmonidae). Ichthyological Exploration of Freshwaters 24: 275–287.Google Scholar
  108. Vähä, J. P., J. Erkinaro, E. Niemelä & C. R. Primmer, 2007. Life-history and habitat features influence the within-river genetic structure of Atlantic salmon. Molecular Ecology 16: 2638–2654.PubMedGoogle Scholar
  109. van Oosterhout, C., W. F. Hutchinson, D. P. Wills & P. Shipley, 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.Google Scholar
  110. Walsh, P. S., D. A. Metzger & R. Higushi, 1991. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10(4): 506–513.PubMedGoogle Scholar
  111. Weir, B. S. & C. C. Cockerham, 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370.Google Scholar
  112. Weiss, S., A. Antunes, C. Schlötterer & P. Alexandrino, 2000. Mitochondrial haplotype diversity among Portuguese trout Salmo trutta L. populations: relevance of the post-Pleistocene recolonization of northern Europe. Molecular Ecology 9: 691–698.PubMedGoogle Scholar
  113. Yue, G. H. & L. Orban, 2005. A simple and affordable method for high-throughput DNA extraction from animal tissues for polymerase chain reaction. Electrophoresis 26: 3081–3083.PubMedGoogle Scholar
  114. Zaccara, S., S. Trasforini, C. M. Antognazza, C. Puzzi, J. R. Britton & G. Crosa, 2015. Morphological and genetic characterization of Sardinian trout Salmo cettii Rafinesque, 1810 and their conservation implications. Hydrobiologia 760: 205–223.Google Scholar
  115. Zachos, F. E., M. Apollonio, E. V. Barmann, M. Festa-Bianchet, U. Gohlich, J. C. Habel, E. Haring, L. Kruckenhauser, S. Lovari, A. D. McDevitt, C. Pertoldi, G. E. Rossner, M. R. Sanchez-Villagra, M. Scandura & F. Suchentrunk, 2013. Species inflation and taxonomic artefacts—a critical comment on recent trends in mammalian classification. Mammalian Biology 78: 1–6.Google Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.ISEM, Université de Montpellier, CNRS, IRD, EPHEMontpellierFrance
  2. 2.Dipartimento di Scienze della Vita e dell’AmbienteUniversita Politecnica delle MarcheAnconaItaly
  3. 3.Office National des ForêtsCorteFrance
  4. 4.Dipartimento di Scienze della Vita e dell’AmbienteUniversità di CagliariCagliariItaly
  5. 5.Dipartimento di STEBICEFUniversità di PalermoPalermoItaly
  6. 6.Faculty of Biology, Institute of ZoologyUniversity of BelgradeBelgradeSerbia
  7. 7.Genome – Research & DiagnosticMontpellierFrance

Personalised recommendations