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Microsatellite DNA data point to extensive but incomplete admixture in a marble and brown trout hybridisation zone

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Abstract

Marble trout, endemic to the Adriatic drainage basin, is severely threatened by hybridisation with non-native brown trout. In the present study, we analysed 12 microsatellite DNA loci to assess genetic population structure and differentiation between sympatric phenotypic marble and brown trout at nine sampling sites in the upper Etsch/Adige River system. F ST and AMOVA analyses revealed significant genetic differentiation between marble and brown trout samples. Thus, admixture between brown and marble trout appears to be incomplete. However, factorial correspondence analysis depicted marble trout, Atlantic brown trout and intermediate genotypes. Bayesian-based individual assignment tests identified indigenous marble trout at five sampling sites. In four other samples no ‘pure’ marble trout were detected. Bidirectional, first-generation hybridisation, involving both sexes of both parental species was observed. In locations where ‘pure’ marble trout still exist, post-F1 hybridisation appears to be directed towards brown trout. This has likely slowed the rate of hybridisation between the two trout species and the decline of relic marble trout populations. Based on these results, restoration management actions are proposed, such as the abandonment of brown trout stocking activities, sharper angling policies, establishment of indigenous marble trout breeding strains and the elaboration of a conservation priority list.

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References

  • Allendorf FW, Ryman N (1987) Genetic management of hatchery stocks. In: Ryman N, Utter F (eds) Population genetics and fishery management. University of Washington Press, Seattle, pp 141–159

    Google Scholar 

  • Allendorf FW, Bayles D, Bottom DL, Currens KP, Frissell CA, Hankin D, Lichatowich JA, Nehlsen W, Trotter PC, Williams TH (1997) Prioritizing Pacific salmon stocks for conservation. Conserv Biol 11:140–152

    Article  Google Scholar 

  • Allendorf FW, Leary RF, Hitt NP, Knudsen KL, Lundquist LL, Spruell P (2004) Intercrosses and the U.S. endangered species act: should hybridized populations be included as Westslope Cutthroat trout? Conserv Biol 18:1203–1213

    Article  Google Scholar 

  • Anderson EC, Waples RS, Kalinowski ST (2008) An improved method for predicting the accuracy of genetic stock identification. Can J Fish Aquat Sci 65:1475–1486

    Article  Google Scholar 

  • Barton NH (2001) The role of hybridisation in evolution. Mol Ecol 10:551–568

    Article  CAS  PubMed  Google Scholar 

  • Beaumont M, Barratt EM, Gottelli D, Kitchener AC, Daniels J, Pritchard JK, Bruford MW (2001) Genetic diversity and introgression in the Scottish wildcat. Mol Ecol 10:319–336

    Article  CAS  PubMed  Google Scholar 

  • Belkhir K, Borsa P, Goudet J, Chikhi L, Bonhomme F (1999) GENETIX, logiciel sous Windows TM pour la génétique des populations. Laboratoire Genome et populations, CNRS UPR 9060, Université de Montpellier II, Montpellier, France

  • Berrebi P, Povc M, Jesenek D, Cattaneo-Berrebi G, Crivelli AJ (2000) The genetic diversity of native, stocked and hybrid populations of marble trout in the Soca river, Slovenia. Heredity 85:277–287

    Article  CAS  PubMed  Google Scholar 

  • Bruford MW, Hanotte O, Brookfield JFY, Burke T (1998) Multilocus and single-locus DNA fingerprinting. In: Hoelzel AR (ed) Molecular genetic analysis of populations: A practical approach. Oxford University Press, Oxford, pp 287–336

    Google Scholar 

  • Delling B, Crivelli AJ, Rubin J-F, Berrebi P (2000) Morphological variation in hybrids between Salmo marmoratus and alien Salmo species in the Volarja stream, Soca River basin, Slovenia. J Fish Biol 57:1199–1212

    Google Scholar 

  • Epifanio J, Philipp D (2001) Simulating the extinction of parental lineages from introgressive hybridization: the effects of fitness, initial proportions of parental taxa, and mate choice. Rev Fish Biol Fish 10:339–354

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Estoup A, Rousset F, Michalakis Y, Cornuet J-M, Adriamanga M, Guyomard R (1998) Comparative analysis of microsatellite and allozyme markers: a case study investigating microgeographic differentiation in brown trout (Salmo trutta). Mol Ecol 7:339–353

    Article  CAS  PubMed  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2621

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Fumagalli L, Snoj A, Jesenek D, Balloux F, Jug T, Duron O, Brossier F, Crivelli AJ, Berrebi P (2002) Extreme genetic differentiation among the remnant populations of marble trout (Salmo marmoratus) in Slovenia. Mol Ecol 11:2711–2716

    Article  CAS  PubMed  Google Scholar 

  • Garcia LV (2003) Controlling the false discovery rate in ecological research. Trends Ecol Evol 18:553–554

    Article  Google Scholar 

  • 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 5:161–171

    Article  Google Scholar 

  • Giuffra E, Guyomard R, Forneris G (1996) Phylogenetic relationships and introgression patterns between incipient parapatric species of Italian brown trout (Salmo trutta L. complex). Mol Ecol 5:207–220

    Google Scholar 

  • Goodman SJ, Barton NH, Swanson G, Abernethy K, Pemberton JM (1999) Introgression through rare hybridisation: a genetic study of a hybrid zone between red and silka deer (Genus Cervus) in Argyll, Scotland. Genetics 152:355–371

    CAS  PubMed  Google Scholar 

  • Gunnell K, Tada MK, Hawthorne FA, Keeley ER, Ptacek MB (2008) Geographic patterns of introgressive hybridization between native Yellowstone cutthroat trout (Oncorhynchus clarkia bouvieri) and introduced rainbow trout (O. mykiss) in the South Fork of the Snake River watershed, Idaho. Conserv Genet 9:49–64

    Article  CAS  Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372

    Article  CAS  PubMed  Google Scholar 

  • Hansen MM (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. Mol Ecol 11:1003–1015

    Article  CAS  PubMed  Google Scholar 

  • Hansen MM, Ruzzante DE, Nielsen EE, Mensberg K-LD (2000) Microsatellite and mitochondrial DNA polymorphism reveals life-history dependant interbreeding between hatchery and wild brown trout (Salmo trutta L.). Mol Ecol 9:583–594

    Article  CAS  PubMed  Google Scholar 

  • Hansen MM, Bekkevold D, Jensen LF, Mensberg K-L, Nielsen EE (2006) Genetic restoration of a stocked brown trout Salmo trutta population using microsatellite DNA analysis of historical and contemporary samples. J Applied Ecol 43:669–679

    Article  CAS  Google Scholar 

  • Jug T, Dovc P, Pohar J, Snoj A (2004) RAPD analysis as a tool for discriminating marble trout from hybrids (marble trout × brown trout) in the zones of hybridisation. J Animal Breed Genet 121:156–162

    Article  CAS  Google Scholar 

  • Jug T, Berrebi P, Snoj A (2005) Distribution of non-native trout in Slovenia and their introgression with native trout populations as observed through microsatellite DNA analysis. Biol Conserv 123:381–388

    Article  Google Scholar 

  • Kalinowski ST (2004) Genetic polymorphism and mixed-stock fisheries analysis. Can J Aquat Sci 61:1075–1082

    Article  CAS  Google Scholar 

  • Kalinowski ST, Manlove KR, Taper ML (2008) ONCOR—software for genetic stock identification. Department of Ecology, Montana State University, USA

    Google Scholar 

  • Kotulas G (1989) Differentiation géographique et structure génétique des populations de Solea vulgaris. PhD Thesis, Université de Montpellier II, Montpellier, France

  • Leary RF, Allendorf FW, Sage GK (1995) Hybridisation and introgression between introduced and native fish. Am Fish Soc Symp 15:91–101

    Google Scholar 

  • Meldgaard T, Crivelli AJ, Jesensek D, Poizat G, Rubin JF, Berrebi P (2007) Hybridization mechanisms between the endangered marble trout (Salmo marmoratus) and the brown trout (Salmo trutta) as revealed by in-stream experiments. Biol Cons 136:602–611

    Article  Google Scholar 

  • Meraner A, Baric S, Pelster B, Dalla Via J (2007) Trout (Salmo trutta) mitochondrial DNA polymorphism in the centre of the marble trout distribution area. Hydrobiologia 579:337–349

    Article  CAS  Google Scholar 

  • Meraner A, Baric S, Dalla Via J (2008) The selection of the ‘wild’: a combined molecular approach for the identification of pure indigenous fish from hybridised populations. Comp Biochem Physiol D 3:36–42

    Google Scholar 

  • O’Reilly P, Hamilton L, McConnell S, Wright J (1996) Rapid analysis of genetic variation in Atlantic salmon (Salmo salar) by PCR multiplexing of dinucleotide and tetranucleotide microsatellites. Can J Fish Aquat Sci 53:2292–2298

    Article  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  CAS  PubMed  Google Scholar 

  • Poteaux C (1995) Interactions genetiques entre formes sauvages et formes domestiques chez la truite commune (Salmo trutta fario L.). PhD Thesis, Université de Montpellier II, Montpellier, France

  • Presa P, Guyomard R (1996) Conservation of microsatellites in three species of salmonids. J Fish Biol 49:1326–1329

    Google Scholar 

  • Pritchard J, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  Google Scholar 

  • Rhymer JM, Simberloff D (1996) Extinction by hybridisation and introgression. Ann Rev Ecol Sys 27:83–109

    Article  Google Scholar 

  • Riedl A (2005) Genetische Charakterisierung von Bachforellenpopulationen in Westösterreich mit Hilfe von Sequenzen der gesamten mitochondrialen Kontrollregion. Master thesis, University of Natural Resources and Applied Life Sciences, Vienna, Austria

  • Rubidge EM, Taylor EB (2005) An analysis of spatial and environmental factors influencing hybridization between native westslope cutthroat trout (Oncorhynchus clarkii lewisi) and introduced rainbow trout (O. mykiss) in the upper Kootenay River drainage, British Columbia. Conserv Genet 6:369–384

    Article  CAS  Google Scholar 

  • Salzburger W, Baric S, Sturmbauer C (2002) Speciation via introgressive hybridisation in East African cichlids? Mol Ecol 11:619–625

    Article  CAS  PubMed  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin, 2000: a software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland

    Google Scholar 

  • Skaala O, Jorstad KE, Borgstrom R (1996) Genetic impact on two wild brown trout (Salmo trutta) populations after release of non-indigenous hatchery spawners. Can J Fish Aquat Sci 53:2027–2035

    Article  Google Scholar 

  • Slatkin M, Excoffier L (1996) Testing for linkage disequilibrium in genotypic data using the expectation–maximization algorithm. Heredity 76:377–383

    Article  PubMed  Google Scholar 

  • Snoj A, Pohar J, Dovc P (1997) The first microsatellite DNA marker for marble trout, BFRO 001. J Anim Sci 75:1983

    CAS  PubMed  Google Scholar 

  • Snoj A, Jug T, Melkic E, Susnik S, Pohar J, Dovc P, Jesensek D, Budihna N (2000) Mitochondrial and microsatellite DNA analysis of marble trout in Slovenia. Quaderni ETP 29:5–11

    Google Scholar 

  • Storey JD (2002) A direct approach to false discovery rates. J R Statist Soc B 64:479–498

    Article  Google Scholar 

  • Susnik S, Snoj A, Pohar J, Dovc P (1997) The microsatellite marker (BFRO 002) characteristic for different geographically remote brown trout, Salmo trutta L., populations. Anim Genetics 28:372

    CAS  Google Scholar 

  • Taylor EB, Boughman W, Groenenboom M, Sniatynski M, Schluter D, Gow JL (2006) Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Mol Ecol 15:343–356

    Article  CAS  PubMed  Google Scholar 

  • Vähä JP, Primmer CR (2006) Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridisation scenarios and with different numbers of loci. Mol Ecol 15:63–72

    Article  PubMed  Google Scholar 

  • Van Houdt JKJ, Pinceel J, Flamand MC, Briquet M, Dupont E, Volckaert FAM, Baret PV (2005) Migration barriers protect indigenous brown trout (Salmo trutta) populations from introgression with stocked hatchery fish. Conserv Gen 6:175–191

    Article  Google Scholar 

  • Waples RS, Teel DJ, Myers JM, Marshall AR (2004) Life-history divergence in Chinook salmon: historic contingency and parallel evolution. Evolution 58:386–403

    Article  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wirtz P (1999) Mother species–father species: unidirectional hybridisation in animals with female choice. Anim Behav 58:1–12

    Article  PubMed  Google Scholar 

  • Xia X, Xie Z (2001) DAMBE: software package for data analysis in molecular biology and evolution. J Hered 92:371–373

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The present study is part of the project ‘TroutExamInvest’ funded by the European Union under its Interreg IIIA programme between Italy and Austria, and the Governments of South Tyrol (Italy) and Tyrol (Austria). The authors thank the head and the collaborators of the Fisheries Office of the Autonomous Province of Bozen/Bolzano, especially H. Erhard and H. Grund for their assistance during sampling activities. Furthermore, the authors thank A. Snoj from the University of Ljubljana (Slovenia) for providing DNA extracts from Slovenian marble trout populations, N. Medgyesy and R. Lackner from the University of Innsbruck for providing samples of the Danubian brown trout population as well as the three anonymous reviewers and G. Buemberger for their valuable suggestions to improve the manuscript.

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Correspondence to Sanja Baric.

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Appendix

See Tables 5 and 6.

Table 5 Pairwise F ST values between the trout populations from South Tyrol and reference samples
Table 6 ΔK values calculated for each of the nine sampling sites in South Tyrol according to the method described by Evanno et al. (2005)

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Meraner, A., Baric, S., Pelster, B. et al. Microsatellite DNA data point to extensive but incomplete admixture in a marble and brown trout hybridisation zone. Conserv Genet 11, 985–998 (2010). https://doi.org/10.1007/s10592-009-9942-9

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