Published September 30, 2021 | Version v1
Journal article Open

A genomic perspective on an old question: Salmo trouts or Salmo trutta (Teleostei: Salmonidae)?

Description

Hashemzadeh Segherloo, Iraj, Freyhof, Jörg, Berrebi, Patrick, Ferchaud, Anne-Laure, Geiger, Matthias, Laroche, Jérôme, Levin, Boris A., Normandeau, Eric, Bernatchez, Louis (2021): A genomic perspective on an old question: Salmo trouts or Salmo trutta (Teleostei: Salmonidae)? Molecular Phylogenetics and Evolution (107204) 162: 1-15, DOI: 10.1016/j.ympev.2021.107204, URL: https://doi.org/10.1016/j.ympev.2021.107204

Files

source.pdf

Files (3.0 MB)

Name Size Download all
md5:5f335944355fcb64cf0742c0ed92fcec
3.0 MB Preview Download

Linked records

Additional details

Identifiers

LSID
urn:lsid:plazi.org:pub:5F335944355FCB64CF07FFC0FF92FFEC

References

  • Aberer, A.J., Krompass, D., Stamatakis, A., 2011. RogueNaRok: An efficient and exact algorithm for rogue taxon identification. Heidelberg Institute for Theoretical Studies: Exelixis-RRDR-2011-10.
  • Aberer, A.J., Krompass, D., Stamatakis, A., 2012. Pruning rogue taxa improves phylogenetic accuracy: an efficient algorithm and webservice. Syst. Biol. 62, 162-166. https://doi.org/10.1093/sysbio/sys078.
  • Alda, F., Tagliacollo, V.A., Bernt, M.J., Waltz, B.T., Ludt, W.B., Faircloth, B.C., Alfaro, M. E., Albert, J.S., Chakrabarty, P., Near, T., 2019. Resolving deep nodes in an ancient radiation of neotropical fishes in the presence of conflicting signals from incomplete lineage sorting. Syst. Biol. 68 (4), 573-593. https://doi.org/10.1093/sysbio/syy085.
  • Alexander, D.H., Novembre, J., Lange, K., 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19 (9), 1655-1664. https://doi.org/10.1101/ gr.094052.109.
  • Alexandrou, M.A., Swartz, B.A., Matzke, N.J., Oakley, T.H., 2013. Genome duplication and multiple evolutionary origins of complex migratory behavior in Salmonidae. Mol. Phylogen. Evol. 69 (3), 514-523.
  • Aljanabi, S.M., Martinez, I., 1997. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res. 25, 4692-4693. https:// doi.org/10.1093/nar/25.22.4692.
  • Andrews, S., 2010. FastQC: a quality control tool for high throughput sequence data. [WWW document]. URL http://www.bioinformatics.babraham.ac.uk/projects/f astqc.
  • 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 (6), 551-560. https://doi.org/ 10.1038/hdy.1996.80.
  • Apostolidis, A., Stoumboudi, M.T., Kalogianni, E., Cote, G., Bernatchez, L., 2011. Genetic divergence among native trout Salmo trutta populations from southern Balkans based on mitochondrial DNA and microsatellite variation. J. Fish Biol. 79, 1950-1960. https://doi.org/10.1111/j.1095-8649.2011.03136.x.
  • Apostolidis, A.P., Loukovitis, D., Tsigenopoulos, C.S., 2008. Genetic characterization of brown trout (Salmo trutta) populations from the southern Balkans using mtDNA sequencing and RFLP analysis. Hydrobiologia 600 (1), 169-176.
  • April, J., Mayden, R.L., Hanner, R.H., Bernatchez, L., 2011. Genetic calibration of species diversity among North America' s freshwater fishes. Proc. Natl. Acad. Sci. 108 (26), 10602-10607.
  • Barbat-Leterrier, A., Guyomard, R., Krieg, F., 1989. Introgression between introduced domesticated strains and Mediterranean native populations of brown trout (Salmo trutta L.). Aquat. Living Resour. 2 (4), 215-223.
  • Bardakci, F., Degerli, N., Ozdemir, O., Basibuyuk, H.H., 2006. Phylogeography of the Turkish brown trout Salmo trutta L.: mitochondrial DNA PCR-RFLP variation. J. Fish Biol. 68 (A), 36-55. https://doi.org/10.1111/jfb.2006.68.issue-a10.1111/j.0022- 1112.2006.00948.x.
  • Bekkevold, D., H¨ojesj¨o, J., Nielsen, E.E., Aldv´en, D., Als, T.D., Sodeland, M., Kent, M.P., Lien, S., Hansen, M.M., 2020. Northern European Salmo trutta (L.) populations are genetically divergent across geographical regions and environmental gradients. Evol. applications 13 (2), 400-416.
  • Benestan, L., Gosselin, T., Perrier, C., Sainte-Marie, B., Rochette, R., Bernatchez, L., 2015. RAD genotyping reveals fine-scale genetic structuring and provides powerful population assignment in a widely distributed marine species, the American lobster (Homarus americanus). Mol. Ecol. 24 (13), 3299-3315. https://doi.org/10.1111/ mec.13245.
  • 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 (2), 351-379. https://doi.org/10.1111/evo.2001.55.issue-210.1111/j.0014-3820.2001.tb01300.x.
  • Bernatchez, L., Guyomard, R., Bonhomme, F., 1992. DNA sequence variation of the mitochondrial control region among geographically and morphologically remote European brown trout Saltmo trutta populations. Mol. Ecol. 1, 161-173. https://doi. org/10.1111/j.1365-294X.1992.tb00172.x.
  • Berrebi, P., 2015. Three brown trout Salmo trutta lineages in Corsica described through allozyme variation. J. Fish Biol. 86 (1), 60-73. https://doi.org/10.1111/jfb.12534.
  • Berrebi, P., Caputo Barucchi, V., Splendiani, A., Muracciole, S., Sabatini, A., Palmas, F., Tougard, C., Arculeo, M., Maric ´, S., 2019. brown trout (Salmo trutta L.) high genetic diversity around the Tyrrhenian Sea as revealed by nuclear and mitochondrial markers. Hydrobiologia 826 (1), 209-231.
  • Berrebi, P., Jesenˇsek, D., Crivelli, A.J., 2017. Natural and domestic introgressions in the marble trout population of Soca River (Slovenia). Hydrobiologia 785, 277-291.
  • Berrebi, P., Povz, M., Jesensek, D., Cattaneo-Berrebi, G., Crivelli, A.J., 2000. The genetic diversity of native, stocked and hybrid populations of marble trout in the Soca river, Slovenia. Heredity 85, 277-287. https://doi.org/10.1046/j.1365-2540.2000.00753. x.
  • Berrebi, P., Tougard, C., Dubois, S., Shao, Z., Koutseri, I., Petkovski, S., Crivelli, A.J., 2013. Genetic diversity and conservation of the Prespa trout in the Balkans. Int. J. Mol. Sci. 14 (12), 23454-23470. https://doi.org/10.3390/ijms141223454.
  • Bianco, P.G., 2014. An update on the status of native and exotic freshwater fishes of I taly. J. Appl. Ichthyol. 30 (1), 62-77. https://doi.org/10.1111/jai.12291.
  • Bouckaert, R., Heled, J., Kuhnert, D., Vaughan, T., Wu, C.-H., Xie, D., Suchard, M.A., Rambaut, A., Drummond, A.J., Prlic, A., 2014. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comp. Biol. 10 (4), e1003537. https://doi.org/ 10.1371/journal.pcbi.1003537.
  • Breiman, L., 2006. randomForest: Breiman and Cutler' s random forests for classification and regression. URL http://stat-www.berkeley.edu/users/breiman/RandomForests, R package version.
  • Catchen, J., Hohenlohe, P.A., Bassham, S., Amores, A., Cresko, W.A., 2013. Stacks: an analysis tool set for population genomics. Mol. Ecol. 22 (11), 3124-3140. https:// doi.org/10.1111/mec.12354.
  • Clement, M., Posada, D., Crandall, K.A., 2000. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9, 1657-1659. https://doi.org/10.1046/j.1365- 294x.2000.01020.x.
  • Crˆete-Lafreni`ere, A., Weir, L.K., Bernatchez, L., Fontaneto, D., 2012. Framing the Salmonidae family phylogenetic portrait: a more complete picture from increased taxon sampling. PLoS ONE 7 (10), e46662. https://doi.org/10.1371/journal. pone.0046662.
  • De Queiroz, K., 2007. Species concepts and species delimitation. Syst. Biol. 56, 879-886. https://doi.org/10.1080/10635150701701083.
  • Delling, B., 2002. Morphological distinction of the marble trout, Salmo marmoratus, in comparison to marbled Salmo trutta from River Otra, Norway. Cybium 26 (4), 283-300.
  • Delling, B., 2010. Diversity of western and southern Balkan trouts, with the description of a new species from the Louros River, Greece (Teleostei: Salmonidae). Ichthyol. Explor. Freshw. 21 (4), 331-344.
  • Delling, B., Crivelli, A.J., 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 (5), 1199-1212. https://doi.org/ 10.1111/jfb.2000.57.issue-510.1111/j.1095-8649.2000.tb00481.x.
  • Delling, B., Doadrio, I., 2005. Systematics of the trouts endemic to Moroccan lakes, with description of a new species (Teleostei: Salmonidae). Ichthyol. Explor. Freshwat. 16, 49-64.
  • Delling, B., Sabatini, A., Muracciole, S., Tougard, C., Berrebi, P., 2020. Morphologic and genetic characterisation of Corsican and Sardinian trout with comments on Salmo taxonomy. Knowl. Manag. Aquat. Ecosyst. 421, 21. https://doi.org/10.1051/kmae/ 2020013.
  • Doadrio, I., Perea, S., Yahyaoui, A., 2015. Two new species of Atlantic trout (Actinopterygii, Salmonidae) from Morocco. Graellsia 71 (2), e031. https://doi.org/ 10.3989/graellsia.2015.v71.i210.3989/graellsia.2015.v71.142.
  • Duftner, N., Weiss, S., Medgyesy, N., Sturmbauer, C., 2003. Enhanced phylogeographic information about Austrian brown trout populations derived from complete mitochondrial control region sequences. J. Fish Biol. 62, 427-435. https://doi.org/ 10.1046/j.1095-8649.2003.00038.x.
  • Edgar, R.C., 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32 (5), 1792-1797. https://doi.org/10.1093/nar/ gkh340.
  • Elliott, J.M., 1994. Quantitative Ecology and the brown trout. Oxford University Press.
  • Emerson, K.J., Merz, C.R., Catchen, J.M., Hohenlohe, P.A., Cresko, W.A., Bradshaw, W. E., Holzapfel, C.M., 2010. Resolving postglacial phylogeography using high-throughput sequencing. Proc. Natl. Acad. Sci. 107 (37), 16196-16200. https://doi. org/10.1073/pnas.1006538107.
  • Epitashvili, G., Geiger, M., Astrin, J., Herder, F., Japoshvili, B., Mumladze, L., 2020. Towards retrieving the Promethean treasure: a first molecular assessment of the freshwater fish diversity of Georgia. Biodivers. Data J. 8 https://doi.org/10.3897/ BDJ.8.e57862.
  • Ferguson, A., Mason, F.M., 1981. Allozyme evidence for reproductively isolated sympatric populations of brown trout Salmo trutta L. in Lough Melvin. Ireland. J. Fish Biol. 18 (6), 629-642. https://doi.org/10.1111/j.1095-8649.1981.tb03805.x.
  • Fern´andez-Mazuecos, M., Mellers, G., Vigalondo, B., S´aez, L., Vargas, P., Glover, B.J., 2017. Resolving recent plant radiations: power and robustness of genotyping-by-sequencing. Syst. Biol. 67, 250-268. https://doi.org/10.1093/sysbio/syx062.
  • Frankham, R., 2015. Genetic rescue of small inbred populations: Meta-analysis reveals large and consistent benefits of gene flow. Mol. Ecol. 24 (11), 2610-2618. https:// doi.org/10.1111/mec.13139.
  • Frankham, R., Ballou, J.D., Dudash, M.R., Eldridge, M.D.B., Fenster, C.B., Lacy, R.C., Mendelson, J.R., Porton, I.J., Ralls, K., Ryder, O.A., 2012. Implications of different species concepts for conserving biodiversity. Biol. Conserv. 153, 25-31.
  • Frankham, R., Ballou, J.D., Ralls, K., Eldridge, M., Dudash, M.R., Fenster, C.B., Lacy, R. C., Sunnucks, P., 2017. Genetic Management of Fragmented Animal and Plant Populations. Oxford University Press.
  • Fruciano, C., Pappalardo, A.M., Tigano, C., Ferrito, V., 2014. Phylogeographical relationships of Sicilian brown trout and the effects of genetic introgression on morphospace occupation. Biol. J. Linn. Soc. 112 (3), 387-398. https://doi.org/ 10.1111/bij.12279.
  • Garc´Ia-Mar´In, J.L., Utter, F.M., Pla, C., 1999. Postglacial colonization of brown trout in Europe based on distribution of allozyme variants. Heredity 82, 46-56. https://doi. org/10.1046/j.1365-2540.1999.00447.x.
  • Geiger, M.F., Herder, F., Monaghan, M.T., Almada, V., Barbieri, R., Bariche, M., Berrebi, P., Bohlen, J., Casal-Lopez, M., Delmastro, G.B., Denys, G.P.J., Dettai, A., Doadrio, I., Kalogianni, E., K¨arst, H., Kottelat, M., Kovaˇci´c, M., Laporte, M., Lorenzoni, M., Marˇci´c, Z., Ozulu ¨˘g, M., Perdices, A., Perea, S., Persat, H., Porcelotti, S., Puzzi, C., Robalo, J., ˇSanda, R., Schneider, M., ˇSlechtov´a, V., Stoumboudi, M., Walter, S., Freyhof, J., 2014. Spatial heterogeneity in the Mediterranean Biodiversity Hotspot affects barcoding accuracy of its freshwater fishes. Mol. Ecol. Resour. 14 (6), 1210-1221. https://doi.org/10.1111/1755- 0998.12257.
  • 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, 161-171. https://doi.org/10.1111/ j.1365-294X.1994.tb00117.x.
  • 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 (2), 207-220.
  • Gratton, P., Allegrucci, G., Sbordoni, V., Gandolfi, A., 2014. The evolutionary jigsaw puzzle of the surviving trout (Salmo trutta L. complex) diversity in the Italian region. A multilocus Bayesian approach. Mol. Phylogen. Evol. 79, 292-304. https://doi.org/ 10.1016/j.ympev.2014.06.022.
  • Griffiths, A.M., Bright, D., Stevens, J.R., 2009. Complete mitochondrial control region sequences indicate a distinct variety of brown trout Salmo trutta in the Aral Sea. J. Fish Biol. 74 (5), 1136-1142.
  • Hall, T., 2005. BioEdit. Version 7.2. 5 Biological sequence alignment editor for Win95/ 98/NT/2K/XP.
  • Hallerman, E.M., 2003. Population genetics: principles and applications for fisheries scientists.
  • Hashemzadeh Segherloo, I., Farahmand, H., Abdoli, A., Bernatchez, L., Primmer, C., Swatdipong, A., Karami, M., Khalili, B., 2012. Phylogenetic status of brown trout Salmo trutta populations in five rivers from the southern Caspian Sea and two inland lake basins, Iran: a morphogenetic approach. J. Fish Biol. 81, 1479-1500. https:// doi.org/10.1111/j.1095-8649.2012.03428.x.
  • Huson, D.H., Bryant, D., 2005. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23, 254-267. https://doi.org/10.1093/molbev/msj030.
  • Jombart, T., Collins, C., 2015. A tutorial for discriminant analysis of principal components (DAPC) using adegenet 2.0.0. London: Imperial College London, MRC Centre for Outbreak Analysis and Modelling. https://adegenet.r-forge.r-project.org /files/tutorial-dapc.pdf.
  • 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 (3), 381-388.
  • Kara, C., Alp, A., Gurlek, M.E., 2011. Morphological variations of the trouts (Salmo trutta and Salmo platycephalus) in the rivers of Ceyhan, Seyhan and Euphrates, Turkey. Turkish J. Fish. Aquat. Sci. 11 (1), 77-85.
  • Kass, R.E., Raftery, A.E., 1995. Bayes factors. J. American Statistical Association 90, 773- 795. https://doi.org/10.1080/01621459.1995.10476572.
  • Keinan, A., Mullikin, J.C., Patterson, N., Reich, D., 2007. Measurement of the human allele frequency spectrum demonstrates greater genetic drift in East Asians than in Europeans. Nat. Genet. 39 (10), 1251-1255. https://doi.org/10.1038/ng2116.
  • Kohout, J., ˇSediv´a, A., Apostolou, A., Stefanov, T., Mari´c, S., Gaffaro˘glu, M., ˇSlechta, V., 2013. Genetic diversity and phylogenetic origin of brown trout Salmo trutta populations in eastern Balkans. Biologia 68 (6), 1229-1237.
  • Kottelat, M., Freyhof, J.R., 2007. Handbook of European Freshwater Fishes. Publications Kottelat, Cornol, Switzerland.
  • Kumar, S., Stecher, G., Tamura, K., 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33 (7), 1870-1874. https:// doi.org/10.1093/molbev/msw054.
  • Leach´e, A.D., Bouckaert, R.R., 2018. Species trees and species delimitation with SNAPP: a tutorial and worked example. Workshop on Population and Speciation Genomics, Cesky ˇKrumlov, Czech Republic. http://evomicsorg.wpengine.netdna-cdn. com/wp-content/uploads/2018/01/BFD-tutorial-1.pdf.
  • Leach´e, A.D., Fujita, M.K., Minin, V.N., Bouckaert, R.R., 2014. Species delimitation using genome-wide SNP data. Syst. Biol. 63, 534-542. https://doi.org/10.1093/sysbio/ syu018.
  • Lobon-Cervi ´´a, J., Esteve, M., Berrebi, P., Duchi, A., Lorenzoni, M., Young, K.A., 2018. Trout and char of central and Southern Europe and Northern Africa. In: Kershner, J., Williams, J., Lobon-Cervi ´´a, J., Gresswell, B. (Eds.), Trout and char of the world. American Fisheries Society, Bethesda, Maryland, pp. 1-32.
  • Lecaudey, L.A., Schliewen, U.K., Osinov, A.G., Taylor, E.B., Bernatchez, L., Weiss, S.J., 2018. Inferring phylogenetic structure, hybridization and divergence times within Salmoninae (Teleostei: Salmonidae) using RAD-sequencing. Mol. Phylogen. Evol. 124, 82-99. https://doi.org/10.1016/j.ympev.2018.02.022.
  • Lerceteau-K¨ohler, E., Schliewen, U., Kopun, T., Weiss, S., 2013. Genetic variation in brown trout Salmo trutta across the Danube, Rhine, and Elbe headwaters: a failure of the phylogeographic paradigm? BMC Evol. Biol. 13 (1), 176. https://doi.org/ 10.1186/1471-2148-13-176.
  • Levin, B., Simonov, E., Rastorguev, S., Boulygina, E., Sharko, F., Tsygankova, S., Gabrielyan, B., Roubenyan, H., Mayden, R., Nedoluzhko, A., 2018. High-throughput sequencing of the mitochondrial genomes from archived fish scales: an example of the endangered putative species flock of Sevan trout Salmo ischchan. Hydrobiologia 822 (1), 217-228. https://doi.org/10.1007/s10750-018-3688-7.
  • Lien, S., Koop, B.F., Sandve, S.R., Miller, J.R., Kent, M.P., Nome, T., Hvidsten, T.R., Leong, J.S., Minkley, D.R., Zimin, A., Grammes, F., Grove, H., Gjuvsland, A., Walenz, B., Hermansen, R.A., von Schalburg, K., Rondeau, E.B., Di Genova, A., Samy, J.K.A., Olav Vik, J., Vigeland, M.D., Caler, L., Grimholt, U., Jentoft, S., Inge Vage, D., de Jong, P., Moen, T., Baranski, M., Palti, Y., Smith, D.R., Yorke, J.A., Nederbragt, A.J., Tooming-Klunderud, A., Jakobsen, K.S., Jiang, X., Fan, D., Hu, Y., Liberles, D.A., Vidal, R., Iturra, P., Jones, S.J.M., Jonassen, I., Maass, A., Omholt, S. W., Davidson, W.S., 2016. The Atlantic salmon genome provides insights into rediploidization. Nature 533 (7602), 200-205. https://doi.org/10.1038/ nature17164.
  • Lo Brutto, S., Hristovski, N., Arculeo, M., 2010. Genetic divergence between morphological forms of brown trout Salmo trutta L. in the Balkan region of Macedonia. J. Fish Biol. 76, 1220-1227. https://doi.org/10.1111/j.1095- 8649.2010.02595.x.
  • Mace, G.M., 2004. The role of taxonomy in species conservation. Philos. Trans. R. Soc. Lond. B. Biol. Sci., 359(1444), 711-719. https://doi.org/10.1098/rstb.2003.1454.
  • MacGuigan, D.J., Near, T.J., Cormack, J.M., 2019. Phylogenomic signatures of ancient introgression in a rogue lineage of darters (Teleostei: Percidae). Syst. Biol. 68 (2), 329-346. https://doi.org/10.1093/sysbio/syy074.
  • Machordom, A., Suarez, J., Almodovar, A., Bautista, J.M., 2000. Mitochondrial haplotype variation and phylogeography of Iberian brown trout populations. Mol. Ecol. 9 (9), 1324-1338. https://doi.org/10.1046/j.1365-294x.2000.01015.x.
  • Mari´c, S., Bajec, S.S., Sch¨offmann, J., Kostov, V., Snoj, A., 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 (1), 249-260. https://doi.org/10.1007/s10750-016-2930-4.
  • Martin, M., 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 10-12. https://doi.org/10.14806/ej.17.1.200.
  • Mascher, M., Wu, S., Amand, P.S., Stein, N., Poland, J., Candela, H., 2013. Application of genotyping-by-sequencing on semiconductor sequencing platforms: a comparison of genetic and reference-based marker ordering in barley. PLoS ONE 8 (10), e76925. https://doi.org/10.1371/journal.pone.0076925.
  • Meldgaard, T., Crivelli, A.J., Jesensek, D., Poizat, G., Rubin, J.-F., 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. Conserv. 136 (4), 602-611.
  • Melville, J., Haines, M.L., Boysen, K., Hodkinson, L., Kilian, A., Smith Date, K.L., Potvin, D.A., Parris, K.M., 2017. Identifying hybridization and admixture using SNPs: application of the DArTseq platform in phylogeographic research on vertebrates. R. Soc. Open Sci. 4 (7), 161061. https://doi.org/10.1098/rsos.161061.
  • 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 (1), 337-349. https://doi.org/10.1007/s10750-006-0479-3.
  • Moran, P., Pendas, A.M., Garcia-Vazquez, E., Izquierdo, J.I., Lobon-Cervla, J., 1995. Estimates of gene flow among neighbouring populations of brown trout. J. Fish Biol. 46 (4), 593-602. https://doi.org/10.1111/j.1095-8649.1995.tb01099.x.
  • Ninua, L., Tarkhnishvili, D., Gvazava, E., 2018. Phylogeography and taxonomic status of trout and salmon from the Ponto-Caspian drainages, with inferences on European brown trout evolution and taxonomy. Ecol. Evol. 8 (5), 2645-2658. https://doi.org/ 10.1002/ece3.3884.
  • Osinov, A., Bernatchez, L., 1996. Atlantic and Danubian phylogenetic groupings of brown trout Salmo trutta complex: genetic divergence, evolution, and conservation. J. Ichthyol. 36, 723-746.
  • Palandaˇcic ´, A., Naseka, A., Ramler, D., Ahnelt, H., 2017. Contrasting morphology with molecular data: an approach to revision of species complexes based on the example of European Phoxinus (Cyprinidae). BMC Evol. Biol. 17, 184. https://doi.org/ 10.1186/s12862-017-1032-x.
  • Patterson, N., Moorjani, P., Luo, Y., Mallick, S., Rohland, N., Zhan, Y., Genschoreck, T., Webster, T., Reich, D., 2012. Ancient admixture in human history. Genetics 192, 1065-1093. https://doi.org/10.1534/genetics.112.145037.
  • Pickrell, J.K., Pritchard, J.K., 2012. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 8, e1002967 https://doi.org/ 10.1038/npre.2012.6956.1.
  • Presa, P., Pardo, B., Martinez, P., Bernatchez, L., 2002. Phylogeographic congruence between mtDNA and rDNA ITS markers in brown trout. Mol. Biol. Evol. 19, 2161-2175. https://doi.org/10.1093/oxfordjournals.molbev.a004041.
  • Pustovrh, G., Snoj, A., Bajec, S., 2014. Molecular phylogeny of Salmo of the western Balkans, based upon multiple nuclear loci. Genet. Sel. Evol. 46 (1), 7. https://doi. org/10.1186/1297-9686-46-7.
  • Razpet, A., Suˇsnik, S., Jug, T., Snoj, A., 2007. Genetic variation among trout in the River Neretva basin. Bosnia and Herzegovina. J. Fish Biol. 70 (sa), 94-110. https://doi. org/10.1111/j.1095-8649.2007.01392.x.
  • Reich, D., Thangaraj, K., Patterson, N., Price, A.L., Singh, L., 2009. Reconstructing Indian population history. Nature 461 (7263), 489-494. https://doi.org/10.1038/ nature08365.
  • Roycroft, E.J., Moussalli, A., Rowe, K.C., 2019. Phylogenomics uncovers confidence and conflict in the rapid radiation of Australo-Papuan todents. Syst. Biol. 69 (3), 431-444. https://doi.org/10.1093/sysbio/syz044.
  • Rozas, J., Ferrer-Mata, A., S´anchez-DelBarrio, J.C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S.E., S´anchez-Gracia, A., 2017. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34, 3299-3302. https://doi.org/10.1093/ molbev/msx248.
  • Russo, C.A.d.M., Selvatti, A.P., Tamura, K., 2018. Bootstrap and rogue identification tests for phylogenetic analyses. Mol. Biol. Evol. 35 (9), 2327-2333. https://doi.org/ 10.1093/molbev/msy118.
  • Sabatini, A., Podda, C., Frau, G., Cani, M.V., Musu, A., Serra, M., Palmas, F., 2018. Restoration of native Mediterranean brown trout Salmo cettii Rafinesque, 1810 (Actinopterygii: Salmonidae) populations using an electric barrier as a mitigation tool. Eur. Zool. J. 85 (1), 137-149.
  • Sanz, N., 2018. In: Brown Trout: Biology, Ecology and Management. John Wiley & Sons, Ltd, Chichester, UK, pp. 15-63. https://doi.org/10.1002/9781119268352.ch2.
  • Sch¨offmann, J., Suˇsnik, S., Snoj, A., 2007. Phylogenetic origin of Salmo trutta L 1758 from Sicily, based on mitochondrial and nuclear DNA analyses. Hydrobiologia 575 (1), 51-55. https://doi.org/10.1007/s10750-006-0281-2.
  • Silvestro, D., Michalak, I., 2012. raxmlGUI: a graphical front-end for RAxML. Org. Divers. Evol. 12 (4), 335-337. https://doi.org/10.1007/s13127-011-0056-0.
  • Snoj, A., Glamuzina, B., Razpet, A., Zablocki, J., Bogut, I., Lerceteau-Kohler ¨, E., Pojski´c, N., Suˇsnik, S., 2010. Resolving taxonomic uncertainties using molecular systematics: Salmo dentex and the Balkan trout community. Hydrobiologia 651 (1), 199-212. https://doi.org/10.1007/s10750-010-0297-5.
  • Snoj, A., Mari´c, S., Bajec, S.S., Berrebi, P., Janjani, S., Schoffmann ¨, J., 2011. Phylogeographic structure and demographic patterns of brown trout in North-West Africa. Mol. Phylogen. Evol. 61 (1), 203-211. https://doi.org/10.1016/j. ympev.2011.05.011.
  • Snoj, A., Mari´c, S., Berrebi, P., Crivelli, A.J., Shumka, S., Suˇsnik, S., 2009. Genetic architecture of trout from Albania as revealed by mtDNA control region variation. Genet. Sel. Evol. 41 (1), 22. https://doi.org/10.1186/1297-9686-41-22.
  • Snoj, A., Melkic ˇ, E., Suˇsnik, S., Muhamedagi´c, S., Dovˇc, P., 2002. DNA phylogeny supports revised classification of Salmothymus obtusirostris. Biol. J. Linn. Soc. 77 (3), 399-411. https://doi.org/10.1046/j.1095-8312.2002.00130.x.
  • Splendiani, A., Fioravanti, T., Giovannotti, M., Olivieri, L., Ruggeri, P., Nisi Cerioni, P., Vanni, S., Enrichetti, F., Caputo Barucchi, V., 2017. Museum samples could help to reconstruct the original distribution of Salmo trutta complex in Italy. J. Fish Biol. 90 (6), 2443-2451.
  • Splendiani, A., Palmas, F., Sabatini, A., Caputo Barucchi, V., 2019. The name of the trout: considerations on the taxonomic status of the Salmo trutta L., 1758 complex (Osteichthyes: Salmonidae) in Italy. Eur. Zool. J. 86 (1), 432-442. https://doi.org/ 10.1080/24750263.2019.1686544.
  • Su´arez, J., Bautista, J.M., Almod´ovar, A., Machordom, A., 2001. Evolution of the mitochondrial control region in Palaearctic brown trout (Salmo trutta) populations: the biogeographical role of the Iberian Peninsula. Heredity 87 (2), 198-206. https:// doi.org/10.1046/j.1365-2540.2001.00905.x.
  • Susnik, S., Knizhin, I., Snoj, A., Weiss, S., 2006. Genetic and morphological characterization of a Lake Ohrid endemic, Salmo (Acantholingua) ohridanus with a comparison to sympatric Salmo trutta. J. Fish Biol. 68 (A), 2-23. https://doi.org/ 10.1111/j.0022-1112.2006.00902.x.
  • Suˇsnik Bajec, S., Pustovrh, G., Jesenˇsek, D., Snoj, A., 2015. Population genetic SNP analysis of marble and brown trout in a hybridization zone of the Adriatic watershed in Slovenia. Biol. Conserv. 184, 239-250.
  • Susnik, S., Schoffmann, J., Snoj, A., 2004. Phylogenetic position of Salmo (Platysalm o) platycephalu s Behnke 1968 from south-central Turkey, evidenced by genetic data. J. Fish Biol. 64 (4), 947-960. https://doi.org/10.1111/j.1095-8649.2004.0363.x.
  • Suˇsnik, S., Snoj, A., Wilson, I.F., Mrdak, D., Weiss, S., 2007a. Historical demography of brown trout (Salmo trutta) in the Adriatic drainage including the putative S. letnica endemic to Lake Ohrid. Mol. Phylogen. Evol. 44 (1), 63-76. https://doi.org/ 10.1016/j.ympev.2006.08.021.
  • Suˇsnik, S., Weiss, S., Odak, T., Delling, B., Treer, T., Snoj, A., 2007b. Reticulate evolution: ancient introgression of the Adriatic brown trout mtDNA in softmouth trout Salmo obtusirostris (Teleostei: Salmonidae). Biol. J. Linn. Soc. 90 (1), 139-152.
  • Swofford, D.L., 2002. Phylogenetic Analysis Using Parsimony (* and other methods). Version.
  • Templeton, A.R., 2004. Using haplotype trees for phylogeographic and species inference in fish populations. Environ. Biol. Fishes. 69 (1-4), 7-20. https://doi.org/10.1023/B: EBFI.0000022870.76912.0c.
  • Tougard, C., Justy, F., Guinand, B., Douzery, E.J., Berrebi, P., 2018. Salmo macrostigma (Teleostei, Salmonidae): Nothing more than a brown trout (S. trutta) lineage? J. Fish Biol. 93, 302-310. https://doi.org/10.1111/jfb.13751.
  • Turan, D., Kalaycι, G., Bektas, Y., Kaya, C., Baycelebi, E., 2020. A new species of trout from the northern drainages of Euphrates River, Turkey (Salmoniformes: Salmonidae). J. Fish Biol. 96 (6), 1454-1462. https://doi.org/10.1111/jfb. v96.610.1111/jfb.14321.
  • Turan, D., Kottelat, M., Bektas, Y., 2011. Salmo tigridis, a new species of trout from the Tigris River, Turkey (Teleostei: Salmonidae). Zootaxa 2993, 23-33.
  • Turan, D., Kottelat, M., Engin, S., 2009. Two new species of trouts, resident and migratory, sympatric in streams of northern Anatolia (Salmoniformes: Salmonidae). Ichthyol. Explor. Freshwat. 20, 333-364.
  • Turan, D., Kottelat, M., Engin, S., 2014. Two new species of trouts from the Euphrates drainage, Turkey (Teleostei: Salmonidae). Ichthyol. Explor. Freshwat. 24, 275-287.
  • Turan, D., Kottelat, M., Kaya, C., 2017. Salmo munzuricus, a new species of trout from the Euphrates River drainage, Turkey (Teleostei: Salmonidae). Ichthyol. Explor. Freshwat. 28, 55-63.
  • Waples, R.S., 1991. Genetic interactions between hatchery and wild salmonids: lessons from the Pacific Northwest. Can. J. Fish. Aquat. Sci. 48 (S1), 124-133. https://doi. org/10.1139/f91-311.
  • Weiss, S., Schlotterer, C., Waidbacher, H., Jungwirth, M., 2001. Haplotype (mtDNA) diversity of brown trout Salmo trutta in tributaries of the Austrian Danube: massive introgression of Atlantic basin fish -by man or nature? Mol. Ecol. 10 (5), 1241-1246. https://doi.org/10.1046/j.1365-294X.2001.01261.x.
  • Whiteley, A.R., Fitzpatrick, S.W., Funk, W.C., Tallmon, D.A., 2015. Genetic rescue to the rescue. Trends Ecol. Evol. 30 (1), 42-49. https://doi.org/10.1016/j. tree.2014.10.009.
  • Zaccara, S., Trasforini, S., Antognazza, C.M., Puzzi, C., Britton, J.R., Crosa, G., 2015. Morphological and genetic characterization of Sardinian trout Salmo cettii Rafinesque, 1810 and their conservation implications. Hydrobiologia 760 (1), 205-223. https://doi.org/10.1007/s10750-015-2322-1.
  • Zachos, F.E., 2018. (New) Species concepts, species delimitation and the inherent limitations of taxonomy. J. Genetics 97 (4), 811-815. https://doi.org/10.1007/ s12041-018-0965-1.