Phylogenetic Analysis of Native Salmo Species in Türkiye Using Mitochondrial 12S rDNA, 16S rDNA, Cytochrome b Sequences, and Cytogenetics
DOI:
https://doi.org/10.24925/turjaf.v14i6.1564-1576.8639Keywords:
Mitochondrial DNA, Salmo sp., Cytogenetic analysis , Phylogenetic, KaryotypeAbstract
In this study, phylogenetic relationships and genetic diversity of Salmo spp. populations in different water bodies in Türkiye were investigated, focusing on morphologically similar specimens to Salmo macrostigma. Significant genetic variability and evolutionary differentiation within these populations have been identified using mitochondrial regions sequences (12S rDNA, 16S rDNA, and Cyt-b), morphological observations, and cytogenetic analysis. Samples collected from eight river basins revealed three main phylogenetic clades and local adaptations influenced by ecological pressures. Cytogenetic findings showed that they have chromosome numbers ranging from 78 to 80 (2n), consistent with known Salmo species. For this purpose, three mitochondrial DNA fragments encoding 12S rDNA, 16S rDNA, and Cyt-b regions were amplified by PCR, sequenced, and then used for phylogenetic analysis of the studied species. The study revealed the need for comprehensive integrative taxonomic approaches to clarify the classification of Salmo spp. with critical implications for conservation strategies in Türkiye biodiversity hotspots. In conclusion, this study not only advances our knowledge of Salmo macrostigma or similar Salmo spp., but also suggests innovative approaches for future Salmonid phylogenetics and cytogenetics studies. The findings have important implications for understanding the evolution, taxonomy, and conservation of these economically and ecologically important fish.
References
Apostolidis, A.P., Triantaphyllidis, C., Kouvatsi, A. & Economidis, P.S. (1997). Mitochondrial DNA sequence variation and phylogeography among Salmo trutta L. (Greek brown trout) populations. Molecular Ecology, 6, 531-542. https://doi.org/10.1046/j.1365-294X.1997.d01-176.x
Bardakci, F., Degerli, N.A.C.İ., Ozdemir, O. & Basibuyuk, H.H. (2006). Phylogeography of the Turkish brown trout Salmo trutta L.: mitochondrial DNA PCR‐RFLP variation. Journal of Fish Biology, 68(A), 36-55. https://doi.org/10.1111/j.0022-1112.2006.00948.x
Baumsteiger, J., Moyle, P.B., Aguilar, A., O’Rourke, S.M. & Miller, M.R. (2017). Genomics clarifies taxonomic boundaries in a difficult species complex. PLoS One 12, e0189417. https://doi.org/10.1371/journal.pone.0189417
Berg, L.S. (1908). Vorläufige Bemerkungen über die europäisch-asiatischen Salmoniden, insbesondere die Gattung Thymallus. Annuaire du Musée Zoologique de l’Academie Imperiale des Sciences de St. Petersbourg. 12, 500-514.
Bernatchez, L. & Osinov, A. (1995). Genetic diversity of trout (genus Salmo) from its most eastern native range based on mitochondrial DNA and nuclear gene variation. Molecular Ecology, 4, 285-298. https://doi.org/10.1111/j.1365-294X.1995.tb00222.x
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. https://doi.org/10.1111/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 Salmo trutta populations. Molecular Ecology, 1, 161-173. https://doi.org/10.1111/j.1365-294X.1992.tb00172.x
Caballero, P., Cobo, F. & González, M.A. (2006). Life history of a sea trout (Salmo trutta L.) population from the north-west Iberian Peninsula (River Ulla, Galicia, Spain). Sea Trout: Biology, Conservation and Management. 234-247. https://doi.org/10.1002/9780470996027
Cortey, M., Pla, C. & García-Marín, J.L. (2004). Historical biogeography of Mediterranean trout. Molecular Phylogenetics and Evolution, 33, 831-844. https://doi.org/10.1016/j.ympev.2004.08.012
Coulson, M.W., Marshall, H.D., Pepin, P. & Carr, S.M. (2006). Mitochondrial genomics of gadine fishes: implications for taxonomy and biogeographic origins from whole-genome data sets. Genome, 49(9), 1115-1130.
Crespi, B.J. & Fulton, M.J. (2004). Molecular systematics of Salmonidae: combined nuclear data yields a robust phylogeny. Molecular phylogenetics and evolution, 31, 658-679. https://doi.org/10.1016/j.ympev.2003.08.012
Delling, B. (2003). Species diversity and phylogeny of Salmo with emphasis on southern trouts (Teleostei, Salmonidae). Zoologiska institutionen, Stockholms Universitet.
Doadrio, I., Perea, S. & Yahyaoui, A. (2015). Two new species of Atlantic trout (Actinopterygii, Salmonidae) from Morocco. Graellsia, 71(2), e031.
Ehrlich, P.R. & Wilson, E.O. (1991). Biodiversity studies: science and policy. Science, 253(5021), 758-762. https://doi.org/10.1126/science.253.5021.758
Englmaier, G.K, Rodríguez, N.V., Bravničar, J., Zangl, L., Persat, H., Marić, S., Ratschan, C., Delling, B., Gonçalves, D.V., Secci-Petretto, G., Froufe, E. & Weiss, S.J. (2024). SNP‐based analysis of European Thymallus spp. (Salmonidae) reveals extensive mito‐nuclear discordance relevant for biogeographic inferences, taxonomy and conservation. Diversity and Distributions, e13845 https://doi.org/10.1111/ddi.13845
Felsenstein, J. (2004). PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. http://www.evolution.gs.washington.edu/phylip.html;
Ferguson, A. (2004). The importance of identifying conservation units: brown trout and pollan biodiversity in Ireland. In Biology and Environment: Proceedings of the Royal Irish Academy (Vol. 104, No. 3, pp. 33-41). Royal Irish Academy.
Freudenstein, J.V., Broe, M.B., Folk, R.A. & Sinn, B.T. (2017). Biodiversity and the species concept—lineages are not enough. Systematic Biology, 66(4), 644-656.
Froese, R. & Pauly, D. (2024). World Wide Web electronic publication. FishBase. Version (01/2024). Available online: https://www.fishbase.se/summary/Salmo-trutta.html (accessed on 19 August 2024).
Fujiwara, A., Nishida-Umehara, C., Sakamoto, T., Okamoto, N., Nakayama, I. & Abe, S. (2011). Improved fish lymphocyte culture for chromosome preparation. Genetica 111. 77-89. https://doi.org/10.1023/A:1013788626712
Gibertoni, P., Jelli, F. & Bracchi, P. (1998). Allevamento, riproduzione e reintroduzione in ambiente naturale di trote fario di ‘ceppo mediterraneo’, Salmo (trutta) trutta, L. Annali della Facoltà di Medicina Veterinaria, 18. 1-20
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. Molecular Ecology, 3, 161-171. https://doi.org/10.1111/j.1365-294X.1994.tb00117.x
Hall, T.A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In Nucleic acids symposium series, 41, 95-98.
Hansen, T., Fjelldal, P.G., Lien, S., Smith, M., Corton, C., Oliver, K., Skelton, J., Betteridge, E., Doulcan, J., Fedrigo, O., Mountcastle, J., Jarvis, E., A McCarthy, S., Chow, W., Howe, K., Torrance, J., Wood, J., Sims, Y., Haggerty, L., Challis, R., Threlfall, J., Mead, D., Durbin, R. & Blaxter, M. (2021). The genome sequence of the brown trout, Salmo trutta Linnaeus 1758. Wellcome Open Research 6, 16838. https://doi.org/10.12688/wellcomeopenres.16838.1
Houston, R.D. & Macqueen, D.J. (2019). Atlantic salmon (Salmo salar L.) genetics in the 21st century: taking leaps forward in aquaculture and biological understanding. Animal Genetics 50, 3-14. https://doi.org/10.1111/age.12748
Iaffaldano, N., Di Iorio, M., Manchisi, A., Esposito, S. & Gibertoni, P.P. (2016). Effective freezing rate for semen cryopreservation in endangered Mediterranean brown trout (Salmo trutta macrostigma) inhabiting the Biferno river (South Italy). Zygote 24. 668-676. https://doi.org/10.1017/S0967199415000647
Kocabas, M. (2009). Comparison of Growth Performance and Morphologic Characteristics of Brown Trout (Salmo trutta) Ecotypes of Turkey. Karadeniz Technical University.
Kottelat, M. (1997). European freshwater fishes. Biologia, 52(5), 1-271.
Kottelat, M., & Freyhof, J. (2007). Handbook of European freshwater fishes (Vol. 13). Cornol, Switzerland: Publications Kottelat.
Küçük, F., Kalaycı, G., Güçlü, S. S., Oral, M. & Turan, D. (2024). A new species of trout from the Köprüçay River, a drainage of Mediterranean Sea, Türkiye (Salmoniformes, Salmonidae). Zoosystematics and Evolution, 100(2), 391-403.
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular biology and evolution, 35(6), 1547-1549. https://doi.org/10.1093/molbev/msy096
Letunic, I. & Bork, P. (2019). Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic acids research. 47, W256-W259. https://doi.org/10.1093/nar/gkz239
Librado, P., Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25. 1451-1452. https://doi.org/10.1093/bioinformatics/btp187
Machordom, A., Suárez, J., Almodóvar, A. & Bautista, J.M. (2000). Mitochondrial haplotype variation and phylogeography of Iberian brown trout populations. Molecular Ecology, 9(9), 1324-1338. https://doi.org/10.1046/j.1365-294x.2000.01015.x
Martin, A.P & Palumbi, S.R. (1993). Body size, metabolic rate, generation time, and the molecular clock. Proceedings of the National Academy of Sciences, 90, 4087-4091. https://doi.org/10.1073/pnas.90.9.4087
Mayrose, I., & Lysak, M. A. (2021). The evolution of chromosome numbers: mechanistic models and experimental approaches. Genome biology and evolution, 13(2), evaa220.
Mearelli, M., Giovinazzo, G., Lorenzoni, M., Carosi, A., Petesse, M.L., Fanò, G. & Lisciarelli M. (1995). Recupero di ceppi autoctoni di Trota fario Salmo (trutta) trutta L. nel bacino umbro del F. Nera: Schema metodologico e risultati preliminari. Biol Ambientale. 5, 10-18.
Miya, M. & Nishida, M. (2015). The mitogenomic contributions to molecular phylogenetics and evolution of fishes: a 15-year retrospect. Ichthyological Research, 62, 29-71. https://doi.org/10.1007/s10228-014-0440-9
Netto, M.R.D.C.B, Pauls, E. & de Mello Affonso, P.R.A.A. (2007). standard protocol for obtaining fish chromosomes under post-mortem conditions. Micron, 38. 214-217. https://doi.org/10.1016/j.micron.2006.07.019
Noakes, D.J. (2014). Overview of salmon and their ecological and economic importance. Salmon. Biology, Ecological Impacts and Economic Importance.
Okumuş, İ., Kurtoglu, I. Z., & Atasaral, Ş. (2007). General overview of Turkish sea trout (Salmo trutta L.) populations. Sea trout: Biology, conservation and management, 115-127.
Okumus, I., Kurtoglu, I.Z. & Atasaral, S. (2006). General overview of Turkish sea trout (Salmo trutta L.) populations. Sea trout: Biology, conservation and management. 115-127. https://doi.org/10.1002/9780470996027
Poretsky, R., Rodriguez-R, L.M. & Luo, C. (2014). Tsementzi D, Konstantinidis KT. Strengths and limitations of 16S rRNA gene amplicon sequencing in revealing temporal microbial community dynamics. PLoS One. 9, e93827. https://doi.org/10.1371/journal.pone.0093827
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D.L., Darling, A., Höhna, S. & Huelsenbeck, J.P. (2012). MRBAYES 3.2: Efficient Bayesian phylogenetic inference and model selection across a large model space. Systematic biology, 61, 539-542 https://doi.org/10.1093/sysbio/sys029
Saenjundaeng, P., De Bello Cioffi, M., de Oliveira, E.A., Tanomtong, A., Supiwong, W., Phimphan, S., Collares-Pereira, M.J., Sember, A., Bertollo, L.A.C., Liehr, T., Yano, C.F., Hatanaka, T. & Ráb, P. (2018). Chromosomes of Asian cyprinid fishes: cytogenetic analysis of two representatives of small paleotetraploid tribe Probarbini. Molecular Cytogenetics, 11, 1-9. https://doi.org/10.1186/s13039-018-0399-8
Saitou, N. & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular biology and evolution. 4, 406-425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989). Molecular Cloning. A Laboratory Manual. Cold Spring Harbor Laboratory Press.
Schultz, N.E., Lane, C.E., Gall, L.L., Gey, D., Bigney, A.R., Reviers, B.D., Rousseau, F., Craig, W. & Schneider, C.W. (2015). A barcode analysis of the genus Lobophora (Dictyotales, Phaeophyceae) in the western Atlantic Ocean with four novel species and the epitypification of L. variegata (JV Lamouroux) EC Oliveira. european Journal of Phycology, 50, 481-500. https://doi.org/10.1080/09670262.2015.1078500
Shedko, S.V., Miroshnichenko, I.L. & Nemkova, G.A. (2013). Phylogeny of salmonids (Salmoniformes: Salmonidae) and its molecular dating: analysis of mtDNA data. Russian Journal of Genetics, 49. 623-637. https://doi.org/10.1134/S1022795413060112
Shen, K.N., Jamandre, B.W., Hsu, C.C., Tzeng, W.N. & Durand, J.D. (2011) Plio-Pleistocene sea level and temperature fluctuations in the northwestern Pacific promoted speciation in the globally-distributed flathead mullet Mugil cephalus. BMC evolutionary biology, 11, 1-17.
Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H., & Flook, P. (1994). Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the entomological Society of America, 87(6), 651-701.
Simons, A.M. & Mayden, R.L. (1998). Phylogenetic relationships of the western North American phoxinins (Actinopterygii: Cyprinidae) as inferred from mitochondrial 12S and 16S ribosomal RNA sequences. Molecular Phylogenetics and Evolution, 9, 308-329. https://doi.org/10.1006/mpev.1997.0467
Skaala, Ø. & Solberg, G. (1997). Biochemical genetic variability and taxonomy of a marmorated salmonid in River Otra, Norway. Nord. J Freshw Res. 3-12.
Snoj, A., Marić, S., Bajec, S.S., Berrebi, P., Janjani, S. & Schöffmann, J.A. (2011). Phylogeographic structure and demographic patterns of brown trout in North-West Africa. Molecular Phylogenetics and Evolution. 61, 203-211. https://doi.org/10.1016/j.ympev.2011.05.011
Suárez, J., Bautista, J.M., Almodóvar, 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
Tamura, K. & Nei, M. (1993) .Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular biology and evolution, 10, 512-526. https://doi.org/10.1093/oxfordjournals.molbev.a040023
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic acids research, 22, 4673-4680. https://doi.org/10.1093/nar/22.22.4673
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?. Journal of Fish Biology, 93, 302-310. https://doi.org/10.1111/jfb.13751
Turan, D., Bayçelebi, E., Aksu, S. & Oral, M. (2024). The trouts of the Marmara and Aegean Sea drainages in Türkiye, with the description of a new species (Teleostei, Salmonidae). Zoosystematics and Evolution. 100, 1-20.
Turan, D., Doğan, E., Kaya, C. & Kanyılmaz, M. (2014). Salmo kottelati, a new species of trout from Alakır stream, draining to the Mediterranean in southern Anatolia, Turkey (Teleostei, Salmonidae). Zookeys. 462, 135-151. https://doi.org/10.3897/zookeys.462.8177
Turan, D., Kottelat, M. & Bektas, Y. (2011). Salmo tigridis, a new species of trout from the Tigris River, Turkey (Teleostei: Salmonidae). Zootaxa 2993(1), 23-33.
Turan, D., Kottelat, M. & Engin, S. (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.
Turan, D., Kottelat, M. & Engin, S. (2014). Two new species of trouts from the Euphrates drainage, Turkey (Teleostei: Salmonidae). Ichthyological Exploration of Freshwaters, 24, 275-287.
Turan, D., Kottelat, M. & Kaya, C. (2002). The trouts of the upper Kura and Aras rivers in Turkey, with description of three new species (Teleostei: Salmonidae). Zootaxa. 5150, 43-64.
Wang, H.Y. & Lee, S.C. (2002). Secondary structure of mitochondrial 12S rRNA among fish and its phylogenetic applications. Molecular Biology and Evolution, 19, 138-148. https://doi.org/10.1093/oxfordjournals.molbev.a004066
Wu, R., Zhang, H., Liu, J., Niu, S., Xiao, Y. & Chen, Y. (2018). DNA barcoding of the family Sparidae along the coast of China and revelation of potential cryptic diversity in the Indo-West Pacific oceans based on COI and 16S rRNA genes. Journal of Oceanology and Limnology, 36, 1753-1770 https://doi.org/10.1007/s00343-018-7214-6
Zouakh, D.E. (2009). Hydrosystèmes continentaux et valorisation des ressources ichtyologiques d’Algérie. Thèse de Doctorat d’état. Faculté des Sciences Biologiques, USTHB, Alger
Downloads
Published
How to Cite
Issue
Section
License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
