Abstract
The eastern-most members of the Salmo trutta species complex in the Aralo-Caspian Sea region were studied to infer their population genetic structure and biogeographic origin. A total of 68 individuals collected from Iranian endorheic inland basins (Namak and Urmia lakes), tributaries of the Caspian (Haraz, Kura, Samur, Volga, and Ural river drainages) and Aral (Amu River) seas, and the Baltic Sea basin were genotyped using 26,202 SNPs via Genotyping-by-Sequencing. The data were analyzed using admixture, discriminant analysis of principal components (DAPC), analysis of molecular variance (AMOVA), species tree, genetic differentiation (FST), allele frequency difference (AFD), and neighbor network approaches. Trout in the southern Caspian Sea basin differ from those of the western and northern Caspian Sea. Based on our results, the Lake Namak trout is divergent from the southern and western Caspian trout populations. Aral Sea and Lake Namak trouts likely originated from the northern and southern Caspian Sea populations, respectively. Although only few populations were considered in this study, six conservation/management units of trouts are proposed.
Similar content being viewed by others
Data availability
All data files are available on request.
References
Abed, A., G. Légaré, S. Pomerleau, J. St-Cyr, B. Boyle & F. J. Belzile, 2019. Genotyping-by-sequencing on the ion torrent platform in barley. Barley. In Harwood, W. (ed), Barley: Methods in Molecular Biology, Vol. 1900. Humana Press, New York, NY: 233–252.
Alexander, D. H., J. Novembre & K. Lange, 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Research 19(9): 1655–1664.
Aljanabi, S. M. & I. Martinez, 1997. Universal and rapid salt-extraction of high-quality genomic DNA for PCR-based techniques. Nucleic Acids Research 25(22): 4692–4693.
Andrews, S., 2010. FastQC: A Quality Control Tool for High Throughput Sequence Data. Babraham Bioinformatics, Babraham Institute, Cambridge, United Kingdom.
Antunes, A., R. Faria, W. E. Johnson, R. Guyomard & P. Alexandrino, 2006. Life on the edge: the long-term persistence and contrasting spatial genetic structure of distinct brown trout life histories at their ecological limits. Journal of Heredity 97(3): 193–205.
Bardakci, F., N. Degerli, O. Ozdemir & H. Basibuyuk, 2006. Phylogeography of the Turkish brown trout Salmo trutta L.: mitochondrial DNA PCR‐RFLP variation. Journal of Fish Biology 68(A):36–55.
Berg, L. S. 1949. Presnovodnye ryby Irana i sopredel’nykh stran (Freshwater fishes of Iran and adjacent countries). Trudy Zoologicheskogo Instituta Akademii Nauk SSSR 8:783–858.
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.
Berner, D., 2019. Allele frequency difference AFD–an intuitive alternative to FST for quantifying genetic population differentiation. Genes 10(4): 308.
Catchen, J., P. A. Hohenlohe, S. Bassham, A. Amores & W. A. Cresko, 2013. Stacks: an analysis tool set for population genomics. Molecular Ecology 22(11): 3124–3140.
Chifman, J. & L. Kubatko, 2014. Quartet inference from SNP data under the coalescent model. Bioinformatics 30(23): 3317–3324.
Derjavin A.N. 1941. Caspian salmon stock reproduction. Baku, AzFAN Publishing (in Russian).
Elliott, J. M., 1994. Quantitative Ecology and the Brown Trout, Oxford University Press:
Emerson, K. J., C. R. Merz, J. M. Catchen, P. A. Hohenlohe, W. A. Cresko, W. E. Bradshaw & C. M. Holzapfel, 2010. Resolving postglacial phylogeography using high-throughput sequencing. Proceedings of the National Academy of Sciences USA 107(37): 16196–16200.
Ferrigno, J.G., 1991. Glaciers of Iran. Glaciers of the Middle East and Africa: Satellite Image Atlas of Glaciers of the World. U.S. Geological Survey Professional Paper 1386-G-2, pp. G31-G47. https://pubs.usgs.gov/pp/p1386g/iran.pdf.
Frankham, R., 2015. Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow. Molecular Ecology 24(11): 2610–2618.
Freyhof, J., C. Kaya, G. Epitashvili & M.F. Geiger, 2021. Oxynoemacheilus phasicus, a new nemacheilid loach from the eastern Black Sea basin with some remarks on other Caucasian Oxynoemacheilus (Teleostei: Nemacheilidae). Zootaxa 4952(1): zootaxa-4952.
Gandlin, A. A., B. Japoshvili, G. Epitashvili, N. J. Mustafaev, H. R. Roubenyan & B. A. Levin, 2022. Phylogeography of the Kura Barbel Barbus cyri De Filippi as Inferred from mtDNA Data. Inland Water Biology 15(1): 11–22.
Gobejishvili, R., N. Lomidze & L. Tielidze, 2011. Late Pleistocene (Würmian) glaciations of the Caucasus. Developments in Quaternary Sciences 15: 141–147.
Griffiths, A., D. Bright & J. Stevens, 2009. Complete mitochondrial control region sequences indicate a distinct variety of brown trout Salmo trutta in the Aral Sea. Journal of Fish Biology 74(5): 1136–1142.
Hallerman, E. M., 2003. Population Genetics: Principles and Applications for Fisheries Scientists, American Fisheries Society, Bethesda, MD:
Hansen, T., P. G. Fjelldal, S. Lien, M. Smith, C. Corton, K. Oliver, J. Skelton, E. Betteridge, J. Doulcan, O. Fedrigo, J. Mountcastle, E. Jarvis, S. A. McCarthy, W. Chow, K. Howe, J. Torrance, J. Wood, Y. Sims, L. Haggerty, R. Challis, J. Threlfall, D. Mead, R. Durbin & M. Blaxter, 2021. The genome sequence of the brown trout, Salmo trutta Linnaeus 1758. Wellcome Open Research 6: 108.
Hashemzadeh Segherloo, I., H. Farahmand, A. Abdoli, L. Bernatchez, C. Primmer, A. Swatdipong, M. Karami & B. Khalili, 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. Journal of Fish Biology 81(5): 1479–1500.
Hashemzadeh Segherloo, I., J. Freyhof, P. Berrebi, A. L. Ferchaud, M. Geiger, J. Laroche, B. A. Levin, E. Normandeau & L. Bernatchez, 2021. A genomic perspective on an old question: Salmo trouts or Salmo trutta (Teleostei: Salmonidae)? Molecular Phylogenetics and Evolution 162: 107204.
Huson, D. H., & D. Bryant, 2005. Estimating phylogenetic trees and networks using SplitsTree 4. www splitstree org.
Jombart, T. & C. Collins, 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.
Kamvar, Z. N., J. F. Tabima, & N. J. Grünwald, 2014. Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2: 281.
Kislov, A. V., A. Panin & P. Toropov, 2014. Current status and palaeostages of the Caspian Sea as a potential evaluation tool for climate model simulations. Quaternary International 345: 48–55.
Kottelat, M. & J. Freyhof, 2007. Handbook of European Freshwater Fishes, Publications Kottelat, Cornol, Switzerland:
Krinsley, D.B., 1970. A geomorphological and paleoclimatological study of the playas of Iran. U.S. Geological Survey Interagency Report IR-Military-1, 329 p. https://apps.dtic.mil/sti/citations/AD0721849.
Kuljanishvili, T., G. Epitashvili, J. Freyhof, B. Japoshvili, L. Kalous, B. Levin, N. Mustafayev, S. Ibrahimov, S. Pipoyan & L. Mumladze, 2020. Checklist of the freshwater fishes of Armenia, Azerbaijan and Georgia. Journal of Applied Ichthyology 36(4): 501–514.
Levin, B., E. Simonov, S. Rastorguev, E. Boulygina, F. Sharko, S. Tsygankova, B. Gabrielyan, H. Roubenyan, R. Mayden & A. Nedoluzhko, 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.
Levin, B., E. Simonov, B. K. Gabrielyan, R. L. Mayden, S. M. Rastorguev, H. R. Roubenyan, F. S. Sharko & A. V. Nedoluzhko, 2022. Caucasian treasure: genomics sheds light on the evolution of half-extinct Sevan trout, Salmo ischchan, species flock. Molecular Phylogenetics and Evolution 167: 107346.
Mangerud, J., M. Jakobsson, H. Alexanderson, V. Astakhov, G. K. Clarke, M. Henriksen, C. Hjort, G. Krinner, J. P. Lunkka, P. Möller & A. Murray, 2004. Ice-dammed lakes and rerouting of the drainage of northern Eurasia during the Last Glaciation. Quaternary Science Reviews 23(11–13): 1313–1332.
Mangerud, J., J. Gosse, A. Matiouchkov & T. Dolvik, 2008. Glaciers in the Polar Urals, Russia, were not much larger during the Last Global Glacial Maximum than today. Quaternary Science Reviews 27(9–10): 1047–1057.
Marić, S., O. Askeyev, A. Askeyev, S. Monakhov, N. Yanybaev, I. Askeyev, D. Galimova & A. Snoj, 2016. Lack of mtDNA variation among remote middle Volga and upper Ural brown trout suggests recent and rapid recolonization. Journal of Applied Ichthyology 32(5): 948–953.
Martin, M., 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet Journal 17(1): 10–12.
Mascher, M., S. Wu, P. S. Amand, N. Stein & J. Poland, 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.
McKinney, G. J., R. K. Waples, L. W. Seeb & J. E. Seeb, 2017. Paralogs are revealed by proportion of heterozygotes and deviations in read ratios in genotyping-by-sequencing data from natural populations. Molecular Ecology Resources 17(4): 656–669.
Miller, L. M. & A. R. Kapuscinski, 2003. Genetic guidelines for hatchery supplementations programs. In Hallerman, E. M. (ed), Population Genetics: Principles and Applications for Fisheries Scientists American Fisheries Society, Bethesda, MD, USA: 329–355.
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 8(5): 2645–2658.
Osinov, A. G. & L. Bernatchez, 1996. Atlantic and Danubian phylogenetic groupings of brown trout Salmo trutta complex: genetic divergence, evolution, and conservation. Journal of Ichthyology 36(9): 723–746.
Parvizi, E., R. Naderloo, A. Keikhosravi, S. Solhjouy-Fard & C. D. Schubart, 2018. Multiple Pleistocene refugia and repeated phylogeographic breaks in the southern Caspian Sea region: insights from the freshwater crab Potamon ibericum. Journal of Biogeography 45(6): 1234–1245.
Pembleton, L. W., N. O. Cogan & J. W. Forster, 2013. St AMPP: an R package for calculation of genetic differentiation and structure of mixed-ploidy level populations. Molecular Ecology Resources 13(5): 946–952.
Saadati, M. A. G. 1977. Taxonomy and distribution of the freshwater fishes of Iran. MS Thesis. Colorado State University: Fort Collins, Co, USA.
Sanz, N., 2018. Phylogeographic history of brown trout: a review, Brown Trout: Biology Ecology and Management. Wiley, New York: 17–63.
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(1): 1–11.
Snoj, A., J. Bravničar, S. Marić, S. Sušnik Bajec, H. Benaissa & J. Schöffmann, 2021. Nuclear DNA reveals multiple waves of colonisation, reticulate evolution and a large impact of stocking on trout in north-west Africa. Hydrobiologia 848(15): 3389–3405.
Suárez, J., J. M. Bautista, A. Almodóvar & A. Machordom, 2001. Evolution of the mitochondrial control region in Palaearctic brown trout (Salmo trutta) populations: the biogeographical role of the Iberian Peninsula. Heredity 87(2): 198–206.
Tabatabaei, S. N., A. Abdoli, F. Ahmadzadeh, C. R. Primmer, A. Swatdipong & I. H. Segherloo, 2020a. Mixed stock assessment of lake-run Caspian Sea trout Salmo caspius in the Lar National Park. Iran. Fisheries Research 230: 105644.
Tabatabaei, S. N., A. Abdoli, I. H. Segherloo, E. Normandeau, F. Ahmadzadeh, F. Nejat & L. Bernatchez, 2020b. Fine-scale population genetic structure of endangered Caspian Sea trout Salmo Caspius: implications for conservation. Hydrobiologia 847(16): 3339–3353.
Tougard, C., F. Justy, B. Guinand, E. J. Douzery & P. Berrebi, 2018. Salmo macrostigma (Teleostei, Salmonidae): nothing more than a brown trout (S. trutta) lineage? Journal of Fish Biology 93(2):302–310.
Tudryn, A., S. A. Leroy, S. Toucanne, E. Gibert-Brunet, P. Tucholka, Y. A. Lavrushin, O. Dufaure, S. Miska & G. Bayon, 2016. The Ponto-Caspian basin as a final trap for southeastern Scandinavian Ice-Sheet meltwater. Quaternary Science Reviews 148: 29–43.
Vera, M., I. Sourinejad, C. Bouza, R. Vilas, A. Pino-Querido, M. R. Kalbassi & P. Martínez, 2011. Phylogeography, genetic structure, and conservation of the endangered Caspian brown trout, Salmo trutta caspius (Kessler, 1877), from Iran. Hydrobiologia 664(1): 51–67.
Weir, B. S. & C. C. Cockerham, 1984. Estimating F-statistics for the analysis of population structure. Evolution 38(6): 1358–1370.
Whiteley, A. R., S. W. Fitzpatrick, W.C. Funk, & D.A. Tallmon, 2015. Genetic rescue to the rescue. Trends in Ecology & Evolution 30(1): 42–49.
Acknowledgements
This work is dedicated to Mesdames Madeleine Drouin and Böyük-Khanim Ahmadi Segherloo. The authors thank Müfit Özuluğ (Istanbul), who provided tissue materials that he collected and allowed JF to participate in his many years of fieldwork. We also thank Guillaume Côté, Cecilia Hernandez, Damien Bovin-Delisle, Noémie Leduc, Clément Rougeux, and Justine Létourneau for valuable help and expertise provided in the laboratory work and during discussions. We also thank the editor and three anonymous reviewers for their constructive comments on a previous version of our manuscript. This work is supported by a NSERC (Canada) Discovery grant (http://www.nserc-crsng.gc.ca) to Louis Bernatchez; grant number 688MIGRD94 to Iraj Hashemzadeh Segherloo by Shahr-e-Kord University (www.sku.ac.ir); and a short-term scholarship (V3 program) from the Fonds de Recherche Québécois sur la Nature et les Technologies (FRQNT: www.frqnt.gouv.qc.ca) to Iraj Hashemzadeh Segherloo. This study is also a product of the FREDIE project, supported by the Leibniz Association Joint Initiative for Research and Innovation (SAW). BAL was supported by the Ministry of Science and Higher Education of the Russian Federation (grant no. 15.BRK.21.0015).
Funding
Funding was provided by Canadian Network for Research and Innovation in Machining Technology, Natural Sciences and Engineering Research Council of Canada, Shahrekord University (688MIGRD94), Fonds Québécois de la Recherche sur la Nature et les Technologies, Leibniz Association Joint Initiative for Research and Innovation, and Ministry of Science and Higher Education of the Russian Federation (15.BRK.21.0015).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Handling Editor: Diego Fontaneto
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Hashemzadeh Segherloo, I., Tabatabaei, S.N., Abdoli, A. et al. Biogeographic insights from a genomic survey of Salmo trouts from the Aralo-Caspian regions. Hydrobiologia 849, 4325–4339 (2022). https://doi.org/10.1007/s10750-022-04993-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-022-04993-8