Skip to main content

Advertisement

SpringerLink
Log in

High-throughput sequencing of the mitochondrial genomes from archived fish scales: an example of the endangered putative species flock of Sevan trout Salmo ischchan

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Sevan trout, Salmo ischchan, dwelling in the mountain Lake Sevan (Caucasus) is a unique species complex. Four sympatric forms of Sevan trout were divergent in both their phenotypes and ecologies. Three forms were lacustrine spawners but were unique in their spawning times and the type of substrate. The fish community of Lake Sevan was strongly impacted by human activity in twentieth century. Two forms of Sevan trout went extinct in the 1980s and the other two forms are at the brink of extinction. The present study demonstrated that archived/historical scales of extinct forms stored at room temperature for up to 44 years are a suitable source of DNA for high-throughput sequencing and for the reconstruction of mitochondrial genomes. In addition, we obtained the mitochondrial genomes of the extant forms for comparison to the extinct forms and reconstruction of a mitogenomic phylogeny of all forms of Sevan trout. The mitogenome gene arrangement was identical in all individuals studied with structure similar to other Salmo spp. The nucleotide sequence divergence between sympatric forms was shallow (P-distance = 0.0003–0.0012). A phylogenetic tree based on mitogenomes confirmed sister position of Sevan trout to the Caspian trout, Salmo trutta caspius (P-distance = 0.0049).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adams, B. K., D. Cote & J. A. Hutchings, 2014. A genetic comparison of sympatric anadromous and resident Atlantic salmon. Ecology of Freshwater Fishes 25: 307–317.

    Article  Google Scholar 

  • Aghasyan, A. L. & M. Y. Kalashyan, 2010. The Red Data Book of the Animals of the Republic of Armenia. Yerevan.

  • Alekseyev, S. S., V. P. Samusenok, A. N. Matveev & M. Y. Pichugin, 2002. Diversification, sympatric speciation, and trophic polymorphism of Arctic charr, Salvelinus alpinus complex, in Transbaikalia. Ecology, Behaviour and Conservation of the Charrs, Genus Salvelinus. Springer, Dordrecht: 97–114.

    Chapter  Google Scholar 

  • Aslanian, A. T., 1979. The problem of origination of Lake Sevan in the light of modern data. Bulletin of Academy of Sciences of Armenian SSR, Earth Sciences 32(3): 3–10 (in Russian).

    Google Scholar 

  • Babayan, A., S. Hakobyan, K. Jenderedjian, S. Muradyan, & M. Voskanov, 2007. Lake Sevan. In World Lakes. Experience and Lessons Learned Brief: 350–362.

  • Bandelt, H. J., P. Forster & A. Röhl, 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16(1): 37–48.

    Article  PubMed  CAS  Google Scholar 

  • Barluenga, M., K. N. Stölting, W. Salzburger, M. Muschick & A. Meyer, 2006. Sympatric speciation in Nicaraguan Crater Lake cichlid fish. Nature 439(7077): 719–723.

    Article  PubMed  CAS  Google Scholar 

  • 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(3): 285–298.

    Article  PubMed  CAS  Google Scholar 

  • 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(3): 161–173.

    Article  PubMed  CAS  Google Scholar 

  • Beshera, K. A. & P. M. Harris, 2014. Mitochondrial DNA phylogeography of the Labeobarbus intermedius complex (Pisces, Cyprinidae) from Ethiopia. Journal of Fish Biology 85(2): 228–245.

    Article  PubMed  CAS  Google Scholar 

  • Bogdanowicz, W., R. Rutkowski, B. K. Gabrielyan, A. Ryspaev, A. N. Asatryan, J. A. Mkrtchyan & B. M. Bujalska, 2017. Fish introductions in the former Soviet Union: the Sevan trout (Salmo ischchan) – 80 years later. PloS One 12(7): e0180605.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brawand, D., C. E. Wagner, Y. I. Li, M. Malinsky, I. Keller, S. Fan, et al., 2014. The genomic substrate for adaptive radiation in African cichlid fish. Nature 513(7518): 375–381.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cawdery, S. A. & A. Ferguson, 1988. Origins and differentiation of three sympatric species of trout (Salmo trutta L.) in Lough Melvin. Polish Archives of Hydrobiology 35: 267–277.

    Google Scholar 

  • Chernomor, O., A. von Haeseler & B. Q. Minh, 2016. Terrace aware data structure for phylogenomic inference from supermatrices. Systematic Biology 65: 997–1008.

    Article  PubMed  PubMed Central  Google Scholar 

  • Consuegra, S., C. García de Leániz, A. Serdio, M. González Morales, L. G. Straus, D. Knox & E. Verspoor, 2002. Mitochondrial DNA variation in Pleistocene and modern Atlantic salmon from the Iberian glacial refugium. Molecular Ecology 11(10): 2037–2048.

    Article  PubMed  CAS  Google Scholar 

  • Crespi, B. J. & M. J. Fulton, 2004. Molecular systematics of Salmonidae: combined nuclear data yields a robust phylogeny. Molecular Phylogenetics and Evolution 31(2): 658–679.

    Article  PubMed  CAS  Google Scholar 

  • Dadikyan, M. G., 1986. Fishes of Armenia. AN Arm. SSR, Yerevan (in Russian).

    Google Scholar 

  • Der Sarkissian, C., L. Ermini, M. Schubert, M. A. Yang, P. Librado, M. Fumagalli, et al., 2015. Evolutionary genomics and conservation of the endangered Przewalski’s horse. Current Biology 25(19): 2577–2583.

    Article  CAS  Google Scholar 

  • Edgar, R. C., 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32(5): 1792–1797.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Franchini, P., C. Fruciano, M. L. Spreitzer, J. C. Jones, K. R. Elmer, F. Henning & A. Meyer, 2014. Genomic architecture of ecologically divergent body shape in a pair of sympatric Crater Lake cichlid fishes. Molecular Ecology 23(7): 1828–1845.

    Article  PubMed  Google Scholar 

  • Fraser, D. J., L. K. Weir, L. Bernatchez, M. M. Hansen & E. B. Taylor, 2011. Extent and scale of local adaptation in salmonid fishes: review and meta-analysis. Heredity 106(3): 404–420.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gabrielyan, B. K., 2010. Fishes of Lake Sevan. Publishing House “Gitutyun” of NAN RA, Yerevan.

    Google Scholar 

  • Grealy, A., K. Douglass, J. Haile, C. Bruwer, C. Gough & M. Bunce, 2016. Tropical ancient DNA from bulk archaeological fish bone reveals the subsistence practices of a historic coastal community in southwest Madagascar. Journal of Archaeological Science 75: 82–88.

    Article  CAS  Google Scholar 

  • Green, R. E., A. S. Malaspinas, J. Krause, A. W. Briggs, P. L. Johnson, C. Uhler, et al., 2008. A complete Neandertal mitochondrial genome sequence determined by high-throughput sequencing. Cell 134(3): 416–426.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gum, B., J. Geist, S. Eckenfels & A. Brinker, 2014. Genetic diversity of upper Lake Constance whitefish Coregonus spp. under the influence of fisheries: a DNA study based on archived scale samples from 1932, 1975 and 2006. Journal of Fish Biology 84(6): 1721–1739.

    Article  PubMed  CAS  Google Scholar 

  • Hahn, C., L. Bachmann & B. Chevreux, 2013. Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads – a baiting and iterative mapping approach. Nucleic Acids Research 41(13): e129.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hansen, M. M., 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. Molecular Ecology 11(6): 1003–1015.

    Article  PubMed  CAS  Google Scholar 

  • Hofman, C. A., T. C. Rick, R. C. Fleischer & J. E. Maldonado, 2015. Conservation archaeogenomics: ancient DNA and biodiversity in the Anthropocene. Trends in Ecology and Evolution 30(9): 540–549.

    Article  PubMed  Google Scholar 

  • Horstkotte, J. & U. Strecker, 2005. Trophic differentiation in the phylogenetically young Cyprinodon species flock (Cyprinodontidae, Teleostei) from Laguna Chichancanab (Mexico). Biological Journal of the Linnean Society 85(1): 125–134.

    Article  Google Scholar 

  • Iwasaki, W., T. Fukunaga, R. Isagozawa, K. Yamada, Y. Maeda, T. P. Satoh, et al., 2013. MitoFish and MitoAnnotator: a mitochondrial genome database of fish with an accurate and automatic annotation pipeline. Molecular Biology and Evolution 30(11): 2531–2540.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Johnston, S. E., M. Lindqvist, E. Niemelä, P. Orell, J. Erkinaro, M. P. Kent, et al., 2013. Fish scales and SNP chips: SNP genotyping and allele frequency estimation in individual and pooled DNA from historical samples of Atlantic salmon (Salmo salar). BMC Genomics 14(1): 439.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jrbashyan, R., G. Chlingaryan, Y. U. Kagramanov, A. Karapetyan, M. Satian, Y. U. Sayadyan, & H. Mkrtchyan, 2001. Geology of Meso-Cenozoic Basins in Central Armenia, with Comment on Indications of Hydrocarbons. Search and Discovery, 30007.

  • Kondrashov, A. S. & M. V. Mina, 1986. Sympatric speciation: when is it possible? Biological Journal of the Linnean Society 27(3): 201–223.

    Article  Google Scholar 

  • Kontula, T., S. V. Kirilchik & R. Väinölä, 2003. Endemic diversification of the monophyletic cottoid fish species flock in Lake Baikal explored with mtDNA sequencing. Molecular Phylogenetics and Evolution 27(1): 143–155.

    Article  PubMed  CAS  Google Scholar 

  • Lanfear, R., B. Calcott, S. Y. Ho & S. Guindon, 2012. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29(6): 1695–1701.

    Article  PubMed  CAS  Google Scholar 

  • Lanfear, R., P. B. Frandsen, A. M. Wright, T. Senfeld & B. Calcott, 2016. PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34(3): 772–773.

    Google Scholar 

  • Langmead, B. & S. L. Salzberg, 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods 9: 357–359.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Larsen, P. F., M. M. Hansen, E. E. Nielsen, L. F. Jensen & V. Loeschcke, 2005. Stocking impact and temporal stability of genetic composition in a brackish northern pike population (Esox lucius L.), assessed using microsatellite DNA analysis of historical and contemporary samples. Heredity 95(2): 136–143.

    Article  PubMed  CAS  Google Scholar 

  • Leigh, J. W. & D. Bryant, 2015. PopART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6(9): 1110–1116.

    Article  Google Scholar 

  • Levin, B. A. & H. R. Rubenyan, 2006. Threatened fishes of the world: Barbus goktschaicus Kessler, 1877 (Cyprinidae). Environmental Biology of Fishes 76(2): 409–410.

    Article  Google Scholar 

  • Levin, B. A., J. Freyhof, Z. Lajbner, S. Perea, A. Abdoli, M. Gaffaroğlu, et al., 2012. Phylogenetic relationships of the algae scraping cyprinid genus Capoeta (Teleostei: Cyprinidae). Molecular Phylogenetics and Evolution 62(1): 542–549.

    Article  PubMed  Google Scholar 

  • Librado, P., C. Der Sarkissian, L. Ermini, M. Schubert, H. Jónsson, A. Albrechtsen, et al., 2015. Tracking the origins of Yakutian horses and the genetic basis for their fast adaptation to subarctic environments. Proceedings of the National Academy of Sciences of USA 112(50): E6889–E6897.

    Article  CAS  Google Scholar 

  • Lien, S., B. F. Koop, S. R. Sandve, J. R. Miller, M. P. Kent, T. Nome, et al., 2016. The Atlantic salmon genome provides insights into rediploidization. Nature 533: 200–205.

    Article  PubMed  CAS  Google Scholar 

  • Lushin, B. P., 1956. Issyk Kul gegarkuni trout. Izdatel’stvo AN KyrgyzSSR, Frunze (in Russian).

    Google Scholar 

  • Malinsky, M., R. J. Challis, A. M. Tyers, S. Schiffels, Y. Terai, B. P. Ngatunga, et al., 2015. Genomic islands of speciation separate cichlid ecomorphs in an East African Crater Lake. Science 350(6267): 1493–1498.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mardanov, A. V., E. S. Bulygina, A. V. Nedoluzhko, V. V. Kadnikov, A. V. Beletskii, S. V. Tsygankova, et al., 2012. Molecular analysis of the intestinal microbiome composition of mammoth and woolly rhinoceros. Doklady Biochemistry and Biophysics 445(1): 203–206.

    Article  PubMed  CAS  Google Scholar 

  • McKeown, N. J., R. A. Hynes, R. A. Duguid, A. Ferguson & P. A. Prodöhl, 2010. Phylogeographic structure of brown trout Salmo trutta in Britain and Ireland: glacial refugia, postglacial colonization and origins of sympatric populations. Journal of Fish Biology 76(2): 319–347.

    Article  PubMed  CAS  Google Scholar 

  • Medina, M., 2003. In DeSalle, R., G. Giribet & W. Wheeler (eds), Techniques in Molecular Systematics and Evolution. Methods and Tools in Biosciences and Medicine. Birkhäuser Verlag, Basel.

    Google Scholar 

  • Meyer, A., T. D. Kocher, P. Basasibwaki & A. C. Wilson, 1990. Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 347(6293): 550–553.

    Article  PubMed  CAS  Google Scholar 

  • Milanovskiy, E. E., 1957. History of formation of Sevan depression in light of knowledge about neotectonics of Lesser Caucasus. In Proceedings of IV Geomorphological Conference on Studying Caucasus and Transcaucasia. Yerevan: 120–146.

  • Miller, L. M. & A. R. Kapuscinski, 1997. Historical analysis of genetic variation reveals low effective population size in a northern pike (Esox lucius) population. Genetics 147(3): 1249–1258.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Nagelkerke, L. A. J., K. M. Leon-Kloosterziel, H. J. Megens, M. De Graaf, O. E. Diekmann & F. A. Sibbing, 2015. Shallow genetic divergence and species delineations in the endemic Labeobarbus species flock of Lake Tana, Ethiopia. Journal of Fish Biology 87(5): 1191–1208.

    Article  PubMed  CAS  Google Scholar 

  • Nedoluzhko, A. V., S. M. Rastorguev, E. Simonov, E. S. Boulygina, F. S. Sharko, S. V. Tsygankova, et al., 2018a. Two complete mitochondrial genomes of extinct form of the Sevan trout Salmo ischchan danilewskii. Mitochondrial DNA Part B: Resources 3(1): 40–41.

    Article  Google Scholar 

  • Nedoluzhko, A. V., S. M. Rastorguev, E. Simonov, E. S. Boulygina, F. S. Sharko, S. V. Tsygankova, Q. Van Nguyen, et al., 2018b. Sequencing of two mitochondrial genomes of endangered form of the Sevan trout Salmo ischchan aestivalis. Mitochondrial DNA Part B: Resources 3(2): 469–471.

    Article  Google Scholar 

  • Nguyen, L.-T., H. A. Schmidt, A. von Haeseler & B. Q. Minh, 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution 32: 268–274.

    Article  PubMed  CAS  Google Scholar 

  • Nielsen, E. E., M. M. Hansen & V. Loeschcke, 1997. Analysis of microsatellite DNA from old scale samples of Atlantic salmon Salmo salar: a comparison of genetic composition over 60 years. Molecular Ecology 6(5): 487–492.

    Article  CAS  Google Scholar 

  • Nielsen, E. E., M. M. Hansen & V. Loeschcke, 1999. Analysis of applications DNA from old scale samples: technical aspects, and perspectives for conservation. Hereditas 130(3): 265–276.

    Article  CAS  Google Scholar 

  • Nielsen, E. E., J. A. T. Morgan, S. L. Maher, J. Edson, M. Gauthier, J. Pepperell, B. J. Holmes, M. B. Bennett & J. R. Ovenden, 2017. Extracting DNA from ‘jaws’: high yield and quality from archived tiger shark (Galeocerdo cuvier) skeletal material. Molecular Ecology Resources 17(3): 431–442.

    Article  PubMed  CAS  Google Scholar 

  • Nikitin, A. G., I. Potekhina, N. Rohland, S. Mallick, D. Reich & M. Lillie, 2017. Mitochondrial DNA analysis of eneolithic trypillians from Ukraine reveals neolithic farming genetic roots. PloS ONE 12(2): e0172952.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Orlando, L., A. Ginolhac, G. Zhang, D. Froese, A. Albrechtsen, M. Stiller, et al., 2013. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature 499(7456): 74–78.

    Article  PubMed  CAS  Google Scholar 

  • Osinov, A. G., 1990. On the origin of the Sevan trout: population-genetic approach. Zhurnal Obschchei Biologii 51: 817–827 (in Russian).

    Google Scholar 

  • 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.

    Google Scholar 

  • Perreault-Payette, A., A. M. Muir, F. Goetz, C. Perrier, E. Normandeau, P. Sirois & L. Bernatchez, 2017. Investigating the extent of parallelism in morphological and genomic divergence among lake trout ecotypes in Lake Superior. Molecular Ecology 26(6): 1477–1497.

    Article  PubMed  CAS  Google Scholar 

  • Pilipenko, A. S., R. O. Trapezov, A. A. Zhuravlev, V. I. Molodin & A. G. Romaschenko, 2015. MtDNA haplogroup A10 lineages in Bronze Age samples suggest that ancient autochthonous human groups contributed to the specificity of the indigenous west Siberian population. PLoS ONE 10(5): e0127182.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Praebel, K., R. Knudsen, A. Siwertsson, M. Karhunen, K. K. Kahilainen, O. Ovaskainen, et al., 2013. Ecological speciation in postglacial European whitefish: rapid adaptive radiations into the littoral, pelagic, and profundal lake habitats. Ecology and Evolution 3(15): 4970–4986.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rambaut, A., M. A. Suchard, D. Xie, & A. J. Drummond, 2014. Tracer v1.6 [available on internet at http://beast.bio.ed.ac.uk/Tracer].

  • Rezaei, A., S. Akhshabi & H. R. Jamalzadeh, 2017. Studies on the mitochondrial genomics in Salmo trutta caspius population in three rivers of Caspian Sea. Journal of Fisheries and Livestock Production 5(1): 1–9.

    Google Scholar 

  • Rogaev, E. I., Y. K. Moliaka, B. A. Malyarchuk, F. A. Kondrashov, M. V. Derenko, I. Chumakov & A. P. Grigorenko, 2006. Complete mitochondrial genome and phylogeny of Pleistocene mammoth Mammuthus primigenius. PLoS Biology 4(3): e73.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ronquist, F. & J. P. Huelsenbeck, 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.

    Article  PubMed  CAS  Google Scholar 

  • Sahoo, P. K., L. Singh, L. Sharma, R. Kumar, V. K. Singh, S. Ali, et al., 2016. The complete mitogenome of brown trout (Salmo trutta fario) and its phylogeny. Mitochondrial DNA Part A: DNA Mapping, Sequencing, and Analysis 27(6): 4563–4565.

    Article  CAS  Google Scholar 

  • Salzburger, W., S. Baric & C. Sturmbauer, 2002. Speciation via introgressive hybridization in East African cichlids? Molecular Ecology 11(3): 619–625.

    Article  PubMed  CAS  Google Scholar 

  • Sarkissyan, S. G., 1962. Petrographic and mineralogical investigation of Lake Sevan Basin. Izdatel’stvo AN ArmSSR, Yerevan (in Russian).

    Google Scholar 

  • Schliewen, U. K., D. Tautz & S. Pääbo, 1994. Sympatric speciation suggested by monophyly of Crater Lake cichlids. Nature 368(6472): 629–632.

    Article  PubMed  CAS  Google Scholar 

  • Schön, I. & K. Martens, 2004. Adaptive, pre-adaptive and non-adaptive components of radiations in ancient lakes: a review. Organisms Diversity and Evolution 4(3): 137–156.

    Article  Google Scholar 

  • Seehausen, O. & C. E. Wagner, 2014. Speciation in freshwater fishes. Annual Review of Ecology, Evolution, and Systematics 45: 621–651.

    Article  Google Scholar 

  • Seehausen, O., E. Koetsier, M. V. Schneider, L. J. Chapman, C. A. Chapman, M. E. Knight, et al., 2003. Nuclear markers reveal unexpected genetic variation and a Congolese-Nilotic origin of the Lake Victoria cichlid species flock. Proceedings of the Royal Society of London B: Biological Sciences 270(1511): 129–137.

    Article  Google Scholar 

  • Sell, J. & Z. Spirkovski, 2004. Mitochondrial DNA differentiation between two forms of trout Salmo letnica, endemic to the Balkan Lake Ohrid, reflects their reproductive isolation. Molecular Ecology 13(12): 3633–3644.

    Article  PubMed  CAS  Google Scholar 

  • Smith, M. J., C. E. Pascal, Z. A. C. Grauvogel, C. Habicht, J. E. Seeb & L. W. Seeb, 2011. Multiplex preamplification PCR and microsatellite validation enables accurate single nucleotide polymorphism genotyping of historical fish scales. Molecular Ecology Resources 11(s1): 268–277.

    Article  PubMed  Google Scholar 

  • Sokolov, A. S., A. V. Nedoluzhko, E. S. Boulygina, S. V. Tsygankova, F. S. Sharko, N. M. Gruzdeva, et al., 2016. Six complete mitochondrial genomes from Early Bronze Age humans in the North Caucasus. Journal of Archaeological Science 73: 138–144.

    Article  CAS  Google Scholar 

  • 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(A): 2–23.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Tamura, K., G. Stecher, D. Peterson, A. Filipski & S. Kumar, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30(12): 2725–2729.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Timmermans, M. J., S. Dodsworth, C. L. Culverwell, L. Culverwell, L. Bocak, D. Ahrens, D. T. Littlewood, et al., 2010. Why barcode? High-throughput multiplex sequencing of mitochondrial genomes for molecular systematics. Nucleic Acids Research. https://doi.org/10.1093/nar/gkq807.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vonlanthen, P., D. Bittner, A. G. Hudson, K. A. Young, R. Müller, B. Lundsgaard-Hansen, et al., 2012. Eutrophication causes speciation reversal in whitefish adaptive radiations. Nature 482(7385): 357–362.

    Article  PubMed  CAS  Google Scholar 

  • Wandeler, P., P. E. Hoeck & L. F. Keller, 2007. Back to the future: museum specimens in population genetics. Trends in Ecology and Evolution 22(12): 634–642.

    Article  PubMed  Google Scholar 

  • https://www.qiagenbioinformatics.com

  • Živaljević, I., D. Popović, A. Snoj & S. Marić, 2017. Ancient DNA analysis of cyprinid remains from the Mesolithic–Neolithic Danube Gorges reveals an extirpated fish species Rutilus frisii (Nordmann, 1840). Journal of Archaeological Science 79: 1–9.

    Article  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Mikhail V. Kovalchuk (National Research Centre “Kurchatov Institute,” Moscow, Russia) for his ongoing support, and Professor Yuri Gerassimov for logistics. We would like to thank Professor Nikolay Kolchanov, Dr. Alexander Pilipenko, and Dr. Rostislav Trapezov for permission to use the Interinstitutional Center of Molecular Paleogenetics infrastructure for DNA manipulations and helpful support. We are thankful to Dr. Alexander Golubtsov and three anonymous reviewers for their valuable comments on manuscript. We also appreciate the thoughtful discussions with Professor Axel Meyer and Professor Michael Mina on the concept of a species flock. This study was funded by the Russian Science Foundation, Grant No. 15-14-10020 (sampling and partially bioinformatics) and the National Research Centre “Kurchatov Institute” (DNA extraction, preparation of libraries, NGS-sequencing, and partially bioinformatics).

Author information

Authors and Affiliations

  1. Laboratory of Fish Ecology, Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, Borok, Yaroslavl’, Russia, 152742

    Boris Levin & Evgeniy Simonov

  2. Cherepovets State University, Vologda Region, Cherepovets, Russia, 162600

    Boris Levin

  3. Siberian Federal University, Krasnoyarsk, Russia, 660041

    Evgeniy Simonov

  4. National Research Centre “Kurchatov Institute”, Moscow, Russia, 123182

    Sergey Rastorguev, Eugenia Boulygina, Svetlana Tsygankova & Artem Nedoluzhko

  5. Institute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences, Moscow, Russia, 119071

    Fedor Sharko

  6. Scientific Center of Zoology and Hydroecology, National Academy of Sciences of Republic of Armenia, Yerevan, Armenia

    Bardukh Gabrielyan & Haikaz Roubenyan

  7. Department of Biology, Saint Louis University, St. Louis, USA

    Richard Mayden

Authors
  1. Boris Levin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Evgeniy Simonov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sergey Rastorguev
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eugenia Boulygina
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fedor Sharko
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Svetlana Tsygankova
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bardukh Gabrielyan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Haikaz Roubenyan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Richard Mayden
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Artem Nedoluzhko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Artem Nedoluzhko.

Additional information

Handling editor: Christian Sturmbauer

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Levin, B., Simonov, E., Rastorguev, S. et al. 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, 217–228 (2018). https://doi.org/10.1007/s10750-018-3688-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-018-3688-7

Keywords

Search

Navigation