Skip to main content

Advertisement

SpringerLink
Log in

Phylogeography, genetic structure, and conservation of the endangered Caspian brown trout, Salmo trutta caspius (Kessler, 1877), from Iran

  • Primary research paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The Caspian Sea, the largest inland closed water body in the world, has numerous endemic species. The Caspian brown trout (Salmo trutta caspius) is considered as endangered according to IUCN criteria. Information on phylogeography and genetic structure is crucial for appropriate management of genetic resources. In spite of the huge number of studies carried out in the Salmo trutta species complex across its distribution range, very few data are available on these issues for S. trutta within the Caspian Sea. Mitochondrial (mtDNA control region) and nuclear (major ribosomal DNA internal transcribed spacer 1, ITS-1, and ten microsatellite loci) molecular markers were used to study the phylogeography, genetic structure, and current captive breeding strategies for reinforcement of Caspian trout in North Iranian rivers. Our results confirmed the presence of Salmo trutta caspius in this region. Phylogenetic analysis demonstrated its membership to the brown trout Danubian (DA) lineage. Genetic diversity of Caspian brown trout in Iranian Rivers is comparable to the levels usually observed in sustainable anadromous European brown trout populations. Microsatellite data suggested two main clusters connected by gene flow among river basins likely by anadromous fish. No genetic differences were detected between the hatchery sample and the remaining wild populations. While the current hatchery program has not produced detectable genetic changes in the wild populations, conservation strategies prioritizing habitat improvement and recovering natural spawning areas for enhancing wild populations are emphasized.

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

  • Abdoli, A., 2000. Inland Water Fishes of Iran, 1st ed. Iranian Museum of Nature and Wild Life, Tehran.

    Google Scholar 

  • Almodovar, A., G. G. Nicola, B. Elvira & J. L. Garcia-Marin, 2006. Introgression variability among Iberian brown trout Evolutionary Significant Units: the influence of local management and environmental features. Freshwater Biology 51: 1175–1187.

    Article  Google Scholar 

  • Ayllon, F., P. Moran & E. Garcia-Vazquez, 2006. Maintenance of a small anadromous subpopulation of brown trout (Salmo trutta L.) by straying. Freshwater Biology 51: 351–358.

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Barannik, V., O. Borysova & F. Stolberg, 2004. The Caspian Sea region: environmental change. Ambio 33: 45–51.

    PubMed  Google Scholar 

  • Baric, S., A. Riedl, A. Meraner, N. Medgyesy, R. Lackner, B. Pelster & J. Dalla-Via, 2010. Alpine headwater streams as reservoirs of remnant populations of the Danubian clade brown trout. Freshwater biology 55: 866–880.

    Article  Google Scholar 

  • 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.

    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: 285–297.

    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: 161–173.

    Article  PubMed  CAS  Google Scholar 

  • Cassens, I., K. Van Waerebeek, P. B. Best, E. A. Crespo, J. Reyes & M. C. Milinkovitch, 2003. The phylogeography of dusky dolphins (Lagenorhynchus obscurus): a critical examination of network methods and rooting procedures. Molecular Ecology 12: 1781–1792.

    Article  PubMed  CAS  Google Scholar 

  • Chapuis, M. P. & A. Estoup, 2007. Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24: 621–631.

    Article  PubMed  CAS  Google Scholar 

  • Coad, B. W., 2000. Criteria for assessing the conservation status of taxa (as applied to Iranian freshwater fishes). Biologia 55: 537–555.

    Google Scholar 

  • Corander, J. & P. Marttinen, 2006. Bayesian identification of admixture events using multilocus molecular markers. Molecular Ecology 15: 2833–2843.

    Article  PubMed  Google Scholar 

  • Cortey, M. & J. L. Garcia-Marin, 2002. Evidence for phylogeographically informative sequence variation in the mitochondrial control region of Atlantic brown trout. Journal of Fish Biology 60: 1058–1063.

    Article  CAS  Google Scholar 

  • Cortey, M., C. Pla & J. L. Garcia-Marin, 2004. Historical biogeography of Mediterranean trout. Molecular Phylogenetics and Evolution 33: 831–844.

    Article  PubMed  Google Scholar 

  • Cortey, M., M. Vera, C. Pla & J. L. Garcia-Marin, 2009. Northern and Southern expansions of Atlantic brown trout (Salmo trutta) populations during the Pleistocene. Biological Journal of the Linnean Society 97: 904–917.

    Article  Google Scholar 

  • Dakin, E. E. & J. C. Avise, 2004. Microsatellite null alleles in parentage analysis. Heredity 93: 504–509.

    Article  PubMed  CAS  Google Scholar 

  • Duftner, N., S. Weiss, N. Medgyesy & C. Sturmbauer, 2003. Enhanced phylogeographic information about Austrian brown trout populations derived from complete mitochondrial control region sequences. Journal of Fish Biology 62: 427–435.

    Article  Google Scholar 

  • Dumont, H. J., 1998. The Caspian lake: history, biota, structure and function. Limnology and Oceanography 43: 44–52.

    Article  CAS  Google Scholar 

  • Elmousadik, A. & R. J. Petit, 1996. High level of genetic differentiation for allelic richness among populations of the argan tree Argania spinosa (L) Skeels endemic to Morocco. Theoretical and Applied Genetics 92: 832–839.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Excoffier, L., P. E. Smouse & J. M. Quattro, 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479–491.

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Garza, J. C. & E. G. Williamson, 2001. Detection of reduction in population size using data from microsatellite loci. Molecular Ecology 10: 305–318.

    Article  PubMed  CAS  Google Scholar 

  • Goudet, J., 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3) [available from http://www.unil.ch/izea/softwares/fstat.html].

  • 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: 1003–1015.

    Article  PubMed  CAS  Google Scholar 

  • Hansen, M. M. & L. F. Jensen, 2005. Sibship within samples of brown trout (Salmo trutta) and implications for supportive breeding. Conservation Genetics 6: 297–305.

    Article  Google Scholar 

  • Hansen, M. M., E. E. Nielsen, D. E. Ruzzante, C. Bouza & K. L. D. Mensberg, 2000. Genetic monitoring of supportive breeding in brown trout (Salmo trutta L.), using microsatellite DNA markers. Canadian Journal of Fisheries and Aquatic Sciences 57: 2130–2139.

    Article  Google Scholar 

  • Hansen, M. M., D. E. Ruzzante, E. E. Nielsen, D. Bekkevold & K. L. D. Mensberg, 2002. Long-term effective population sizes, temporal stability of genetic composition and potential for local adaptation in anadromous brown trout (Salmo trutta) populations. Molecular Ecology 11: 2523–2535.

    Article  PubMed  Google Scholar 

  • Harley, E. H., 2001. AGARst. A program for calculating allele frequencies, GST and RST from microsatellite data. University of Cape Town, South Africa.

    Google Scholar 

  • Hillis, D. M. & M. T. Dixon, 1991. Ribosomal DNA: molecular evolution and phylogenetic inference. Quarterly Review of Biology 66: 411–453.

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck, J. P. & F. Ronquist, 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.

    Article  PubMed  CAS  Google Scholar 

  • Hynes, R. A., A. Ferguson & M. A. Mccann, 1996. Variation in mitochondrial DNA and post-glacial colonization of north Western Europe by brown trout. Journal of Fish Biology 48: 54–67.

    Article  CAS  Google Scholar 

  • Jalali, M. A. & B. M. Amiri, 2009. Threatened fishes of the world: Salmo trutta caspius (Kessler, 1877) (Salmoniforms: Salmonidae). Environmental Biology of Fishes 86: 375–376.

    Article  Google Scholar 

  • Kheyrandish, A., A. Abdoli, H. Mostafavi, H. Niksirat, M. Naderi & S. Vatandoost, 2010. Age and growth of brown trout (Salmo trutta) in six rivers of the Southern part of Caspian basin. American Journal of Animal and Veterinary Sciences 5: 8–12.

    Article  Google Scholar 

  • Kiabi, B. H., A. Abdoli & M. Naderi, 1999. Status of the fish fauna in the South Caspian basin of Iran. Journal of Zoology in the Middle East 18: 57–65.

    Google Scholar 

  • Koljonen, M. L., J. Tahtinen, M. Saisa & J. Koskiniemi, 2002. Maintenance of genetic diversity of Atlantic salmon (Salmo salar) by captive breeding programmes and the geographic distribution of microsatellite variation. Aquaculture 212: 69–92.

    Article  CAS  Google Scholar 

  • Konovalov, D. A., C. Manning & M. T. Henshaw, 2004. KINGROUP: a program for pedigree relationship reconstruction and kin group assignments using genetic markers. Molecular Ecology Notes 4: 779–782.

    Article  Google Scholar 

  • Laikre, L., A. Antunes, A. Apostolidis, P. Berrebi, A. Duguid, A. Ferguson, J. L. Garcia-Marin, R. Guyomard, M. M. Hansen, K. Hindar, M. L. Koljonen, C. Largiader, P. Martinez, E. E. Nielsen, S. Palm, D. Ruzzante, N. Ryman & C. Triantaphyllidis, 1999. Conservation genetic management of brown trout (Salmo trutta L.) in Europe. Report by the concerted action on identification, management and exploitation of genetic resources in the brown trout (Salmo trutta) (“TROUTCONCERT”; EU FAIR CT97-3882). ISBN 87-987732-0-8 1999.

  • Langella, O., 2002. POPULATIONS 1.2.26. Logiciel de Génétique de populations. Laboratoire populations, génétique et évolution. CNRS UPR 9034. Gif-sur-Yvette. France [available from http://www.bioinformatics.org/project/?group_id=84].

  • Luikart, G., F. W. Allendorf, J. M. Cornuet & W. B. Sherwin, 1998. Distortion of allele frequency distributions provides a test for recent population bottlenecks. Journal of Heredity 89: 238–247.

    Article  PubMed  CAS  Google Scholar 

  • Machado-Schiaffino, G., E. Dopico & E. Garcia-Vazquez, 2007. Genetic variation losses in Atlantic salmon stocks created for supportive breeding. Aquaculture 264: 59–65.

    Article  Google Scholar 

  • Martinez, P., C. Bouza, J. Castro, M. Hermida, B. G. Pardo & L. Sanchez, 2007. Analysis of a secondary contact between divergent lineages of brown trout Salmo trutta L. from Duero basin using microsatellites and mtDNA RFLPs. Journal of Fish Biology 71: 195–213.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nei, M., 1987. Molecular evolutionary genetics. Columbia University Press, New York.

    Google Scholar 

  • Nei, M. & F. Tajima, 1981. DNA polymorphism detectable by restriction endonucleases. Genetics 97: 145–163.

    PubMed  CAS  Google Scholar 

  • Niksirat, H. & A. Abdoli, 2009. On the status of the critically endangered Caspian brown trout, Salmo trutta caspius, during recent decades in the southern Caspian Sea basin. Zoology in the Middle East 46: 55–60.

    Google Scholar 

  • Noges, P., K. Kangur, T. Noges, A. Reinart, H. Simola & M. Viljanen, 2008. Highlights of large lake research and management in Europe. Hydrobiologia 599: 259–276.

    Article  CAS  Google Scholar 

  • Novikov, G. G., A. V. Semenova, A. N. Stroganov & V. Tagizade, 2008. Allozyme variability in the populations of brown trout Salmo trutta from the rivers of Iran. Journal of Ichthyology 48: 421–426.

    Article  Google Scholar 

  • O’connell, M. & J. M. Wright, 1997. Microsatellite DNA in fishes. Reviews in Fish Biology and Fisheries 7: 331–363.

    Article  Google Scholar 

  • Osinov, A. G., 2009. Iranian samples of brown trout Salmo trutta or rainbow trout Oncorhynchus mykiss: comparison of evidence from allozyme and mitochondrial DNA control region sequence analysis. Journal of Ichthyology 49: 825–828.

    Article  Google Scholar 

  • Osinov, A. G. & L. Bernatchez, 1996. “Atlantic” and “Danube” phylogenetic groups of the sea trout Salmo trutta complex: genetic divergence, evolution, protection. Voprosy Ikhtiologii 36: 762–786.

    Google Scholar 

  • Page, R. D. M., 1996. TreeView: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12: 357–358.

    PubMed  CAS  Google Scholar 

  • Pino-Querido, A., M. Hermida, M. Vilariño, C. Bouza & P. Martinez, 2010. Statistical properties and performance of pairwise relatedness estimators using turbot (Scophthalmus maximus L.) family data. Aquaculture Research 41: 528–534.

    Article  Google Scholar 

  • Piry, S., G. Luikart & J. M. Cornuet, 1999. BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity 90: 502–503.

    Article  Google Scholar 

  • Posada, D. & K. A. Crandall, 2001. Intraspecific gene genealogies: trees grafting into networks. Trends in Ecology & Evolution 16: 37–45.

    Article  Google Scholar 

  • Presa, P. & R. Guyomard, 1996. Conservation of microsatellites in three species of salmonids. Journal of Fish Biology 49: 1326–1329.

    Google Scholar 

  • Presa, P., B. G. Pardo, P. Martinez & L. Bernatchez, 2002. Phylogeographic congruence between mtDNA and rDNA ITS markers in brown trout. Molecular Biology and Evolution 19: 2161–2175.

    PubMed  CAS  Google Scholar 

  • Ramezani, H., 2009. Effects of different protein and energy levels on growth performance of Caspian brown trout, Salmo trutta caspius (Kessler, 1877). Journal of Fisheries and Aquatic Science 4: 203–209.

    Article  CAS  Google Scholar 

  • Rohlf, F., 1993. NTSYS-pc. Numerical taxonomy and multivariate analysis system, Version 2.1. Setauket, New York.

    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 

  • Rousset, F., 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145: 1219–1228.

    PubMed  CAS  Google Scholar 

  • Rousset, F., 2008. GENEPOP ‘007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources 8: 103–106.

    Article  Google Scholar 

  • Ruzzante, D. E., M. M. Hansen & D. Meldrup, 2001. Distribution of inbreeding coefficients, relatedness and influence of stocking on native anadromous brown trout (Salmo trutta) population structure. Molecular Ecology 10: 2107–2118.

    Article  PubMed  CAS  Google Scholar 

  • Sambrook, J., E. F. Fritsch & T. Maniatis, 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor, New York.

    Google Scholar 

  • Sanz, N., M. Cortey, C. Pla & J. L. Garcia-Marin, 2006. Hatchery introgression blurs ancient hybridization between brown trout (Salmo trutta) lineages as indicated by complementary allozymes and mtDNA markers. Biological Conservation 130: 278–289.

    Article  Google Scholar 

  • Sanz, N., R. M. Araguas, R. Fernandez, M. Vera & J. L. Garcia-Marin, 2009. Efficiency of markers and methods for detecting hybrids and introgression in stocked populations. Conservation Genetics 10: 225–236.

    Article  CAS  Google Scholar 

  • Sarvi, K., H. Niksirat, B. M. Amiri, S. M. Mirtorabi, G. R. Rafiee & M. Bakhtiyari, 2006. Cryopreservation of semen from the endangered Caspian brown trout (Salmo trutta caspius). Aquaculture 256: 564–569.

    Article  CAS  Google Scholar 

  • Schneider, S., D. Roessli & L. Excoffier, 2000. Arlequin, Version 2.000: a software for population genetics data analysis. G.A.B. Laboratory). University of Geneva, Switzerland, Geneva.

    Google Scholar 

  • Sedgwick, S. D., 1995. Trout farming handbook. Alden Press, Oxford.

    Google Scholar 

  • Snoj, A., I. Bogut & S. Susnik, 2008. Evidence of a genetically distinct population of Vrljika softmouth trout Salmo obtusirostris Heckel evolved by vicariance. Journal of Fish Biology 72: 1945–1959.

    Article  Google Scholar 

  • Tamura, K., J. Dudley, M. Nei & S. Kumar, 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596–1599.

    Article  PubMed  CAS  Google Scholar 

  • Van Oosterhout, C., W. F. Hutchinson, D. P. M. Wills & P. Shipley, 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.

    Article  Google Scholar 

  • Vera, M., M. Cortey, N. Sanz & J. L. Garcia-Marin, 2010a. Maintenance of an endemic lineage of brown trout (Salmo trutta) within the Duero river basin. Journal of Zoological Systematics and Evolutionary Research 48: 181–187.

    Article  Google Scholar 

  • Vera, M., N. Sanz, M. M. Hansen, A. Almodovar & J. L. Garcia-Marin, 2010b. Population and family structure of brown trout, Salmo trutta, in a Mediterranean stream. Journal of Marine and Freshwater research 61: 676–685.

    Article  Google Scholar 

  • Vilas, R., C. Bouza, J. Castro, A. López & P. Martinez, 2010. Management units of brown trout from Galicia (NW: Spain) based on spatial genetic structure analysis. Conservation Genetics 11: 897–906.

    Article  Google Scholar 

  • Walsh, P. S., D. A. Metzger & R. Higuchi, 1991. CHELEX-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10: 506–513.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to express our gratitude to the manager and staffs of Kelardasht Culture and Breeding Centre of Salmonids, Iran for providing the fish. We thank L. Insua, M. Portela, S. Sánchez, M. López, S. Gómez, M. Otero, and Z. Ghasemi for technical assistance. This research was supported by funding from University of Santiago de Compostela (Spain) and University of Tarbiat Modares (Iran).

Author information

Authors and Affiliations

  1. Departamento de Genética. Facultad de Veterinaria, Universidad de Santiago de Compostela, Campus de Lugo, 27002, Lugo, Spain

    Manuel Vera, Iman Sourinejad, Carmen Bouza, Román Vilas, Ania Pino-Querido & Paulino Martínez

  2. Department of Fisheries Science, Faculty of Agriculture and Natural Resources, University of Hormozgan, 3995, Bandar Abbas, Iran

    Iman Sourinejad

  3. Department of Fisheries, Faculty of Marine Sciences, Tarbiat Modares University, Noor, Mazandaran, Iran

    Mohammad R. Kalbassi

  4. Research and Development Center for Biotechnology (RDCB), Tarbiat Modares University, Tehran, Iran

    Mohammad R. Kalbassi

Authors
  1. Manuel Vera
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Iman Sourinejad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carmen Bouza
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Román Vilas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ania Pino-Querido
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mohammad R. Kalbassi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Paulino Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Manuel Vera.

Additional information

Handling editor: M. Power

Electronic supplementary material

Below is the link to the electronic supplementary material.

10750_2010_581_MOESM1_ESM.eps

Figure S1. Neighbor-Joining tree among the haplotypes found in Iranian Rivers. The numbers indicate the robustness of the branches using Neighbor-Joining (NJ above branch, bootstrap value >50) and Bayesian inference (BI, below branch, Posterior probability >50) (EPS 1.4 MB)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vera, M., Sourinejad, I., Bouza, C. et al. Phylogeography, genetic structure, and conservation of the endangered Caspian brown trout, Salmo trutta caspius (Kessler, 1877), from Iran. Hydrobiologia 664, 51–67 (2011). https://doi.org/10.1007/s10750-010-0581-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-010-0581-4

Keywords

Search

Navigation