Genetic diversification and population structure of Barbus cyri De Filippi, 1865 (Teleostei: Cyprinidae) in northern Iran inferred from the mitochondrial D-loop gene sequence

Abstract

A genetic survey of Barbus cyri populations from two biogeographical endorheic basins (Caspian Sea and Urmia Lake) was carried out using a mitochondrial marker (partial D-loop) in order to ascertain intra- and inter-population genetic diversity, population demography and to address their genetic structure which is the key to conservation action planning. Analyses were conducted on sequences obtained from 68 individuals collected from 10 sampling sites, from two basins. By means of morphological characteristics all specimens collected from the Caspian Sea basin were ascribed to Barbus cyri. Genetic diversity values (h and π) of sampling groups were all different from 0 (in Babolrud River population) to 0.857 (in Kalibar River population). Population connectivity and colonization patterns of the studied area were inferred from an analysis of molecular variance distribution and evolutionary relationships among haplotypes. The results point to different levels of isolation among sampling groups due to ecological and anthropogenic factors and the effect of an artificial barrier on genetic variability and conservation status of the population. Finally, this study confirms the uncertainty associated with systematic classification of Barbus spp. based on morphological characters due to the phenotypic plasticity of the species.

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References

  1. Allen MB, Vincent SJ, Alsop GI, Ismail-zadeh A, Flecker R (2003) Late Cenozoic deformation in the South Caspian region: effects of a rigid basement block within a collision zone. Tectonophysics 366(3):223–239

    Article  Google Scholar 

  2. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University press, p 464

  3. Beheregaray LB (2008) Twenty years of phylogeography: the state of the field and the challenges for the southern hemisphere. Mol Ecol 17:3754–3774

    PubMed  Google Scholar 

  4. Briggs JC (2000) Centrifugal speciation and centres of origin. J Biogeogr 27(5):1183–1188

    Article  Google Scholar 

  5. Cecconi F, Giorgi M, Mariottini P (1995) Unique features in the mitochondrial D-loop region of the European seabass Dicentrarchus labrax. Gene 160(2):149–155

    CAS  Article  PubMed  Google Scholar 

  6. Choleva L, Musilova Z, Kohoutova-Sediva A, Paces J, Rab P et al (2014) Distinguishing between incomplete lineage sorting and genomic introgressions: complete fixation of allospecific mitochondrial DNA in a sexually reproducing fish (Cobitis; Teleostei), despite clonal reproduction of hybrids. PLoS One 9(6):e80641. https://doi.org/10.1371/journal.pone.0080641

    Article  PubMed  PubMed Central  Google Scholar 

  7. Coad BW (2017) Freshwater fishes of Iran, personal website. www.briancoad.com. accessible on 26. April. 2017

  8. Darvishzadeh A (2007) Geology of Iran. Amir-Kabir Publications, Tehran

    Google Scholar 

  9. Esmaeili HR, Coad BW, Mehraban HR, Masoudi M, Khaefi R, Abbasi K, Mostafavi H, Vatandoust S (2014) An updated checklist of fishes of the Caspian Sea basin of Iran with a note on their zoogeography. Iran J Ichthyol 1(3):152–184

    Google Scholar 

  10. Esmaeili HR, Mehraban H, Abbasi K, Keivany Y, Coad B (2017) Review and updated checklist of freshwater fishes of Iran: taxonomy, distribution and conservation status. Iran J Ichthyol 4(Suppl. 1):1–114

    Google Scholar 

  11. Excoffier L, Lischer H (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  12. Ferrito V, Pappalardo AM, Canapa A, Barucca M, Doadrio I, Olmo E, Tigano C (2013) Mitochondrial phylogeography of the killifish Aphanius fasciatus (Teleostei, Cyprinodontidae) reveals highly divergent Mediterranean populations. Mar Biol 160(12):3193–3208

    Article  Google Scholar 

  13. Freyhof J, Esmaeili HR, Sayyadzadeh G, Geiger M (2014) Review of the crested loaches of the genus Paracobitis from Iran and Iraq with the description of four new species (Teleostei: Nemacheilidae). Ichthyol Explor Freshw 25(1):11–38

    Google Scholar 

  14. Gonzalez EG, Pedraza-Lara C, Doadrio I (2014) Genetic diversity and population history of the Endangered Killifish Aphanius baeticus. J Hered. 2014 Jun 17:esu034. Doi: https://doi.org/10.1093/jhered/esu034

  15. Gorbatenky GG, Byzgu SE, Kunichan LA (1986) Mineralization and ionic content of the Dniester water and prediction of changes in human impact. In modern state ecosystems of the Dniester River and reservoirs. Kishinev, Kodru

    Google Scholar 

  16. Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600

    CAS  PubMed  Google Scholar 

  17. Iguchi M, Okita K, Nakatani T, Kasai N (1997) Structure of turbulent round bubbling jet generated by premixed gas and liquid injection. Int J Multiphase Flow 23(2):249–262

    CAS  Article  Google Scholar 

  18. Jackson J, Priestley K, Allen M, Berberian M (2002) Active tectonics of the south Caspian basin. Geophys J Int 148(2):214–245

    Google Scholar 

  19. Khaefi R, Vatandoust S, Esmaeili HR (2017) Re-description of Barbus miliaris de Filippi, 1863 (Teleostei: Cyprinidae) from the endorheic Namak Lake basin of Iran. FishTaxa 2(1):33–42

    Google Scholar 

  20. Kotlik P, Bogutskaya NG, Ekmekci FG (2004) Circum Black Sea phylogeography of Barbus freshwater fishes: divergence in the Pontic glacial refugium. Mol Ecol 13(2004):87–95

    CAS  Article  PubMed  Google Scholar 

  21. Kotlik P, Marková S, Choleva L, Bogutskaya NG, Ekmekçi FG, Ivanova PP (2008) Divergence with gene flow between Ponto-Caspian refugia in an anadromous cyprinid Rutilus frisii revealed by multiple gene phylogeography. Mol Ecol 17(4):1076–1088

    CAS  Article  PubMed  Google Scholar 

  22. Kuksa VI (1994) Southern seas: the Aral, Caspian, Azov and black in conditions of anthropogenic stress. Gidrometeoizdat, Sankt-Peterburg, p 319

    Google Scholar 

  23. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    CAS  Article  PubMed  Google Scholar 

  24. Li WH (1997) Molecular Evolution. Sinauer, Sunderlan, Mass

    Google Scholar 

  25. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    CAS  Article  PubMed  Google Scholar 

  26. Liu H, Chen Y (2003) Phylogeny of the east Asian cyprinids inferred from sequences of the mitochondrial DNA control region. Can J Zool 81:1938–1946

    CAS  Article  Google Scholar 

  27. Lopes-Cunha M, Aboim MA, Mesquita N, Alves MJ, Doadrio I, Coelho MM (2012) Population genetic structure in the Iberian cyprinid fish Iberochondrostoma lemmingii (Steindachner, 1866): disentangling species fragmentation and colonization processes. Biol J Linn Soc 105(3):559–572

    Article  Google Scholar 

  28. Lukyanenko VI (2002) Destruction threat of the Caspian sturgeons and urgent measures in their rescuing. Utilization and Protection of Natural Resources in Russia Bulletin No 5–6

  29. MacManes M (2013) MacManes Salt Extraction Protocol. figshare

  30. Maggs CA, Castilho R, Foltz D, Henzler C, Jolly MT, Kelly J, Perez KE, Stam W, Vainola R, Viard F, Wares J (2008) Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology 89(Supplement):S108–S122

    Article  PubMed  Google Scholar 

  31. Martinez-Bouzas C, Castro A, Fernandez-Fernandez I, Rodriguez-Filgueira JL, de Pancorbo MM (2003) Genetic structure of autochthonous Basques through analysis of the HVI and HVII regions of mitochondrial DNA. International Congress S 1239:495–499

  32. Miller MP (1997) Tools for population genetic analyses (TFPGA) 1.3. A window program for the analysis of allozyme and molecular population genetic data. Computer software distributed by author

  33. Motamedi M, Madjdzadeh SM, Teimori A, Esmaeili HR, Mohsenzadeh S (2014) Morphological and molecular perspective on geographical differentiation of Barbus populations (Actinopterygii; Cyprinidae) within Iranian freshwater drainages. Turk J Fish Aquat Sc 14(2):339–351

    Google Scholar 

  34. Naseka AM (2010) Zoogeographical freshwater divisions of the Caucasus as a part of the west Asian transitional region. Proceedings of the zoological institute, Russian. Acad Sci 314(4):469–492

    Google Scholar 

  35. Nei M, Kumar S (2000) Molecular evolution and Phylogenetics. Oxford University Press, New York

    Google Scholar 

  36. Olden JD (2016) Challenges and opportunities for fish conservation in dam-impacted waters. In: Closs GP, Krkosek M, Olden JD (eds) Conservation of freshwater fishes. Cambridge University Press, Cambridge, pp 107–142

    Google Scholar 

  37. Ovenden L (1990) Peat accumulation in northern wetlands. Quat Res 33:377–386

    Article  Google Scholar 

  38. Peng Z, He S, Zhang Y (2004) Phylogenetic relationship of glyptosternoid fishes (Siluriformes: Sisoridae) inferred from mitochondrial cytochrome b gene sequence. Mol Phylogenet Evol 31:979–987

    CAS  Article  PubMed  Google Scholar 

  39. Perea S, Böhme M, Zupančič P, Freyhof J, Šanda R, Özuluğ M, Abdoli A, Doadrio I (2010) Phylogenetic relationships and biogeographical patterns in Circum-Mediterranean subfamily Leuciscinae (Teleostei, Cyprinidae) inferred from both miotochondrial and nuclear data. BMC Evol Biol 10:265

    Article  PubMed  PubMed Central  Google Scholar 

  40. Rambaut A, Drummond A (2009) Tracer, version 1.4. Computer program and documentation distributed by the author, website http://beast.bio.ed.ac.uk/Tracer

  41. Reilinger R, McClusky S, Vernant P, Lawrence S, Ergintav S, Cakmak R, Ozener H, Kadirov F, Guliev I, Stepanyan R, Nadariya M (2006) GPS constraints on continental deformation in the Africa-Arabia-Eurasia continental collision zone and implications for the dynamics of plate interactions. J Geophys Res Solid Earth 111(B05411):1–26. https://doi.org/10.1029/2005JB004051

  42. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed  PubMed Central  Google Scholar 

  43. Saadati MAG (1977) Taxonomy and distribution of the freshwater fishes of Iran. M.S. Thesis, Colorado State University, Fort Collins. xiii + 212 pp

  44. Saifali M, Arshad A, Yazdani Moghaddam F, Esmaeili HR, Hasanzadeh Kiabi B, Duad SK, Aliabadian M (2012) Molecular genetic differences of spirlin (Actinopterygii: Cyprinidae) in the Caspian Sea basin of Iran. Evol Bioinforma 8:219–227

    Google Scholar 

  45. Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337

    Article  Google Scholar 

  46. Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129(2):555–562

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  49. Teimori A, Mostafavi H, Esmaeili HR (2016) An update note on diversity and conservation of the endemic fishes in Iranian inland waters. Turk J Zool 40(1):87–102

    Article  Google Scholar 

  50. Templeton AR (2008) Gene flow, haplotype patterns and modern human origins. In:eLS. John Wiley & Sons Ltd, Chichester

  51. Wang M, Yang JX, Chen XY (2013) Molecular phylogeny and biogeography of Percocypris (Cyprinidae, Teleostei). PLoS One 8(6):e61827

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. Wu X, Luo J, Huang S, Chen Z, Xiao H, Zhang Y et al (2013) Molecular Phylogeography and evolutionary history of Poropuntius huangchuchieni (Cyprinidae) in Southwest China. PLoS One 8(11):e79975. https://doi.org/10.1371/journal.pone.0079975

    Article  PubMed  PubMed Central  Google Scholar 

  53. Xian Liu J, Gao T, Yokogawa K, Zhang Y (2006) Differential population structure and demographic history of two closely related and species, Japanese seabass (Lateolabrax japonicas) in the northwestern Pacific. Mol Phylogenet Evol 39:799–811

    Article  Google Scholar 

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Acknowledgements

We are pleased to thank, B.W. Coad and H.R. Zamanian for editing the ms; M. Masoudi, H. Mehraban, A. Gholamhosseini, R. Zamanianjejad, S. Vatandoust, A. Joladeh-Roudbal and G.H. Kamran for helping with fish collection in Iran. The research work was funded by Shiraz University and was approved by Ethics Committee of Biology Department of Shiraz University (ECBD-SU- 909821).

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Correspondence to Haimd Reza Esmaeili.

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Khaefi, R., Esmaeili, H.R., Ansari, M.H. et al. Genetic diversification and population structure of Barbus cyri De Filippi, 1865 (Teleostei: Cyprinidae) in northern Iran inferred from the mitochondrial D-loop gene sequence. Environ Biol Fish 101, 181–192 (2018). https://doi.org/10.1007/s10641-017-0690-2

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Keywords

  • Mitochondrial markers
  • Genetic diversity
  • Evolutionary relationships
  • D-loop