Diversity, mitochondrial phylogeny, and ichthyogeography of the Capoeta capoeta complex (Teleostei: Cyprinidae)

  • Halimeh Zareian
  • Hamid Reza Esmaeili
  • Ali Gholamhosseini
  • Bella Japoshvili
  • Müfit Özuluğ
  • Richard L. Mayden
Primary Research Paper

Abstract

Fish species of the genus Capoeta are known for their special mouth morphology (inferior mouth with the horny edge to the lower jaw), short dorsal fin with seven to nine branched rays, and their tumultuous taxonomic history. The genus Capoeta has had a complex evolutionary history with high diversification in the Middle East and is closely related with genus Luciobarbus. Earlier attempts to clarify the complex taxonomy of the group established four species groups, namely C. capoeta, C. damascina, C. tinca, and C. trutta species group. Based on this study, the C. capoeta group currently includes nine taxa (seven previous + two newly included members) and all reviewed in this paper based on morphological characters and mitochondrial genes. Capoeta macrolepis, revalidated as a distinct species, and Capoeta fusca are additional members of the C. capoeta group. Molecular time tree shows that the separation of Capoeta from its relative Luciobarbus was about 12.43–16.99 MYA. Based on the time tree presented herein, the high diversity of Capoeta in the Tigris–Euphrates system, the nesting of Capoeta within the tetraploid Luciobarbus in the mitochondrial trees and the high diversity of Luciobarbus in the Tigris–Euphrates system, it is proposed that the origination and diversification of Capoeta occurred in the palaeo-drainages of the Tigris–Euphrates system. From here, dispersion of Capoeta to the other nearby basins could have been possible through freshwater corridors during the Pliocene or Pleistocene.

Keywords

Capoeta Molecular analyses Systematics Biogeography Distribution 

References

  1. Abdurakhmanov, Yu A, 1962. Ryby Presnykh vod Azerbaidzhana [Freshwater Fishes of Azerbaidzhan]. Akademii Nauk Azerbaidzhanskoi SSR, Institut Zoologii, Baku: 407.Google Scholar
  2. Alwan, N., 2010. Systematics, taxonomy, phylogeny and zoogeography of the Capoeta damascina species complex (Pisces: Teleostei: Cyprinidae) inferred from comparative morphology and molecular markers. Unpublished PhD Thesis Dissertation. Johann Wolfgang Goethe-Universität, Frankfurt am Main.Google Scholar
  3. Alwan, N., H. R. Esmaeili & F. Krupp, 2016a. Molecular phylogeny and zoogeography of the Capoeta damascina species complex (Pisces: Teleostei: Cyprinidae). PLoS ONE 11: e0156434.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Alwan, N., H. Zareian & H. R. Esmaeili, 2016b. Capoeta coadi, a new species of cyprinid fish from the Karun River drainage, Iran based on morphological and molecular evidences (Teleostei, Cyprinidae). Zookeys 572: 155–180.CrossRefGoogle Scholar
  5. Amirinia, S., A., Bagherian & E., Jarfi, 2005. Karyotype of four Barbus species of Iran. Report submitted to the Ministry of Agriculture Jehad of Iran.Google Scholar
  6. Arai, R., 2011. Fish Karyotypes. A Check List. Springer, Tokyo.CrossRefGoogle Scholar
  7. Bănărescu, P. M., 1999. The Freshwater Fishes of Europe. Cyprinidae 2. Part I: Rhodeus to Capoeta, Vol. 5. Wiebelsheim: AULA-Verlag.Google Scholar
  8. Barrett, J. C., B. Fry, J. Maller & M. J. Daly, 2005. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21: 263.CrossRefPubMedGoogle Scholar
  9. Berberian, M. & R. S. Yeats, 1999. Patterns of historical earthquake rupture in the Iranian Plateau. Bulletin of the Seismological Society of America 89: 120–139.Google Scholar
  10. 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.Google Scholar
  11. Berg, L. S., 1964. Freshwater fishes of the U.S.S.R. and adjacent countries. 4th edition. Israel Program for Scientific Translations Ltd, Jerusalem, Israel.Google Scholar
  12. Berrebi, P., & C. S. Tsigenopoulos, 2003. Phylogenetic organization of the genus Barbus sensu stricto: a review based on data using molecular markers. In Bănărescu, P & N. G. Bogutskaya (eds) The Freshwater Fishes of Europe, Vol. 5/II: Cyprinidae, Part II: Barbus. AULA-Verlag: 11–22.Google Scholar
  13. Berrebi, P., A. Chenuil, P. Kotlík, A. Machordom & C. S. Tsigenopoulos, 2014. Disentangling the evolutionary history of the genus Barbus sensu lato, a twenty years adventure. In Alves, M. J., A. Cartaxana, A. M. Correia & L. F. Lopes (eds), Professor Carlos Almaça (1934–2010) – Estado da arte em áreas científicas do seu interesse. Museu Nacional de História Natural e da Ciência, Lisboa: 29–55.Google Scholar
  14. Bertin, L. & R. Estève, 1948. Catalogue des types de Poissons du Muséum National d’Histoire Naturelle. 4è partie Ostariophysaires (Cypriniformes). Paris.Google Scholar
  15. Bianco, P. G. & P. Bănărescu, 1982. A contribution to the knowledge of the Cyprinidae of Iran (Pisces, Cypriniformes). Cybium 6: 75–96.Google Scholar
  16. Bogutskaya, N. G. & A. M. Naseka, 2004. Katalog beschelyustnykh i ryb presnykh i solonovatykh vod Rossii c nomenklaturnymi i taksonomicheskimi kommentariyami [Catalogue of Agnathans and Fishes of Fresh and Brackish Waters of Russia with comments on nomenclature and taxonomy]. Zoological Institute, Russian Academy of Sciences and KMK Scientific Press Ltd, Moscow.Google Scholar
  17. Bruford, M. W., O. Hanotte, J. F. Y. Brokfield & T. Burke, 1992. Single-locus and multilocus DNA fingerprinting. In Hoelzel, A.R. (ed.) Molecular Genetic Analysis of Populations: A Practical Approach. Oxford University Press, New York: 225–269.Google Scholar
  18. Coad, B. W., 1979. Poisonous and venomous freshwater fishes of Iran. Pahlavi Medical Journal 9: 388–407.Google Scholar
  19. Coad, B. W., 1980. A provisional, annotated checklist of the freshwater fishes of Iran. Journal of the Bombay Natural History Society 76: 86–105.Google Scholar
  20. Coad, B. W. 1981. Fishes of Afghanistan, an annotated checklist. National Museum of Canada Publications in Zoology No. 14: i-v+1-26.Google Scholar
  21. Coad, B. W., 1991. Fishes of the Tigris-Euphrates Basin: a critical checklist. Syllogeus 68: 1–49.Google Scholar
  22. Coad, B. W., 1995. Freshwater fishes of Iran. Acta scientiarum naturalium Academiae scientiarum Bohemicae – Brno 29: 1–64.Google Scholar
  23. Coad, B. W., 1996. Fishes from the qanats of Iran. Publicaciones Especiales Instituto Español de Oceanografía 21: 63–79.Google Scholar
  24. Coad, B. W., 2014. Fishes of Afghanistan. Pensoft Publisher, Sofia, Moscow.Google Scholar
  25. Coad, B. W. 2017. Freshwater fishes of Iran. Retrieved from http://www.briancoad.com. Accessed: February 2017.
  26. Coad, B. W. & F. Krupp, 1994. Capoeta aculeata (Valenciennes in Cuv. and Val. 1844), a valid species of cyprinid fish from Iran (Teleostei: Cyprinidae). Zoology in the Middle East 10: 63–72.CrossRefGoogle Scholar
  27. Collares-Pereira, M. J. & J. M. Madeira, 1990. Cytotaxonomic studies in Iberian cyprinids. III. Karyology of Portuguese populations of Barbus Cuvier, 1817, with some reconsiderations on the karyological evolution of Cyprinidae. Caryologia 43: 17–26.CrossRefGoogle Scholar
  28. Collares-Pereira, M. J. & L. Moreira Da Costa, 1999. Intraspecific and interspecific genome size variation in Iberian Cyprinidae and the problem of diploidy and polyploidy, with review of genomes sizes within the family. Folia Zoologica 48: 61–76.Google Scholar
  29. Dadikyan, M. G., 1986. Ryby Armenii [Fishes of Armenia]. Izdatel’stvo Akademiya Nauk Armyanskoi SSR, Yerevan.Google Scholar
  30. Dercourt, J. E. A., L. P. Zonenshain, L. E. Ricou, V. G. Kazmin, X. Le Pichon, A. L. Knipper & B. Biju-Duval, 1986. Geological evolution of the Tethys belt from the Atlantic to the Pamirs since the Lias. Tectonophysics 123: 241–315.CrossRefGoogle Scholar
  31. Dorafshan, S. & A. Roozdar, 2016. Karyological analysis of small-scaled Damascus barbel, Capoeta damascina (Valenciennes, 1842) from Tigris Basin. Iranian Journal of Fisheries Sciences 15: 542–551.Google Scholar
  32. Drummond, A. J. & A. Rambaut, 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Drummond, A. J., S. Y. Ho, M. J. Phillips & A. Rambaut, 2006. Relaxed phylogenetics and dating with confidence. PLOS Biology 4: e88.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Durand, J. D., C. S. Tsigenopoulos, E. Unlu & P. Berrebi, 2002. Phylogeny and biogeography of the family Cyprinidae in the Middle East inferred from mitochondrial cytochrome b DNA evolutionary significance of the region. Molecular Phylogenetics and Evolution 22: 91–100.CrossRefPubMedGoogle Scholar
  35. Eschmeyer, F. & Van Der Laan 2017. Catalog of Fishes: Genera, Species, References.10/10/2016.Google Scholar
  36. Esmaeili, H. R., B. W. Coad, A. Gholamifard, N. Nazari & A. Teimory, 2010. Annotated checklist of the freshwater fishes of Iran. Zoosystematica Rossica 19: 361–386.Google Scholar
  37. Esmaeili, H. R., A. Teimori, G. Sayyadzadeh, M. Masoudi & B. Reichenbacher, 2014. Phylogenetic relationships of the tooth-carp Aphanius (Teleostei: Cyprinodontidae) in the river systems of southern and south-western Iran based on mtDNA sequences. Zoology in the Middle East 60: 29–38.CrossRefGoogle Scholar
  38. Esmaeili, H. R., S. Babai, A. Gholamifard, A. Pazira, A. Gholamhosseini & B. W. Coad, 2015. Fishes of the Persis region of Iran: an updated checklist and ichthyogeography. Iranian Journal of Ichthyology 2: 201–223.Google Scholar
  39. Esmaeili, H. R., H. Zareian, S. Eagderi & N. Alwan, 2016. Review on the taxonomy of Tigris scraper, Capoeta umbla (Heckel, 1843) and its confirmation record from the Iranian part of Tigris River, Persian Gulf basin (Teleostei: Cyprinidae). FishTaxa 1: 35–44.Google Scholar
  40. Felsenstein, J., 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.CrossRefPubMedGoogle Scholar
  41. Ghanavi, H. R., E. G. Gonzalez & I. Doadrio, 2016. Phylogenetic relationships of freshwater fishes of the genus Capoeta (Actinopterygii, Cyprinidae) in Iran. Ecology and Evolution 6: 8205–8222.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Gorshkova, G., S. Gorshkov & D. Golani, 2002. Karyotypes of Barbus canis and Capoeta damascina (Pisces, Cyprinidae) from the Middle East. Italian Journal of Zoology 69: 191–194.CrossRefGoogle Scholar
  43. Günther, A., 1868. Catalogue of the Physostomi in the Collection of the British Museum. London.Google Scholar
  44. Hall, T. A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.Google Scholar
  45. Heckel, J. J., 1843. Ichthyologie [von Syrien]. In von Russegger,J. Reisen in Europa, Asien und Africa, mit besonderer Rücksicht auf die naturwissenschaftlichen Verhältnisse der betreffenden Länder unternommen in den Jahren 1835 bis 1841, etc. E. Schweizerbart’sche Verlagshandlung, Vol. 1. Stuttgart: 990–1099.Google Scholar
  46. Heckel, J. J., 1849. Die Fische Persiens gesammelt von Theodor Kotschy. In Russegger, J. (ed.), Reisen in Europa, Asien und Afrika, Vol. 2. Stuttgart: Schweizerbartsche Verlagsbuchhandlung, Stuttgart: 255–335.Google Scholar
  47. Heckel, J. J., 1849. Naturhistorischer Anhang. In: J. Russegger (ed.) Reisen in Europa, Asien und Afrika, Vol. 2(3). Stuttgart: 209–357.Google Scholar
  48. Holčík, J. & L. Jedlička, 1994. Geographical variation of some taxonomically important characters in fishes: the case of the bitterling Rhodeus sericeus. Environmental Biology of Fishes 41: 147–170.CrossRefGoogle Scholar
  49. Horowitz, A., 1979. The Quaternary of Israel. Academic Press, Inc., New York: 1–394.Google Scholar
  50. Howes, G. J., 1982. Anatomy and evolution of the jaw in the semiplotine carps with a review of the genus Cyprinion Heckel, 1843 (Teleostei: Cyprinidae). Bulletin of the British Museum of Natural History 42: 299–335.Google Scholar
  51. Huelsenbeck, J. P. & B. Ranala, 2004. Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Systematic Biology 53: 904–913.CrossRefPubMedGoogle Scholar
  52. Johari, S. A., B. W. Coad, S. Mazloomi, M. Kheyri & S. Asghari, 2009. Biological and morphometric characteristics of Capoeta fusca, a cyprinid fish living in the qanats of south Khorasan, Iran (Osteichthyes: Cyprinidae). Zoology in the Middle East 47: 63–70.CrossRefGoogle Scholar
  53. Johari, S. A., S. Mazloumi, A. Abdoli, H. Khajavi & S. Asghari, 2010. Identification and distribution of fish fauna in qanats and standing rivers of Qae’nat (South Khorasan Province, I. R. Iran). Journal of Fisheries 4: 115–120. In Farsi.Google Scholar
  54. Jouladeh-Roudbar, A., S. Vatandoust, S. Eagderi, S. Jafari-Kenari & H. Mousavi-Sabet, 2015. Freshwater fishes of Iran; an updated checklist. AACL Bioflux 8: 855–909.Google Scholar
  55. Jouladeh-Roudbar, A., S. Eagderi, H. R. Ghanavi & I. Doadrio, 2016. Taxonomic review of the genus Capoeta Valenciennes, 1842 (Actinopterygii, Cyprinidae) from central Iran with the description of a new species. FishTaxa 1: 166–175.Google Scholar
  56. Jouladeh-Roudbar, A., S. Eagderi, H. R. Ghanavi & I. Doadrio, 2017. A new species of the genus Capoeta Valenciennes, 1842 from the Caspian Sea basin in Iran (Teleostei, Cyprinidae). ZooKeys 682: 137–155.CrossRefGoogle Scholar
  57. Kähsbauer, P., 1963. Zur Kenntnis der Ichthyofauna von Iran. Annalen des Naturhistorischen Museums Wien 66: 317–355.Google Scholar
  58. Karaman, M. S., 1969. Süßwasserfische der Türkei. 7. Teil. Revision der kleinasiatischen und vorderasiatischen Arten des Genus Capoeta (Varicorhinus, Partim). Mitteilungen aus dem hamburgischen Zoologischen Museum und Institut 66: 17–54.Google Scholar
  59. Keyserling, E., 1861. Neue Cypriniden aus Persien. Zeitschrift für die Gesammten. Naturwissenschaften Halle 17: 1–24.Google Scholar
  60. Kiliç, D. N. & E. Ünlü, 2001. Karyotypes of cyprinid fish Capoeta trutta and Capoeta capoeta umbla (Cyprinidae) from the Tigris River. Turkish Journal of Zoology 25: 389–393.Google Scholar
  61. Kinzelbach, R., 1980. Hydrobiologie am orontes. Natur und Museum 110(1): 9–18.Google Scholar
  62. Kinzelbach, R., 1987. Faunal history of some freshwater invertebrates of the northern Levant. In Krupp, F., W. Schneider, & R. Kinzelbach, (eds), Proceedings of the Symposium on the Fauna and Zoogeography of the Middle East, Mainz, 1985. Dr. Ludwig Reichert Verlag, Wiesbaden: 41–61.Google Scholar
  63. Kosswig, C., 1965. Zur historischen Zoogeographie der Ichthyofauna im Süsswasser des südlichen Kleinasiens. Zoologische Jahrbücher für Systematik 92: 83–90.Google Scholar
  64. Kosswig, C., 1973. Uber die Ausbreitungswege sogenannter perimediterraner Süsswasserfische. Bonner Zoologische Beiträge 24: 165–177.Google Scholar
  65. Kottelat, M. & J. Freyhof, 2007. Handbook of European Freshwater Fishes. Published by the authors, Cornol.Google Scholar
  66. Kozhara, A. V., Yu G Izyumov & A. N. Kas’yanov, 1996. General and geographic variation of the vertebral numbers in some freshwater fish. Journal of Ichthyology 36: 179–194.Google Scholar
  67. Krupp, F., 1985. Systematik und Zoogeographie der Süßwasserfische des levantinischen Grabenbruchsystems und der Ostküste des Mittelmeeres. Dissertation zur Erlangung des Grades “Doktor der Naturwissenschaften” am Fachbereich Biologie der Johannes Gutenberg - Universität in Mainz, Mainz.Google Scholar
  68. Krupp, F. 1987. Freshwater ichthyogeography of the Levant. In Krupp, F., W. Schneider, & R. Kinzelbach (eds), Proceedings of the Symposium on the Fauna and Zoogeography of the Middle East, Mainz, 1985. Beihefte zum Tübinger Atlas des Vorderen Orients, Reihe A (Naturwissenschaften), 28, Dr. Ludwig Reichert Verlag, Wiesbaden: 229–237.Google Scholar
  69. Krupp, F. & W. Schneider, 1989. The fishes of the Jordan River drainage basin and Azraq Oasis. Fauna of Saudi Arabia 10: 347–416.Google Scholar
  70. Krysanov, E. Y., 1999. Karyotypes of Varicorhinus capoeta and Barbus goktschaicus (Cypriniformes) from Lake Sevan, Armenia. Journal of Ichthyology 39: 187–189.Google Scholar
  71. Lévêque, C. & J. Daget, 1984. Cyprinidae. In Daget, J., Gosse, J.-P. (ed.), Thys van den Audenaerde DFE. Check-list of the freshwater fishes of Africa, Vol. I. Paris: ORSTOM. MRAC, Tervuren: 217–342.Google Scholar
  72. Levin, B. A., A. R. Rubenyan & V. B. Salnikov, 2005. Phenetic diversity of khramulya Capoeta capoeta (Ostariophysi, Cyprinidae). Journal of Ichthyology 45: 754–767.Google Scholar
  73. Levin, B. A., J. Freyhof, Z. Lajbner, S. Perea, A. Abdoli, M. Gaffaroğlu, M. Özulug, H. R. Rubenyan, V. B. Salnikov & I. Doadrio, 2012. Phylogenetic relationships of the algae scraping cyprinid genus Capoeta (Teleostei: Cyprinidae). Molecular Phylogenetics and Evolution 62: 542–549.CrossRefPubMedGoogle Scholar
  74. Levin, B. A., A. S. Golubtsov, Y. Y. Dgebuadze & N. S. Mugue, 2013. New evidence of homoplasy within the African genus Varicorhinus (Cyprinidae): an independent origin of specialized scraping forms in the adjacent drainage systems of Ethiopia inferred from mtDNA analysis. African Zoology 48: 400–406.CrossRefGoogle Scholar
  75. Naran, D., P. H. Skelton & M. H. Villet, 2007. Karyology of three evolutionarily hexaploid southern African species of yellowfish, Labeobarbus Rüppell, 1836 (Cyprinidae). African Zoology 42: 254–260.CrossRefGoogle Scholar
  76. Naseka, A. M., 1996. Comparative study on vertebral column in the Gobioninae (Cyprinidae, Pisces) with special reference to its systematics. Publicaciones Especiales Instituto Español de Oceanografía 21: 149–167.Google Scholar
  77. Naseka, A. M., 2010. Zoogeographical freshwater divisions of the Caucasus as a part of the West Asian Transitional Region. Proceedings of the Zoological Institute, Russian Academy of Sciences 314: 469–492.Google Scholar
  78. Nelson, J. S., T. Grande & M. V. H. Wilson, 2016. Fishes of the World, 5th ed. Wiley, New Jersey.CrossRefGoogle Scholar
  79. Nikolskii, A. M., 1897. Reptiles, amphibians and fishes, collected by N. A. Zarudnyi in eastern Persia. Ezhegodnik Zoologicheskogo Muzeya Imperatorskoi Akademii Nauk. St. Petersburg 2: 306–348. (in Russian).Google Scholar
  80. Nikolskii, A. M., 1899. Reptiles, amphibians and fishes collected on the second expedition of N. A. Zarudnyi to Persia in 1898. Ezhegodnik Zoologicheskago Muzeya Imperatorskoi Akademii Nauk. St. Petersburg 4: 375–417. (in Russian).Google Scholar
  81. Nikolskii, G. V., 1938. Ryby Tadzhikistana [Fishes of Tadzhikistan]. Izdatel’stvo Akademii Nauk SSSR, Leningrad (in Russian).Google Scholar
  82. Ocean Drilling Stratigraphic Network. http://www.odsn.de.
  83. Özuluğ, M. & J. Freyhof, 2008. Capoeta turani, a new species of barbel from River Seyhan, Turkey (Teleostei: Cyprinidae). Ichthyological Exploration of Freshwaters 19: 289–296.Google Scholar
  84. Palumbi, S. R., 1996. Nucleic acids II: The polymerase chain reaction. In Hillis, D. M., C. Moritz, & B. K. Mable (eds), Molecular Systematics, 2nd ed. Sinauer, Sunderland, MA.Google Scholar
  85. Perdices, A., J. A. Carmona, C. Fernandez-Delgado & I. Doadrio, 2001. Nuclear and mitochondrial data reveal high genetic divergence among Atlantic and Mediterranean populations of the Iberian killifish Aphanius iberus (Teleostei, Cyprinodotidae). Heredity 87: 314–324.CrossRefPubMedGoogle Scholar
  86. Por, F. D. & C. Dimentman, 1989. The legacy of Tethys. An aquatic biogeography of the Levant. Monographiae Biologicae 63: 214.Google Scholar
  87. Pourali, D. S., L. A. Bazyar & K. B. Hasanzadeh, 2006. A karyological study of Barbus capito, Barbus mursa and two populations of Capoeta capoeta from Northern Iran. Iranian Journal of Natural Resources 58: 831–842.Google Scholar
  88. Rainboth, W. J., 1981. Systematics of the Asiatic Barbins (Pisces, Cyprinidae). Unpublished Ph.D. Dissertation. The University of Michigan, Ann Arbor.Google Scholar
  89. Ramsay, A. T., C. W. Smart & J. C. Zachos, 1998. A model of early to middle Miocene deep ocean circulation for the Atlantic and Indian Oceans. Geological Society, London 131: 55–70.CrossRefGoogle Scholar
  90. Reshetnikov, Yu S & F. M. Shakirova, 1993. Zoogeograficheskii analiz ikhtiofauny srednei Asii po spiskam presnovodnykh ryb [Zoogeographical analysis of the ichthyofauna of Central Asia by lists of freshwater fish]. Voprosy Ikhtiologii 33: 37–45.Google Scholar
  91. Ronquist, F. & J. P. Huelsenbeck, 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.CrossRefPubMedGoogle Scholar
  92. Saadati, M., 1977. Taxonomy and distribution of the freshwater fishes of Iran. M. Sc. Thesis. Colorado State University, Fort Collins, Colorado.Google Scholar
  93. Safar, P., K. Mahmood, K. Bahram & S. Masoud, 2000. Karyological study of two populations of Capoeta capoeta from North Iran. Cytologia 65: 231–234.CrossRefGoogle Scholar
  94. Schmidt, T. R. & J. R. Gold, 1993. Complete sequence of the mitochondrial cytochrome b gene in the cherry fin shiner, Lythrurus roseipinnis (teleostei, Cyprinidae). Copeia 3: 880–883.CrossRefGoogle Scholar
  95. Stamatakis, A., 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.CrossRefPubMedGoogle Scholar
  96. Takin, M., 1972. Iranian geology and continental drift in the Middle East. Nature 235: 147–150.CrossRefGoogle Scholar
  97. Tamura, K., G. Stecher, D. Peterson, A. Filipski & S. Kumar, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.CrossRefPubMedPubMedCentralGoogle Scholar
  98. Tsigenopoulos, C. S., J. D. Durand, E. Ünlü & P. Berrebi, 2003. Rapid radiation of the Mediterranean Luciobarbus species (Cyprinidae) after the Messinian salinity crisis of the Mediterranean Sea, inferred from mitochondrial phylogenetic analysis. Biological Journal of the Linnean Society 80: 207–222.CrossRefGoogle Scholar
  99. Tsigenopoulos, C. S., P. Kasapidis & P. Berrebi, 2010. Phylogenetic relationships of hexaploid large-sized barbs (genus Labeobarbus, Cyprinidae) based on mtDNA data. Molecular Phylogenetics and Evolution 56: 851–856.CrossRefPubMedGoogle Scholar
  100. Turan, D., M. Kottelat, S. G. Kirankaya & S. Engin, 2006. Capoeta ekmekciae, a new species of cyprinid fish from northeastern Anatolia (Teleostei: Cyprinidae). Ichthyological Exploration of Freshwaters 17: 147–156.Google Scholar
  101. Turan, D., M. Kottelat & F. G. Ekmekçi, 2008. Capoeta erhani, a new species of cyprinid fish from Ceyhan River, Turkey (Teleostei: Cyprinidae). Ichthyological Exploration of Freshwaters 19: 263–270.Google Scholar
  102. Vaumas, E. De., 1957. Plateaux, plaines et dépressions de la Syrie intérieure septentrionale. Bull la Société géographie d’Égypte 30: 97–235.Google Scholar
  103. Vreven, E. J., T. Musschoot, J. Snoeks & U. K. Schliewen, 2016. The African hexaploid Torini (Cypriniformes: Cyprinidae): review of a tumultuous history. Zoological Journal of the Linnean Society 177: 231–305.CrossRefGoogle Scholar
  104. Ward, R. D., T. S. Zemlak, B. H. Innes, P. R. Last & P. D. N. Hebert, 2005. DNA barcoding Australia’s fish species. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 360: 1847–1857.CrossRefPubMedPubMedCentralGoogle Scholar
  105. Wolfart, R., 1967. Geologie von Syrien und dem Libanon. Gebrüder Bornträger, Berlin.Google Scholar
  106. Wossughi Gh., 1978. Beitrag zur Systematik und Zoogeographie der Cyprinidae (Pisces: Teleostei) des Mittleren Ostens, unter besonderer Berllcksichtigung des Irans. Ph.D. thesis, Fachbereich Biologie der Universitlit HamburgGoogle Scholar
  107. Yang, L., T. Sado, M. V. Hirt, E. Pasco-Viel, M. Arunachalam, J. Li, X. Wang, J. Freyhof, K. Saitoh, A. M. Simons, M. Miya, S. He & R. L. Mayden, 2015. Phylogeny and polyploidy: resolving the classification of cyprinine fishes (Teleostei: Cypriniformes). Molecular Phylogenetics and Evolution 85: 97–116.CrossRefPubMedGoogle Scholar
  108. Zareian, H., H. R. Esmaeili & J. Freyhof, 2016a. Capoeta anamisensis, a new species from the Minab and Hasan Langhi River drainages in Iran (Teleostei: Cyprinidae). Zootaxa 4083: 126–142.CrossRefPubMedGoogle Scholar
  109. Zareian, H., H. R. Esmaeili, A. Heidari, M. R. Khoshkholgh & H. Mousavi-Sabet, 2016b. Contribution to the molecular systematics of the genus Capoeta from the south Caspian Sea basin using mitochondrial cytochrome b sequences (Teleostei: Cyprinidae). Molecular Biology Research Communications 5: 65–75.PubMedPubMedCentralGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  • Halimeh Zareian
    • 1
  • Hamid Reza Esmaeili
    • 1
    • 5
  • Ali Gholamhosseini
    • 1
  • Bella Japoshvili
    • 2
  • Müfit Özuluğ
    • 3
  • Richard L. Mayden
    • 4
  1. 1.Ichthyology and Molecular Systematics Research Laboratory, Zoology Section, Department of Biology, College of SciencesShiraz UniversityShirazIran
  2. 2.Hydrobiology and Ichthyology Laboratory, Institute of ZoologyIlia State UniversityTbilisiGeorgia
  3. 3.Department of Biology, Faculty of ScienceIstanbul UniversityIstanbulTurkey
  4. 4.Department of BiologySaint Louis UniversitySt. LouisUSA
  5. 5.Department of Earth and Environmental Sciences, Palaeontology & GeobiologyLudwig-Maximilians-University MunichMunichGermany

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