Phylogenetic relationships and taxonomy of Luciobarbus barbulus (Heckel, 1847) (Teleostei: Cyprinidae)

Abstract

Luciobarbus barbulus (Heckel, 1847), a cyprinid fish of the Persian Gulf basin is re-described. Its identity is discussed and its phylogenetic relationship among the tribe Barbini is reconstructed. Luciobarbus barbulus can be distinguished from its close species, L. pectoralis by having thicker lower lip, stronger last unbranched dorsal fin ray and with stronger serration, longer barbels and posterior barbel passes the middle of the eye (vs. not reaching the middle of the eye in L. pectoralis), confirming the identity of both, as distinct species. Moreover, phylogenetic analysis based on the mtCOI sequences, placed the sequenced L. barbulus in a distinct clade corresponding to the tribe Barbini which includes Aulopyge, Barbus and Luciobarbus (three genera from Eurasia and North of Africa), sister to L. pectoralis from Orontes River with genetic distance of 1.7% applying the Kimura 2 Parameter (K2P) model.

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

References

  1. Almaça, C., Remarks on some Heckel’s species of Barbus from western Asia, Arq. Mus. Nac., B, 1983, vol. 2, no. 12, pp. 95–102.

    Google Scholar 

  2. Almaça, C., Notes on some species of western Palaearctic Barbus (Cyprinidae, Pisces), Arq. Mus. Nac., C, 1984a, vol. 2, no. 1, pp. 1–76.

    Google Scholar 

  3. Almaça, C., Form relationships among western Palaearctic species of Barbus (Cyprinidae, Pisces), Arq. Mus. Nac., A, 1984b, vol. 2, no. 12, pp. 207–248.

    Google Scholar 

  4. Almaça, C., On some Barbus species from Western Asia (Cyprinidae, Pisces), Ann. Naturhist. Mus. Wien, Ser. B, 1986, vol. 87, pp. 5–30.

    Google Scholar 

  5. Almaça, C., Evolutionary, biogeographical, and taxonomical remarks on Mesopotamian species of Barbus s.s., Arq. Mus. Nac., Nova Ser., 1991, vol. 2, no. 4, pp. 63–78.

    Google Scholar 

  6. Bănărescu, P.M. and Bogutskaya, N.G., The Freshwater Fishes of Europe, Vol. 5/II: Cyprinidae 2, Part II: Barbus, Wiebelsheim: Aula Verlag, 2003.

    Google Scholar 

  7. Banister, K.E., A revision of the large Barbus (Pisces: Cyprinidae) of East and Central Africa. Studies on African Cyprinidae Part II. Bull. Br. Mus. Nat., 1973, vol. 26, pp. 1–148.

    Google Scholar 

  8. Berg, L.S., Ryby presnykh vod SSSR i sopredel’nykh stran (Freshwater Fishes of Soviet Union and Adjacent Countries), Moscow: Akad. Nauk SSSR, 1949, vol. 2.

  9. Bergsten, J., Bilton, D.T., Fujisawa, T., Elliott, M., Monaghan, M.T., Balke, M., Hendrich, L., Geijer, J., Her rmann, J., Foster, G.N., and Ribera, I., The effect of geographical scale of sampling on DNA barcoding, Syst Biol., 2012, vol. 61, no. 5, pp. 851–869.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Bogutskaya, N.G. and Naseka, A.M., Katalog neschelyustnykh i ryb presnykh and solonovatykh vod Rossii (Catalogue of Agnatha Species and Fishes from Fresh and Brackish Waters of Russia), Moscow: KMK, 2004.

    Google Scholar 

  11. Borkenhagen, K., A new genus and species of cyprinid fish (Actinopterygii, Cyprinidae) from the Arabian Peninsula, and its phylogenetic and zoogeographic affinities, Environ. Biol. Fish., 2014, vol. 97, no. 10, pp. 1179–1195.

    Article  Google Scholar 

  12. Borkenhagen, K. and Krupp, F., Taxonomic revision of the genus Carasobarbus Karaman, 1971 (Actinopterygii, Cyprinidae), ZooKeys, 2013, no. 339, pp. 1–53.

    Article  Google Scholar 

  13. Boulenger, G.A., On some freshwater fishes from Smyrna, Ann. Mag. Nat. Hist., Ser. 6, 1896, vol. 18, pp. 153–154.

    Article  Google Scholar 

  14. Boulenger, G.A., Catalogue of the Fresh-Water Fishes of Africa in the British Museum (Natural History), London: Br. Mus. Nat. Hist., 1911, vol. 2.

  15. Casal-Lopez, M., Perea, S., Yahyaoui, A., and Doadrio, I., Taxonomic review of the genus Luciobarbus Heckel, 1843 (Actinopterygii, Cyprinidae) from northwestern Morocco with the description of three new species, Graellsia, 2015, vol. 71, no. 2, p. e027.

    Article  Google Scholar 

  16. Chenuil, A., Galtier, N. and Berrebi, P., A test of the hypothesis of an autopolyploid vs. allopolyploid origin for a tetraploid lineage: application for the genus Barbus, Heredity, 1999, vol. 82, pp. 373–380. doi 10.1038/sj.hdy.6884890

    Article  PubMed  Google Scholar 

  17. Coad, B.W., Zoogeography of the fishes of the Tigris- Euphrates Basin, Zool. Middle East, 1996, vol. 13, pp. 51–70.

    Article  Google Scholar 

  18. Coad, B.W., Personal website. http://www.briancoad.com. Accessed February 2017.

    Google Scholar 

  19. Doadrio, I., Phylogenetic relationships and classification of western Palaearctic species of the genus Barbus (Osteichthyes, Cyprinidae), Aquat. Living Resour., 1990, vol. 3, pp. 265–282.

    Article  Google Scholar 

  20. Durand, J.D., Tsigenopoulos, C.S., Unlu, E., and Berrebi, P., Phylogeny and biogeography of the family Cyprinidae in the Middle East inferred from cytochrome b DNA—evolutionary significance of this region, Mol. Phylogenet. Evol., 2002, vol. 22, pp. 91–100. doi 10.1006/mpev.2001.1040

    CAS  Article  PubMed  Google Scholar 

  21. Eschmeyer, W.N. and Fong, J.D., Species by family/subfamily, in Catalog of Fishes, San Francisco: Calif. Acad. Sci., 2015.

    Google Scholar 

  22. Esmaeili, H.R., Coad, B.W., Gholamifard, A., Nazari, N., and Teimory, A., Annotated checklist of the freshwater fishes of Iran, Zoosyst. Ross., 2010, vol. 19, pp. 361–386.

    Google Scholar 

  23. Esmaeili, H.R., Teimori, A., Owfi, F., Abbasi, K., and Coad, B.W., Alien and invasive freshwater fish species in Iran: Diversity, environmental impacts and management, Iran. J. Ichthyol., 2014a, vol. 1, no. 2, pp. 62–72.

    Google Scholar 

  24. Esmaeili, H.R., Coad, B.W., Mehraban, H.R., Masoudi, M., Khaefi, R., Abbasi, K., Mostafavi, H., and Vatandoust, S., An updated checklist of fishes of the Caspian Sea basin of Iran with a note on their zoogeography, Iran. J. Ichthyol., 2014b, vol. 1, pp. 152–184.

    Google Scholar 

  25. Esmaeili, H.R., Mehraban, H., Abbasi, K., Eagderi, S., Keivany, Y., and Coad, B., Review and updated checklist of freshwater fishes of Iran: Taxonomy, distribution and conservation status, Iran. J. Ichthyol., 2017, vol. 4, suppl. 1, pp. 1–114.

    Google Scholar 

  26. Galtier, N., Gouy, M., and Gautier, C., SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny, Comput. Appl. Biosci., 1996, vol. 12, no. 6, pp. 543–548.

    CAS  PubMed  Google Scholar 

  27. Geiger, M., Herder, F., Monaghan, M., Almada, V., Barbieri, R., Bariche, M., Berrebi, P., Bohlen, J., Casal-Lopez, M., Delmastro, G., Denys, G., Dettai, A., Doadrio, I., Kalogianni, E., Kärst, H., et al., Spatial heterogeneity in the Mediterranean Biodiversity Hotspot affects barcoding accuracy of its freshwater fishes, Mol. Ecol. Resour., 2014, vol. 14, pp. 1210–1221.

    CAS  Article  PubMed  Google Scholar 

  28. Geldiay, R. and Balık, S., Türkiye Tatlısu Balıkları, Izmir: Ege Üniv. Ürünleri Fak. Yayınları, 1999, no. 16, p. 46.

    Google Scholar 

  29. Griffiths, H.I., Schwalb, A., and Stevens, L.R., Environmental change in southwestern Iran: the Holocene ostracod fauna of Lake Mirabad, Holocene, 2001, vol. 11, no. 6, pp. 757–764.

    Article  Google Scholar 

  30. Hall, T.A., BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT, Nucleic Acids Symp. Ser., 1999, vol. 41, pp. 95–98.

    CAS  Google Scholar 

  31. Heckel, J.J., Naturhistorischer Anhang. Die Fische persiens, gesammelt von Theodor Kotschy, in Reisen in Europa, Asien und Afrika, mit Besonderer Beruecksichtigung auf Dienaturwissenschaflichen Verhaeltnisse der Betreffenden Länder, Unternommen in den Jahren 1835 bis 1841, Stuttgart: E. Schweizerbartsche Verlag, 1841, vol. 2, part 3, pp. 255–272.

    Google Scholar 

  32. Heckel, J.J., Abbildungen und Beschreibungen der Fische Syriensnebsteinerneuen Classification und Characteristiksämmtlicher Gattungen der Cyprinen, Stuttgart., 1843.

    Google Scholar 

  33. Howes, G.J., The phylogenetic position of the Yugoslavian cyprinid fish genus Aulopyge Heckel, 1841, with an appraisal of the genus Barbus Cuvier & Cloquet, 1816 and the subfamily Cyprininae, Bull. Br. Mus. Nat. Hist., Zool., 1987, vol. 52, no. 5, pp. 165–196.

    Google Scholar 

  34. Ivanova, N.V., Zemlak, T.S., Hanner, R.H., and Hebert, P.D.N., Universal primer cocktails for fish DNA barcoding, Mol. Ecol. Notes, 2007, vol. 7, pp. 544–548. doi 10.1111/j.1471-8286.2007.01748.x

    CAS  Article  Google Scholar 

  35. Jouladeh-Roudbar, A., Vatandoust, S., Eagderi, S., Jafari-Kenari, S., and Mousavi-Sabet, H., Freshwater fishes of Iran; an updated checklist, AACL Bioflux, 2015, vol. 8, no. 6, pp. 855–909.

    Google Scholar 

  36. Karaman, M.S., Süßwasserfische der Türkei. 8. Teil. Revision der BarbenEuropas, Vorderasiens und Nordafrikas, Mitt. Hamb. Zool. Mus. Inst., 1971, vol. 67, pp. 175–254.

    Google Scholar 

  37. Kottelat, M. and Freyhof, J., Handbook of European Freshwater Fishes, Cornol: Kottelat, 2007.

    Google Scholar 

  38. Krupp, F., Systematik und Zoogeographie der Süßwasserfische des levantinischen Grabenbruchsystems und der Ostküste des Mittelmeeres, Dissertation Doktor der Naturwissenschaften, Mainz: Johannes Gutenberg-Univ. Mainz, 1985.

    Google Scholar 

  39. Kuru, M., Recent systematic status of inland fishes of Turkey, GÜ, Gazi Eğitim Fakültesi Dergisi, 2004, vol. 24, no. 3, pp. 1–21.

    Google Scholar 

  40. Levin, B.A., Freyhof, J., Lajbner, Z., Perea, S., Abdoli, A., Gaffaroğlu, M., Özuluğ, M., Rubenyan, H.R., Salnikov, V.B., and Doadrio, I., Phylogenetic relationships of the algae scraping cyprinid genus Capoeta (Teleostei: Cyprinidae), Mol. Phylogenet. Evol., 2011, vol. 62, no. 1, pp. 542–549. doi 10.1016/j.ympev.2011.09.004

    Article  PubMed  Google Scholar 

  41. Machordom, A. and Doadrio, I., Evolutionary history and speciation modes in thecyprinid genus Barbus, Proc. R. Soc. London, Ser. B, 2001, vol. 268, pp. 1297–1306. doi 10.1098/rspb.2001

    CAS  Article  Google Scholar 

  42. Nelson, J.S., Fishes of the World, New York: Wiley, 2016, 5th ed.

    Google Scholar 

  43. Perdices, A., Carmona, J.A., Fernández-Delgado, C., and Doadrio, I., Nuclear and mitochondrial data reveal high genetic divergence among Atlantic and Mediterranean populations of the Iberian killifish Aphanius iberus (Teleostei: Cyprinodontidae), Heredity, 2001, vol. 87, no. 3, pp. 314–324. doi 10.1046/j.1365-2540.2001.00888.x

    CAS  Article  PubMed  Google Scholar 

  44. Poll, M. and Lambert, J., Barbus choutedeni, espéce nouvelle du sous genre, Rev. Zool. Bot. Afr., 1961, vol. 64, pp. 265–271.

    Google Scholar 

  45. Stamatakis, A., RAxML-VI-HPC: maximum likelihoodbased phylogenetic analyses with thousands of taxa and mixed models, Bioinformatics, 2006, vol. 22, pp. 2688–2690. https://doi.org/10.1093/bioinformatics/btl446.

    CAS  Article  PubMed  Google Scholar 

  46. Stiassny, M.L.J. and Sakharova, H., Review of the smiliogastrin cyprinids of the Kwilu River (Kasai Basin, central Africa), revised diagnosis for Clypeobarbus (Cyprinidae: Cyprininae: Smiliogastrini) and description of a new species, J. Fish. Biol., 2016, vol. 88, no. 4, pp. 1394–1412.

    CAS  Article  PubMed  Google Scholar 

  47. Tsigenopoulos, C.S. and Berrebi, P., Molecular phylogeny of north Mediterranean freshwater barbs (genus Barbus: Cyprinidae) inferred from cytochrome b sequences: biogeographic and systematic implications, Mol. Phylogenet. Evol., 2000, vol. 14, no. 2, pp. 165–179. doi 10.1006/mpev. 1999.0702

    CAS  Article  PubMed  Google Scholar 

  48. Tsigenopoulos, C.S., Durand, J.D., Ünlü, E., and Berrebi, P., Rapid radiation of the Mediterranean Luciobarbus species (Cyprinidae) after the Messinian salinity crisis of the Mediterranean Sea, inferred from mitochondrial phylogenetic analysis, Biol. J. Linn. Soc., 2003, vol. 80, no. 2, pp. 207–222.

    Article  Google Scholar 

  49. Tsigenopoulos, C.S., Kasapidis, P., and Berrebi, P., Phylogenetic relationships of hexaploid large-sized barbs (genus Labeobarbus, Cyprinidae) based on mtDNA data, Mol. Phylogenet. Evol., 2010, vol. 56, pp. 851–856. doi 10.1016/j.ympev.2010.02.006

    Article  PubMed  Google Scholar 

  50. Turan, D., Ekmekçi, F.G., Ilhan, A., and Engin, S., Luciobarbus kottelati, a new species of barbel (Teleostei: Cyprinidae) from the Büyük Menderes River, Turkey, with rediagnose of L. lydianus, Zootaxa, 2008, vol. 1824, pp. 35–44.

    Google Scholar 

  51. Valiallahi, J., A revision of Barbus species of Iran (Cypriniformes: Cyprinidae), PhD Thesis, Tehran: Univ. of Tarbiat Modares, 2000.

    Google Scholar 

  52. Yang, L., Sado, T., Hirt, M.V., Pasco-Viel, E., Arunachalam, M., Li, J., Wang, X., Freyhof, J., Saitoh, K., Simons, A.M., and Miya, M., Phylogeny and polyploidy: resolving the classification of cyprinine fishes (Teleostei: Cypriniformes), Mol. Phylogenet. Evol., 2015, vol. 85, pp. 97–116. doi 10.1016/j.ympev.2015.01.014

    Article  PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to H. R. Esmaeili.

Additional information

The article is published in the original.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Khaefi, R., Teimori, A. & Esmaeili, H.R. Phylogenetic relationships and taxonomy of Luciobarbus barbulus (Heckel, 1847) (Teleostei: Cyprinidae). J. Ichthyol. 57, 835–845 (2017). https://doi.org/10.1134/S0032945217060078

Download citation

Keywords

  • COI sequences
  • freshwater fish
  • Middle East
  • biodiversity
  • Luciobarbus pectoralis