Hydrobiologia

, Volume 785, Issue 1, pp 47–59 | Cite as

Dressing down: convergent reduction of the mental disc in Garra (Teleostei: Cyprinidae) in the Middle East

  • I. Hashemzadeh Segherloo
  • A. Abdoli
  • S. Eagderi
  • H. R. Esmaeili
  • G. Sayyadzadeh
  • L. Bernatchez
  • E. Hallerman
  • M. F. Geiger
  • M. Özulug
  • J. Laroche
  • J. Freyhof
Primary Research Paper

Abstract

In the Middle East, species of Garra are believed to have invaded the area in two independent waves from the Indo-Malayan biogeographic region. This hypothesis is based on the structure of the mental disc, a unique specialization of the lower lip, which is believed to be an adaptation to fast-flowing waters. While several species have such a mental disc, others completely lack a mental disc, being adapted to slow-moving water or to subterranean life. In this study, the phylogenetic relationships of Middle Eastern Garra species, including 16 described and 4 undescribed species, were analysed using mitochondrial cytochrome c oxidase I sequences. The results are concordant with traditional hypotheses on two invasion events; however, these invasion events are independent from the presence, absence or shape of the mental disc. We postulate convergent reduction of the mental disc in 5–6 independent lineages of Garra in the Middle East.

Keywords

COI Cyprinidae Labeonin Mental disc reduction Middle East 

Supplementary material

10750_2016_2902_MOESM1_ESM.docx (22 kb)
Supplementary material 1 (DOCX 22 kb)

References

  1. Altschul, S. F., T. L. Madden, A. A. Schäffer, J. Zhang, Z. Zhang, W. Miller & D. J. Lipman, 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25(17): 3389–3402.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bailey, R. G. & L. Ropes, 1998. Ecoregions: the ecosystem geography of the oceans and continents. Springer, Berlin.CrossRefGoogle Scholar
  3. Bănărescu, P., 1992. Zoogeography of Fresh Waters. Vol. 2. Distribution and Dispersal of Freshwater Animals in North America and Eurasia. Aula-Verlag, Wiesbaden: 520–1091.Google Scholar
  4. Behrens-Chapuis, S., F. Herder, M. Geiger, H. Esmaeili, N. Hamidan, M. Özuluğ & R. Šanda, 2015. Adding nuclear rhodopsin data where mitochondrial COI indicates discrepancies – can this marker help to explain conflicts in cyprinids? DNA Barcodes 3(1): 187–199.CrossRefGoogle Scholar
  5. Briggs, J. C., 1995. Global Biogeography. Elsevier.Google Scholar
  6. Brown, W. L. & E. O. Wilson, 1956. Character displacement. Systematic Zoology 5(2): 49–64.CrossRefGoogle Scholar
  7. Chu, X. & Y. Province, 1989. The Fishes of Yunnan, China, Part I. Cyprinidae. Science Press, Beijing.Google Scholar
  8. Coad, B. W., 2010. Freshwater Fishes of Iraq. Pensoft, Sofia and Moscow.Google Scholar
  9. Darriba, D., G. L. Taboada, R. Doallo & D. Posada, 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9(8): 772.CrossRefPubMedPubMedCentralGoogle Scholar
  10. De Laubenfels, D. J., 1975. Mapping the world’s vegetation. Regionalization of formations and flora. Syracuse Geographical Series (USA) no 4.Google Scholar
  11. Drummond, A. J., M. A. Suchard, D. Xie & A. Rambaut, 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29(8): 1969–1973.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Durand, J.-D., P. Bianco, J. Laroche & A. Gilles, 2003. Insight into the origin of endemic Mediterranean ichthyofauna: phylogeography of Chondrostoma genus (Teleostei, Cyprinidae). Journal of Heredity 94(4): 315–328.CrossRefPubMedGoogle Scholar
  13. Ellenberg, H. & D. Mueller-Dombois, 1969. A framework for a classification of world vegetation. UNESCO report SCWS/269, Paris.Google Scholar
  14. Eschmeyer, W. N., R. Fricke & R. van der Laan. 2016. Catalog of Fishes. http://www.calacademy.org/scientists/projects/catalog-of-fishes.
  15. Estoup, A., C. Largiader, E. Perrot & D. Chourrout, 1996. Rapid one-tube DNA extraction for reliable PCR detection of fish polymorphic markers and transgenes. Molecular Marine Biology and Biotechnology 5(4): 295–298.Google Scholar
  16. Fagan, B., 2014. The Attacking Ocean: The Past, Present, and Future of Rising Sea Levels. Bloomsbury Publishing, New York.Google Scholar
  17. Farashi, A., M. Kaboli, H. R. Rezaei, M. R. Naghavi, H. Rahimian & B. Coad, 2014. Reassessment of the taxonomic position of Iranocypris typhlops Bruun & Kaiser, 1944 (Actinopterygii, Cyprinidae). ZooKeys 374: 69–77.CrossRefGoogle Scholar
  18. Geiger, M., F. Herder, M. Monaghan, V. Almada, R. Barbieri, M. Bariche, P. Berrebi, J. Bohlen, M. Casal-Lopez & G. Delmastro, 2014. Spatial heterogeneity in the Mediterranean biodiversity hotspot affects barcoding accuracy of its freshwater fishes. Molecular Ecology Resources 14(6): 1210–1221.CrossRefPubMedGoogle Scholar
  19. Gray, S., B. Robinson & K. Parsons, 2005. Testing alternative explanations of character shifts against ecological character displacement in brook sticklebacks (Culaea inconstans) that coexist with ninespine sticklebacks (Pungitius pungitius). Oecologia 146(1): 25–35.CrossRefPubMedGoogle Scholar
  20. Guindon, S., J. F. Dufayard, V. Lefort, M. Anisimova, W. Hordijk & O. Gascuel, 2010. New algorithms and methods to estimate Maximum-Likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59(3): 307–321.CrossRefPubMedGoogle Scholar
  21. Hamidan, N. A., M. F. Geiger & J. Freyhof, 2014. Garra jordanica, a new species from the Dead Sea basin with remarks on the relationship of G. ghorensis, G. tibanica and G. rufa (Teleostei: Cyprinidae). Ichthyolology and Exploration of Freshwaters 25: 223–236.Google Scholar
  22. Hashemzadeh Segherloo, I., L. Bernatchez, K. Golzarianpour, A. Abdoli, C. Primmer & M. Bakhtiary, 2012. Genetic differentiation between two sympatric morphs of the blind Iran cave barb Iranocypris typhlops. Journal of Fish Biology 81(5): 1747–1753.CrossRefPubMedGoogle Scholar
  23. Hedges, S. B., 2001. Afrotheria: plate tectonics meets genomics. Proceedings of the National Academy of Sciences USA 98(1): 1–2.CrossRefGoogle Scholar
  24. Holdridge, L. R., 1967. Life zone ecology, rev ed. Centro Científico Tropical, San José.Google Scholar
  25. Huelsenbeck, J. P. & F. Ronquist, 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8): 754–755.CrossRefPubMedGoogle Scholar
  26. Ivanova, N. V., T. S. Zemlak, R. H. Hanner & P. D. Hebert, 2007. Universal primer cocktails for fish DNA barcoding. Molecular Ecology Notes 7(4): 544–548.CrossRefGoogle Scholar
  27. Karanth, P. K., 2006. Out-of-India Gondwanan origin of some tropical Asian biota. Current Science 90(6): 789–792.Google Scholar
  28. Kimura, M., 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16(2): 111–120.CrossRefPubMedGoogle Scholar
  29. Küçük, F. A., E. S. Bayçelebi, S. S. Güçlü & I. Gülle, 2015. Description of a new species of Hemigrammocapoeta (Teleostei: Cyprinidae) from Lake Isıklı, Turkey. Zootaxa 4052(3): 359–365.CrossRefPubMedGoogle Scholar
  30. 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.CrossRefPubMedGoogle Scholar
  31. Marshall, L. G., 1988. Land mammals and the great American interchange. American Scientist 76(4): 380–388.Google Scholar
  32. Menon, A. G. K., 1964. Monograph of the cyprinid fishes of the genus Garra Hamilton. Memoirs of the Indian Museum 14(4): 173–260.Google Scholar
  33. Pfennig, D. W. & K. S. Pfennig, 2010. Character displacement and the origins of diversity. The American Naturalist 176(Suppl 1): S26.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Pfennig, K. S. & D. W. Pfennig, 2009. Character displacement: ecological and reproductive responses to a common evolutionary problem. The Quarterly Review of Biology 84(3): 253.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Robinson, B. W. & D. W. Pfennig, 2013. Inducible competitors and adaptive diversification. Current Zoology 59(4): 537–552.CrossRefGoogle Scholar
  36. Robinson, B. W. & D. S. Wilson, 1994. Character release and displacement in fishes: a neglected literature. American Naturalist 144: 596–627.CrossRefGoogle Scholar
  37. Rögl, F., 1999. Mediterranean and Paratethys: facts and hypotheses of an Oligocene to Miocene paleogeography (short overview). Geologica Carpathica 50(4): 339–349.Google Scholar
  38. Ronquist, F. & J. P. Huelsenbeck, 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12): 1572–1574.CrossRefPubMedGoogle Scholar
  39. Sayyadzadeh, G., H. R. Esmaeili & J. Freyhof, 2015. Garra mondica, a new species from the Mond River drainage with remarks on the genus Garra from the Persian Gulf basin in Iran (Teleostei: Cyprinidae). Zootaxa 4048(1): 75–89.CrossRefPubMedGoogle Scholar
  40. Schluter, D., 2000. The Ecology of Adaptive Radiation. Oxford University Press, Oxford.Google Scholar
  41. Schmidthüsen, J., 1976. Atlas zur Biogeographie. Bibliographisches Institut, Zürich.Google Scholar
  42. Schultz, J., 1995. The Ecozones of the World: The Ecological Divisions of the Geosphere. Springer, Berlin.CrossRefGoogle Scholar
  43. Shermer, M., 2002. In Darwin’s Shadow: The Life and Science of Alfred Russel Wallace: A Biographical Study on the Psychology of History. Oxford University Press, Oxford.Google Scholar
  44. Stamatakis, A., 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22(21): 2688–2690.CrossRefPubMedGoogle Scholar
  45. Stiassny, M. L. & A. Getahun, 2007. An overview of labeonin relationships and the phylogenetic placement of the Afro-Asian genus Garra Hamilton, 1922 (Teleostei: Cyprinidae), with the description of five new species of Garra from Ethiopia, and a key to all African species. Zoological Journal of the Linnean Society 150(1): 41–83.CrossRefGoogle Scholar
  46. Talwar, P. K., 1991. Inland Fishes of India and Adjacent Countries, Vol. 2. CRC Press, Boca Raton, FL.Google Scholar
  47. Tamura, K., S. Glen, P. Daniel, F. Alan & K. Sudhir, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.CrossRefPubMedPubMedCentralGoogle Scholar
  48. Tang, Q., A. Getahun & H. Liu, 2009. Multiple in-to-Africa dispersals of labeonin fishes (Teleostei: Cyprinidae) revealed by molecular phylogenetic analysis. Hydrobiologia 632(1): 261–271.CrossRefGoogle Scholar
  49. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin & D. G. Higgins, 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25(24): 4876–4882.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 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(2): 851–856.CrossRefPubMedGoogle Scholar
  51. Vasilyan, D. & G. Carnevale, 2013. The Afro-Asian labeonine genus Garra Hamilton, 1822 (Teleostei, Cyprinidae) in the Pliocene of Central Armenia: Palaeoecological and palaeobiogeographical implications. Journal of Asian Earth Sciences 62: 788–796.CrossRefGoogle Scholar
  52. Wallace, A. R., 1876. The Geographical Distribution of Animals, with a Study of the Relations of Living and Extinct Faunas as Elucidating the Past Changes of the Earth’s Surface; with Maps and Illustrations; in Two Volumes. Cambridge University Press, Cambridge.Google Scholar
  53. Walter, H. & E. Box, 1976. Global classification of natural terrestrial ecosystems. Vegetatio 32(2): 75–81.CrossRefGoogle Scholar
  54. Xia, X., 2013. DAMBE5: a comprehensive software package for data analysis in molecular biology and evolution. Molecular Biology and Evolution 30(7): 1720–1728.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Xia, X. & P. Lemey, 2009. Assessing Substitution Saturation with DAMBE. In Salemi, M. & A.-M. Vandamme (eds), The phylogenetic handbook: a practical approach to DNA and protein phylogeny. Cambridge University Press, Cambridge: 615–630.CrossRefGoogle Scholar
  56. Xia, X., Z. Xie, M. Salemi, L. Chen & Y. Wang, 2003. An index of substitution saturation and its application. Molecular Phylogenetics and Evolution 26(1): 1–7.CrossRefPubMedGoogle Scholar
  57. Yang, L. & R. L. Mayden, 2010. Phylogenetic relationships, subdivision, and biogeography of the cyprinid tribe Labeonini (sensu) (Teleostei: Cypriniformes), with comments on the implications of lips and associated structures in the labeonin classification. Molecular Phylogenetics and Evolution 54(1): 254–265.CrossRefPubMedGoogle Scholar
  58. Yang, L., M. Arunachalam, T. Sado, B. A. Levin, A. S. Golubtsov, J. Freyhof, J. P. Friel, W.-J. Chen, M. Vincent Hirt & R. Manickam, 2012. Molecular phylogeny of the cyprinid tribe Labeonini (Teleostei: Cypriniformes). Molecular Phylogenetics and Evolution 65(2): 362–379.CrossRefPubMedGoogle Scholar
  59. Zhang, E., 2005. Phylogenetic relationships of labeonine cyprinids of the disc-bearing group (Pisces: Teleostei). Zoological Studies 44(1): 130–143.Google Scholar
  60. Zheng, L., Y. Junxing & C. Xiaoyong, 2012. Phylogeny of the Labeoninae (Teleostei, Cypriniformes) based on nuclear DNA sequences and implications on character evolution and biogeography. Current Zoology 58(6): 837–850.CrossRefGoogle Scholar
  61. Zhou, W., X.-F. Pan & M. Kottelat, 2005. Species of Garra and Discogobio (Teleostei: Cyprinidae) in the Yuanjiang (Upper Red River) drainage of Yunnan Province, China with a description of a new species. Zoological Studies Taipei 44(4): 445.Google Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • I. Hashemzadeh Segherloo
    • 1
  • A. Abdoli
    • 2
  • S. Eagderi
    • 3
  • H. R. Esmaeili
    • 4
  • G. Sayyadzadeh
    • 4
  • L. Bernatchez
    • 5
  • E. Hallerman
    • 6
  • M. F. Geiger
    • 7
  • M. Özulug
    • 8
  • J. Laroche
    • 5
  • J. Freyhof
    • 9
  1. 1.Department of Fisheries and Environmental Sciences, Faculty of Natural Resources and Earth SciencesShahr-e-Kord UniversityShahr-e-KordIran
  2. 2.Department of Biodiversity and Ecosystem Management, Environmental Science Research InstituteShahid Beheshti UniversityTehranIran
  3. 3.Department of Fisheries, Faculty of Natural ResourcesUniversity of TehranKarajIran
  4. 4.Department of Biology, College of SciencesShiraz UniversityShirazIran
  5. 5.Institut de Biologie Intégrative et des Systèmes (IBIS), Pavillon Charles-Eugène-MarchandUniversité LavalQuebec CityCanada
  6. 6.Department of Fish and Wildlife Conservation, College of Natural Resources and EnvironmentVirginia Polytechnic Institute and State UniversityBlacksburgUSA
  7. 7.Zoological Research Museum A. Koenig - Leibniz Institute for Animal Biodiversity, Foundation under Public LawBonnGermany
  8. 8.Department of Biology, Faculty of ScienceIstanbul UniversityIstanbulTurkey
  9. 9.German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-LeipzigLeipzigGermany

Personalised recommendations