Morphometry and DNA barcoding reveal cryptic diversity in the genus Enteromius (Cypriniformes: Cyprinidae) from the Congo basin, Africa

  • Marjolein Van Ginneken Department of Biology, Systemic Physiological and Ecotoxicological Research, University of Antwerp, Groenenborgerlaan 171, 2020 Antwerpen
  • Eva Decru Royal Museum for Central Africa, Section Vertebrates, Ichthyology, Leuvensesteenweg 13, 3080 Tervuren and Department of Biology, Laboratory of Biodiversity and Evolutionary Genomics, KU Leuven, Charles Deberiotstraat 32, 3000 Leuven
  • Erik Verheyen Royal Belgian Institute of Natural Sciences, OD Taxonomy and Phylogeny, Vautierstraat 29, 1000 Brussels, Belgium; Department of Biology, Evolutionary Ecology Group, University of Antwerpen, Campus Drie Eiken, building D, room D.150 Universiteitsplein 1, 2610 Antwerpen
  • Jos Snoeks Royal Museum for Central Africa, Section Vertebrates, Ichthyology, Leuvensesteenweg 13, 3080 Tervuren and Department of Biology, Laboratory of Biodiversity and Evolutionary Genomics, KU Leuven, Charles Deberiotstraat 32, 3000 Leuven
DOI: https://doi.org/10.5852/ejt.2017.310
Keywords: ‘Barbus’, COI, integrative taxonomy, species richness

Abstract

One of the main challenges to adequately conserve the African fish fauna is to improve our so far unsatisfactory taxonomic knowledge of important portions of the ichthyofauna. In the present study, we attempted to unravel the taxonomic diversity of some species of Enteromius Cope, 1867, a problematic African fish genus, recently collected in the north-eastern part of the Congo basin. We used an integrative approach, combining DNA barcodes and morphological analyses. For one of the species complexes found, the E. miolepis/eutaenia species complex, we evaluated taxonomic diversity over a larger geographic scale within the Congo drainage system. Although initial literature-based species identifications allowed us to assign all examined specimens to four tentative species, DNA barcodes indicated the presence of 23 distinct mitochondrial lineages. The majority of these lineages appeared endemic to particular rivers, and in most rivers multiple lineages occur in sympatry. Subsequent exploratory morphometric analyses indicated that almost all these lineages are morphologically distinguishable and that they may therefore represent undescribed species. As only a part of the Congo basin and a subset of the species diversity within Enteromius were examined, it appears that the species richness of Enteromius in the Congo basin is severely underestimated.

References

Agnèse J.F., Berrebi P., Lévêque C. & Guégan J.F. 1990. Two lineages, diploid and tetraploid, demonstrated in African species Barbus (Osteichthyes, Cyprinidae). Aquatic Living Resources 3: 305–311. https://doi.org/10.1051/alr:1990031

Bamba M. 2012. The ‘Barbus’ species (Cypriniformes, Cyprinidae) from Côte d’Ivoire: A Systematic Revision of Some West African Species Complexes. PhD thesis, KU Leuven, Belgium.

Bamba M., Vreven E.J. & Snoeks J. 2011. Description of Barbus teugelsi sp. nov. (Cypriniformes: Cyprinidae) from the Little Scarcies basin in Guinea, Africa. Zootaxa 2988: 48–65.

Banyankimbona G., Vreven E. & Snoeks J. 2012. ‘Barbus’ devosi, new species from the Malagarazi River basin in Burundi and Tanzania, East Africa (Cypriniformes: Cyprinidae). Ichthyological Exploration of Freshwaters 23: 181–192.

Becker S., Hanner R.H. & Steinke D. 2011. Five years of FISH-BOL: Brief status report. Mitochondrial DNA 22: 3–9. https://doi.org/10.3109/19401736.2010.535528

Berrebi P. & Tsigenopoulos C.S. 2003. Phylogenetic organization of the genus Barbus sensu stricto: A review based on data obtained using molecular markers. In: Bãnãrescu P.M. & Bogutskaya N.G. (eds) The Freshwater Fishes of Europe Volume 5/II Cyprinidae 2, Part II: Barbus: 11–22. Aula-Verlag, Wiesbaden.

Berrebi P. & Valiushok D. 1998. Genetic divergence among morphotypes of Lake Tana (Ethiopia) barbs. Biological Journal of the Linnean Society 64: 369–384. https://doi.org/10.1111/j.1095-8312.1998.tb00338.x

Berrebi P., Kottelat M., Skelton P. & Rab P. 1996. Systematics of Barbus: State of the art and heuristic comments. Folia Zoologica 45: 5–12.

Berrebi P., Chenuil A., Kotlik P., Machordom A. & Tsigenopoulos C.S. 2014. Disentangling the evolutionary history of the genus Barbus sensu latu, a twenty years adventure. In: Alves M.J., Cartaxana A., Correia A.M. & Lopes L.F. (eds) Professor Carlos Almaça (1934–2010) – Estado da arte em áreas científicas do seu interesse: 29–55. Museu Nacional de História Natural e da Ciência, Lisboa.

Bookstein F.L., Chernoff B., Elder R.L., Humphries J.M., Smith G.R. & Strauss R.E. 1985. Morpho-metrics in Evolutionary Biology: the Geometry of Size and Shape Change, with Examples from Fishes. Academy of Natural Sciences of Philadelphia, Philadelphia.

Collins R.A. & Cruickshank R.H. 2012. The seven deadly sins of DNA barcoding. Molecular Ecology Resources 13: 969–975. https://doi.org/10.1111/1755-0998.12046

Decru E., Vreven E. & Snoeks J. 2012. A revision of the West African Hepsetus (Characiformes; Hepsetidae) with a description of H. akawo sp. nov. and a redescription of H. odoe (Bloch, 1794). Journal of Natural History 46: 1–23. https://doi.org/10.1080/00222933.2011.622055

Decru E., Moelants T., De Gelas K., Vreven E., Verheyen E. & Snoeks J. 2016. Taxonomic challenges in freshwater fishes: a mismatch between morphology and DNA barcoding in fish of the north-eastern part of the Congo basin. Molecular Ecology Resources 16: 342–352. https://doi.org/10.1111/1755-0998.12445

DeSalle R., Egan M.G. & Siddall M. 2011. The unholy trinity, taxonomy, species delimitation and DNA barcoding. Philosophical Transactions of the Royal Society B 360: 1905–1916. https://doi.org/10.1098/rstb.2005.1722

Edgar R.C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792–1797. https://doi.org/10.1093/nar/gkh340

Fernández M.H. & Vrba E.S. 2005. A complete estimate of the phylogenetic relationships in Ruminantia: a dated species-level supertree of the extant ruminants. Biological Reviews 80: 269–302. https://doi.org/10.1017/s1464793104006670

Fouquet A., Gilles A., Vences M., Marty C., Blanc M. & Gemmell N.J. 2007. Underestimation of species richness in Neotropical frogs revealed by mtDNA analyses. PLoS ONE 2: e1109. https://doi.org/10.1371/journal.pone.0001109

Froese R. & Pauly D. 2017. FishBase. Available from www.fishbase.org [accessed 30 Mar. 2017].

Golubtsov A.S. & Krysanov E.Y. 1993. Karyological study of some cyprinid species from Ethiopia. The ploidy differences between large and small Barbus of Africa. Journal of Fish Biology 42: 445–455. https://doi.org/10.1111/j.1095-8649.1993.tb00347.x

Goodier S.A.M., Cotterill F.P.D., O’Ryan C., Skelton P.H. & de Wit M.J. 2011. Cryptic diversity of African Tigerfish (Genus Hydrocynus) reveals palaeogeographic signatures of linked Neogene geotectonic events. PLoS ONE 6: e28875. https://doi.org/10.1371/journal.pone.0028775

Hammer Ø., Harper D.A.T. & Ryan P.D. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4: 1–9.

Hebert P.D.N., Cywinska A., Ball S.L. & de Waard J.R. 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society B 270: 313–321. https://doi.org/10.1098/rspb.2002.2218

Ivanova N.V., Zemlak T.S., Hanner R.H. & Hebert P.D. 2007. Universal primer cocktails for fish DNA barcoding. Molecular Ecology Notes 7: 544–548. https://doi.org/10.1111/j.1471-8286.2007.01748.x

Koblmüller S., Egger B., Sturmbauer C. & Sefc K.M. 2010. Rapid radiation, ancient incomplete lineage sorting and ancient hybridization in the endemic Lake Tanganyika cichlid tribe Tropheini. Molecular Phylogenetics and Evolution 55: 318–334. https://doi.org/10.1016/j.ympev.2009.09.032

Lavoué S. & Sullivan J.P. 2014. Petrocephalus boboto and Petrocephalus arnegardi, two new species of African electric fish (Osteoglossomorpha, Mormyridae) from the Congo River basin. ZooKeys 400: 43–65. https://doi.org/10.3897/zookeys.400.6743

Lévêque C. & Daget J. 1984. Cyprinidae. In: Daget J., Gosse J.P. & Van den Audenaerde T.D. (eds) Check-list of the Freshwater Fishes of Africa (CLOFFA1): 217–342. ORSTOM & MRAC, Paris & Tervuren.

Lowenstein J.H., Osmundson T.Z., Becker S., Hanner R. & Stiassny M.L.J. 2011. Incorporating DNA barcodes into a multi-year inventory of the fishes of the hyperdiverse Lower Congo River, with a multi-gene performance assessment of the genus Labeo as a case study. Mitochondrial DNA 21: 1–19. https://doi.org/10.3109/19401736.2010.537748

Messing J. 1983. New M13 vectors for cloning. Methods in Enzymology 101: 20–78. https://doi.org/10.1016/0076-6879(83)01005-8

Oellermann L.K. & Skelton P.H. 1990. Hexaploidy in yellowfish species (Barbus, Pisces, Cyprinidae) from southern Africa. Journal of Fish Biology 37: 105–115. https://doi.org/10.1111/j.1095-8649.1990.tb05932.x

Olayemi A., Nicolas V., Hulselmans J.A.N., Missoup A.D., Fichet-Calvet E., Amundala D., Dudu A., Dierckx T., Wendelen W., Leirs H. & Verheyen E. 2012. Taxonomy of the African giant pouched rats (Nesomyidae: Cricetomys): molecular and craniometric evidence support an unexpected high species diversity. Zoological Journal of the Linnean Society 165: 700–719. https://doi.org/10.1111/j.1096-3642.2012.00823.x

Pereira L.H.G., Hanner R., Foresti F. & Oliveira C. 2013. Can DNA barcoding accurately discriminate megadiverse Neotropical freshwater fish fauna? BMC Genetics 14: 20. https://doi.org/10.1186/1471-2156-14-20

Pethiyagoda R., Meegaskumbura M. & Maduwage K. 2012. A synopsis of the South Asian fishes referred to Puntius (Pisces: Cyprinidae). Ichthyological Exploration of Freshwaters 23: 69–95.

Poll M. 1976. Exploration du Parc National de l’Upemba Mission G.F. de Witte, 73: Poissons. Fondation pour favoriser les recherches scientifiques en Afrique, Bruxelles.

Rab P., Machordom A., Perdices A. & Guegan J.F. 1995. Karyotypes of three «small» Barbus species (Cyprinidae) from Republic of Guinea (Western Africa) with a review on karyology of African small Barbus. Caryologia 48: 299–307. https://doi.org/10.1080/00087114.1995.10797339

Ren Q. & Mayden R.L. 2016. Molecular phylogeny and biogeography of African diploid barbs, ‘Barbus’, and allies in Africa and Asia (Teleostei: Cypriniformes). Zoologica Scripta 45 (6): 642–649. https://doi.org/10.1111/zsc.12177

Runge J. 2007. The Congo River, Central Africa. In: Gupta A. (ed.) Large Rivers: Geomorphology and Management: 293–309. John Wiley & Sons Ltd, West Sussex.

Schmidt R.C. & Bart Jr. H.L. 2015. Nomenclatural changes should not be based on equivocally supported phylogenies: Reply to Yang et al. 2015. Molecular Phylogenetics and Evolution 90: 193–194. https://doi.org/10.1016/j.ympev.2015.05.025

Snoeks J. 2004. The Cichlid Diversity of Lake Malawi/Nyassa/Niassa: Identification, Distribution and Taxonomy. Cichlid Press, Texas.

Snoeks J., Harrison I.J. & Stiassny M.L.J. 2011. The status and distribution of freshwater fishes. In: Darwall W., Smith K., Allen D., Holland R., Harrison I. & Brooks E. (eds) The Diversity of Life in African Freshwaters: Underwater, under Threat. An Analysis of the Status and Distribution of Freshwater Species throughout Mainland Africa: 42–91. IUCN, Gland & Cambridge.

Steinke D. & Hanner R. 2011. The FISH-BOL collaborators’ protocol. Mitochondrial DNA 22: 10–14. https://doi.org/10.3109/19401736.2010.536538

Stiassny M.L., Denton J.S. & Monsebula Iyaba R.J.C. 2013. A new ectoparasitic distichodontid of the genus Eugnathichthys (Characiformes: Citharinoidei) from the Congo basin of central Africa, with a molecular phylogeny for the genus. Zootaxa 3693: 479–490. https://doi.org/10.11646/zootaxa.3693.4.4

Swartz E.R., Skelton P.H. & Bloomer P. 2009. Phylogeny and biogeography of the genus Pseudobarbus (Cyprinidae): shedding light on the drainage history of rivers associated with the Cape Floristic Region. Molecular Phylogenetics and Evolution 51: 75–84. https://doi.org/10.1016/j.ympev.2008.10.017

Tamura K., Peterson D., Peterson N., Stecher G., Nei M. & Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731–2739. https://doi.org/10.1093/molbev/msr121

Tsigenopoulos C.S., Kasapidis P. & Berrebi P. 2010. Phylogenetic relationships of hexaploid large-sized barbs (genus Labeobarbus, Cyprinidae) based on mtDNA data. Molecular Phylogenetics and Evolution 56: 851–856. https://doi.org/10.1016/j.ympev.2010.02.006

Tweddle D. & Skelton P.H. 2008. New species of ‘Barbus’ and Labeobarbus (Teleostei: Cyprinidae) from the South Rukuru River, Malawi, Africa. Smithiana Publications in Aquatic Biodiversity, Bulletin 8: 25–39.

Yang L., Sado T., Hirt M.V., Pasco-Viel E., Arunachalam M., Li J., Wang X., Freyhof J., Saitoh K., Simons A.M., Miya M., He S. & Mayden R.L. 2015. Phylogeny and polyploidy: Resolving the classification of cyprinine fishes (Teleostei: Cypriniformes). Molecular Phylogenetics and Evolution 85: 97–116. https://doi.org/10.1016/j.ympev.2015.01.014

Published
2017-04-12
How to Cite
Van Ginneken, M., Decru, E., Verheyen, E., & Snoeks, J. (2017). Morphometry and DNA barcoding reveal cryptic diversity in the genus Enteromius (Cypriniformes: Cyprinidae) from the Congo basin, Africa. European Journal of Taxonomy, (310). https://doi.org/10.5852/ejt.2017.310
Issue
No. 310 (2017): Morphometry and DNA barcoding reveal cryptic diversity in the genus Enteromius (Cypriniformes: Cyprinidae) from the Congo basin, Africa
Section
Zoology
Copyright (c) 2017 Marjolein Van Ginneken, Eva Decru, Erik Verheyen, Jos Snoeks

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