Advertisement

Parasitology Research

, Volume 107, Issue 6, pp 1405–1413 | Cite as

Molecular phylogeny of monogeneans parasitizing African freshwater Cichlidae inferred from LSU rDNA sequences

  • Monika Mendlová
  • Antoine Pariselle
  • Martina Vyskočilová
  • Andrea Šimková
Original Paper

Abstract

The African freshwater fish of Cichlidae are parasitized by five genera of monogeneans belonging to Dactylogyridea. Ectoparasitic Scutogyrus, Onchobdella, and the highly diversified Cichlidogyrus represent three genera located on the gills, while the endoparasitic Enterogyrus and Urogyrus are located in the stomach and the urinary bladder, respectively. Representatives of four dactylogyridean genera (except for Urogyrus) were collected from seven cichlid species in West Africa. The aim of this study was to investigate the phylogenetic relationships between ectoparasitic and endoparasitic dactylogyridaen monogeneans specific to African freshwater Cichlidae and other representatives of Dactylogyridae, including a wide range of species from both freshwater and marine environments. All phylogenetic analyses point to the polyphyletic origin of the subfamily Ancyrocephalinae. Both Enterogyrus and Onchobdella were found to be monophyletic. The phylogenetic position of Scutogyrus longicornis was placed within the Cichlidogyrus species, which suggests the non-monophyly of Cichlidogyrus. Therefore, we have proposed a taxonomical revision of the species recently considered to be Scutogyrus. However, these four dactylogyridean genera-specific to cichlids do not form a monophyletic group. Using LSU rDNA analyses, we found that Enterogyrus and Onchobdella form a clade with Protogyrodactylus, i.e., the parasite species does not live in cichlids, which suggests that endoparasitism in cichlid monogeneans is not an ancestral feature.

Keywords

Maximum Parsimony Neighbor Join Cichlid Fish Male Copulatory Organ Bayesian Inference Analysis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This study was supported by Research Project of Masaryk University (No. MSM 0021622416). The field work was partially funded by Ichthyoparasitology Research Centre of the Ministry of Education, Youth, and Sports of the Czech Republic LC 522. We would like to thank Martina Davidová, Naďa Musilová, Eva Řehulková, and Radim Blažek from the Laboratory of Parasitology, Faculty of Science, Masaryk University, Brno, for field assistance with fish dissection. We are very grateful to Gregor Speas for the English revision for the final version.

References

  1. Bilong-Bilong CF (1988) Enterogyrus malmbergi n. sp. (Monogenea - Ancyrocephalidae) parasite de l´estomac du Cichlidae Tilapia nilotica Linne, 1757 au Sud - Cameroun. Ann Fac Sc Bio Biochim 3:51–58Google Scholar
  2. Bilong-Bilong CF, Euzet L (1995) Onchobdella bopeleti n. sp. (Monogenea, Ancyrocephalidae) parasite branchial de Hemichromis fasciatus (Peters, 1857) (Cichlidae). J Afr Zool 109:253–258Google Scholar
  3. Bilong-Bilong CF, Birgi E, Lambert A (1989) Enterogyrus melenensis n. sp. (Monogenea, Ancyrocephalidae), parasite stomacal de Hemichromis fasciatus Peters, 1857 (Téléosteén, Cichlidae) du Sud-Cameroun. Rev Zool Afr 103:99–105Google Scholar
  4. Bilong-Bilong CF, Birgi E, Euzet L (1991) Enterogyrus barombiensis n. sp. (Monogenea, Ancyrocephalidae) parasite stomacal de trois Cichlidae endémiques du lac du cratére Barombi Mbo (Cameroun). Ann Parasitol Hum Comp 66:105–108Google Scholar
  5. Bilong-Bilong CF, Birgi E, Euzet L (1994) Urogyrus cichlidarium gen. nov., Urogyridae fam. nov., monogéne parasite de la vessie urinaire de poisson cichlidés au Cameroun. Can J Zool 72:561–566CrossRefGoogle Scholar
  6. Bilong-Bilong CF, Euzet L, Birgi E (1996) Monogenean stomach parasites of cichlid fishes from Cameroon: two new species of the genus Enterogyrus Paperna, 1963 (Ancyrocephalidae). Syst Parasitol 34:37–42CrossRefGoogle Scholar
  7. Bychowsky BE, Nagibina LF (1978) Revision of Ancyrocephalinae Bychowsky, 1937. Parazitol Sbornik 28:5–15Google Scholar
  8. Dossou C (1982) Parasites de poissons d´eau douce du Bénin III. Espéces nouvelles du genre Cichlidogyrus (Monogenea) parasites de Cichlidae. Bull de l´IFAN 44:295–322Google Scholar
  9. Dossou C, Birgi E (1984) Monogénes parasites d´Hemichromis fasciatus Peters, 1857 (Teleostei, Cichlidae). Ann Sci Nat Zool 6:101–109Google Scholar
  10. Douëllou L (1993) Monogeneans of the genus Cichlidogyrus Paperna, 1960 (Dactylogyridae: Ancyrocephalinae) from cichlid fishes of Lake Kariba (Zimbabwe) with descriptions of five new species. Syst Parasitol 25:159–186CrossRefGoogle Scholar
  11. Eid N, Negm M (1987) Some morphological study on a new species of endoparasitic monogenetic trematode Enterogyrus niloticus in the intestine of Tilapia nilotica. J Egypt Vet Med Assoc 47:79–86Google Scholar
  12. Ergens R (1981) Nine species of the genus Cichlidogyrus Paperna, 1960 (Monogenea: Ancyrocephalinae) from Egyptian fishes. Folia Parasitol 28:205–214Google Scholar
  13. Ergens R, Lom J (1970) Causative agents of fish diseases. Academia Praha, Prague (In Czech)Google Scholar
  14. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  15. Fischthal JH, Allison LN (1940) Acolpenteron ureteroecetes n. g., n. sp., a monogenetic trematode from the ureters of black basses. J Parasitol 26:34–35Google Scholar
  16. Gibson DI, Timofeeva TA, Gerasev PI (1996) A catalogue of the nominal species of the monogeneans genus Dactylogyrus Diesing, 1850 and their host genera. Syst Parasitol 35:3–48CrossRefGoogle Scholar
  17. Gussev AV, Fernando CH (1978) Dactylogyridae (Monogenoidea) from the stomach of fishes. Folia Parasitol 20:207–212Google Scholar
  18. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids S 41:95–98Google Scholar
  19. Hassouna N, Michot B, Bachellerie JP (1984) The complete nucleotide sequence of mouse 28S rRNA gene. Implications for the process of size increase of the large subunit rRNA in higher eukaryotes. Nucleic Acids Res 12:3563–3583CrossRefPubMedGoogle Scholar
  20. Kohn A (1990) Kritskyia moraveci n. g., n. sp. (Monogenea, Dactylogyridae) from the urinary bladder and ureters of Rhamidia quelen (Quoy and Gaimard, 1824) (Pisces, Pimelodidae) in Brazil. Syst Parasitol 17:81–85CrossRefGoogle Scholar
  21. Kritsky DC, Boeger WA (1989) The phylogenetic status of Ancyrocephalidae Bychowsky, 1937 (Monogenea: Dactylogyroidea). J Parasitol 75:207–211CrossRefPubMedGoogle Scholar
  22. Malmberg G (1957) On the occurence of Gyrodactylus on Swedish fishes. Skr Söd Sver Fiskför Asskr 1956:19–76 (in Swedish)Google Scholar
  23. Murray AM (2001) The fossil record and biogeography of the Cichlidae (Actinopterygii: Labroidei). Biol J Linn Soc 78:517–532CrossRefGoogle Scholar
  24. Paperna I (1963) Enterogyrus cichlidarium n. gen. n. sp., a monogenetic trematode parasitic in the intestine of a fish. Bull Res Counc Isr 11:183–187Google Scholar
  25. Paperna I (1968a) Monogenetic trematodes collected from freshwater fish in Ghana. Second report. Bull Fish Cult Israel 20:88–99Google Scholar
  26. Paperna I (1968b) Onchobdella n. gen. New genus of monogenetic trematodes (Dasctylogyridae, Bychowski 1933) from cichlid fish from West Africa. Proc Helminthol Soc Wash 35:200–206Google Scholar
  27. Paperna I, Thurston JP (1969) Monogenetic trematodes collected from cichlid fish in Uganda; including the description of five new species of Cichlidogyrus. Rev Zool Bot Afr 79:15–33Google Scholar
  28. Pariselle A, Euzet L (1994) Three new species of Cichlidogyrus Paperna, 1960 (Monogenea, Ancyrocephalidae) parasitic on Tylochromis jentinki (Steindachner, 1895) (Pisces, Cichlidae) in West Africa. Syst Parasitol 29:229–234Google Scholar
  29. Pariselle A, Euzet L (1995) Scutogyrus gen. n. (Monogenea: Ancyrocephalidae) for Cichlidogyrus longicornis minus Dossou, 1982, C. l. longicornis, and C. l. gravivaginus Paperna and Thurston, 1969, with description of three new species parasitic on African cichlids. J Helminthol Soc Wash 62:157–173Google Scholar
  30. Pariselle A, Euzet L (1996) Cichlidogyrus Paperna, 1960 (Monogenea, Ancyrocephalidae): gill parasites from West African Cichlidae of the subgenus Coptodon Regan, 1920 (Pisces), with description of six new species. Syst Parasitol 34:109–124CrossRefGoogle Scholar
  31. Pariselle A, Euzet L (2009) Systematic revision of dactylogyridean parasites (Monogenea) from cichlid fishes in Africa, the Levant and Madagascar. Zoosystema 31:849–898Google Scholar
  32. Pariselle A, Lambert A, Euzet L (1991) A new haptor in mesoparasitic monogeneans of the genus Enterogyrus Paperna, 1963, with a description of Enterogyrus foratus n. sp., stomach parasites of cichlids in West Africa. Syst Parasitol 20:211–220CrossRefGoogle Scholar
  33. Pariselle A, Bilong-Bilong CF, Euzet L (2003) Four new species of Cichlidogyrus Paperna, 1960 (Monogenea, Ancyrocephalidae), a gill parasites from African mouthbreeder tilapias of the genera Sarotherodon and Oreochromis (Pisces, Cichlidae), with a redescription of C. thurstonae Ergens, 1981. Syst Parasitol 56:201–210. doi: 10.1023/B:SYPA.0000003807.27452 CrossRefPubMedGoogle Scholar
  34. Plaisance L, Littlewood DTJ, Olson PD, Morand S (2005) Molecular phylogeny of gill monogeneans (Platyhelminthes, Monogenea, Dactylogyridae) and colonization of Indo-West pacific butterflyfish hosts (Perciformes, Chaedontidae). Zool Scr 34:425–436. doi: 10.1111/j.1463-6409.2005.00191 CrossRefGoogle Scholar
  35. Posada D, Crandal AK (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  36. Poulin R (2002) The evolution of monogenean diversity. Int J Parasitol 32:245–254CrossRefPubMedGoogle Scholar
  37. Pouyaud L, Desmarais E, Deveney M, Pariselle A (2006) Phylogenetic relationships among monogenean gill parasites (Dactylogyridea, Ancyrocephalidae) infesting tilapiine hosts (Cichlidae): systematic and evolutionary implications. Mol Phylogenet Evol 38:241–249. doi: 10.1016/j.ympev.2005.08.013 CrossRefPubMedGoogle Scholar
  38. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi: 10.1093/bioinformatics/btg180 CrossRefPubMedGoogle Scholar
  39. Šimková A, Plaisance L, Matějusová I, Morand S, Verneau O (2003) Phylogenetic relationships of the Dactylogyridae Bychowsky, 1933 (Monogenea: Dactylogyridea): the need for the systematic revision of the Ancyrocephalinae Bychowsky, 1937. Syst Parasitol 54:1–11. doi: 10.1017/S0031182006009942 CrossRefPubMedGoogle Scholar
  40. Šimková A, Matějusová I, Cunningham CO (2006) A molecular phylogeny of the Dactylogyridae sensu Kritsky & Boeger (1989) (Monogenea) based on the D1−D3 domains of large subunit rDNA. Parasitology 132:43–53. doi: 10.1017/S0031182006009942 CrossRefGoogle Scholar
  41. Swofford DL (2002) PAUP* Phylogenetic Analysis using Parsimony and other Methods. Version 4.0b10. Sinauer, SunderlandGoogle Scholar
  42. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefPubMedGoogle Scholar
  43. Timofeeva TA, Gerasev PI, Gibbon DI (1997) A catalogue of the nominal species of the monogenean family Dactylogyridae Bychowsky, 1933 (excluding Dactylogyrus Diesing, 1850). Syst Parasitol 38:153–158CrossRefGoogle Scholar
  44. Viozzi GP, Gutiérrez PA (2001) Philureter trigoniopsis, a new genus and species (Dactylogyridae, Ancyrocephalinae) from the ureters and urinary bladder of Glaxias maculatus (Osmeriformes: Galaxiidae) in Patagonia (Argentina). J Parasitol 97:392–394Google Scholar
  45. Wu XY, Zhu XQ, Xie MQ, Li AX (2007) The evaluation for generic-level monophyly of Ancyrocephalinae (Monogenea, Dactylogyridae) using ribosomal DNA sequence data. Mol Phylogenet Evol 44:530–544. doi: 10.1016/j.ympev.2007.03.025 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Monika Mendlová
    • 1
  • Antoine Pariselle
    • 2
  • Martina Vyskočilová
    • 1
  • Andrea Šimková
    • 1
  1. 1.Department of Botany and Zoology, Faculty of ScienceMasaryk UniversityBrnoCzech Republic
  2. 2.IRD (ex ORSTOM), UR 203/UMR 5554, ISE-MUniversité Montpellier II - CC 065Montpellier Cedex 5France

Personalised recommendations