Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-19T23:11:41.977Z Has data issue: false hasContentIssue false

Parasite hybridization in African Macrogyrodactylus spp. (Monogenea, Platyhelminthes) signals historical host distribution

Published online by Cambridge University Press:  06 May 2010

MAXWELL BARSON
Affiliation:
Laboratory of Animal Diversity and Systematics, Department of Biology, Katholieke Universiteit Leuven, Ch. Debériotstraat 32, B-3000Leuven, Belgium Department of Biological Sciences, University of Zimbabwe, PO Box MP167, Mt. Pleasant, Harare, Zimbabwe
IVA PŘIKRYLOVÁ
Affiliation:
Department of Botany and Zoology, Masaryk University, Kotlarska 2, 611 37Brno, Czech Republic
MAARTEN P. M. VANHOVE
Affiliation:
Laboratory of Animal Diversity and Systematics, Department of Biology, Katholieke Universiteit Leuven, Ch. Debériotstraat 32, B-3000Leuven, Belgium Department of African Zoology, Royal Museum for Central Africa, Leuvensesteenweg 13, B-3080Tervuren, Belgium
TINE HUYSE*
Affiliation:
Laboratory of Animal Diversity and Systematics, Department of Biology, Katholieke Universiteit Leuven, Ch. Debériotstraat 32, B-3000Leuven, Belgium
*
*Corresponding author: Tine Huyse, Laboratory of Animal Diversity and Systematics, Department of Biology, Katholieke Universiteit Leuven, Ch. Deberiotstraat 32, B-3000Leuven, Belgium. Tel: +32 16 323966. Fax: +32 16 324575. E-mail: [email protected]

Summary

Macrogyrodactylus spp. from the gills of Clarias gariepinus in Zimbabwe and Kenya, and C. anguillaris in Senegal were identified using haptoral sclerite morphology and by sequencing the nuclear ribosomal DNA internal transcribed spacers (ITS) 1 and 2, partial 18S and the complete 5·8S rRNA gene. A molecular phylogeny was constructed using all sequenced Macrogyrodactylus species to date. Based on morphology, Macrogyrodactylus congolensis, M. heterobranchii, M. clarii, and M. karibae were identified, with one specimen from Zimbabwe displaying morphological features that were intermediate between M. heterobranchii and M. clarii. In the intermediate form, the partial 18S and ITS1 sequence was identical to that of M. clarii while the remaining ITS1 and complete ITS2 region was almost identical to M. heterobranchii as was the partial cox1 fragment, thus strongly suggesting a hybrid origin. At present, the catfish host of M. heterobranchii and M. clarii do not co-occur in southern Zimbabwe; this hybridization event is therefore proof of historical sympatry of both fish species.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Agnèse, J.-F. and Teugels, G. G. (2005). Insight into the phylogeny of African Clariidae (Teleostei, Siluriformes): implications for their body shape evolution, biogeography and taxonomy. Molecular Phylogenetics and Evolution 36, 546553.Google Scholar
Agnèse, J. F., Teugels, G. G., Galbusera, P., Guyomard, R. and Volckaert, F. (1997). Morphometric and genetic characterization of sympatric populations of Clarias gariepinus and C. anguillaris from Senegal. Journal of Fish Biology 50, 11431157.Google Scholar
Arafa, S. Z., El-Naggar, M. M. and El-Abbassy, S. A. (2009). Mode of attachment and histopathological effects of Macrogyrodactylus clarii, a monogenean parasite of the catfish Clarias gariepinus, with a report on host response. Acta Parasitologica 54, 103112.Google Scholar
Avise, J. C. (1994). Molecular Markers, Natural History and Evolution. Chapman and Hall, New York, USA.CrossRefGoogle Scholar
Barson, M., Bray, R. A., Ollevier, F. and Huyse, T. (2008). Taxonomy and faunistics of the helminth parasites of Clarias gariepinus (Burchell, 1822), and Oreochromis mossambicus (Peters, 1852) from temporary pans and pools of the Save River floodplain, Zimbabwe. Comparative Parasitology 75, 228240.Google Scholar
Bell-Cross, G. (1965). Movement of fish across the Congo-Zambezi watershed in the Mwinilunga District of Northern Rhodesia. In Proceedings of the Central African Scientific and Medical Congress, Lusaka, Northern Rhodesia (ed. Snowball, G. J.), p. 415424. Pergamon Press, Oxford, UK.Google Scholar
Bush, A. O., Fernández, J. C., Esch, G. W. and Seed, J. R. (2001). Parasitism. The Diversity and Ecology of Animal Parasites. Cambridge University Press, Cambridge, UK.Google Scholar
Combes, C. (2001). Parasitism. The Ecology and Evolution of Intimate Interactions. University of Chicago Press, Chicago, IL, USA.Google Scholar
Douëllou, L. and Chishawa, A. M. M. (1995). Monogeneans of three siluriform fish species in Lake Kariba, Zimbabwe. Journal of African Zoology 109, 99–115.Google Scholar
Fuertes Aguilar, J., Rosselló, J. A. and Nieto Feliner, G. (1999). Nuclear ribosomal DNA (nrDNA) concerted evolution in natural and artificial hybrids of Armeria (Plumbaginaceae). Molecular Ecology 8, 13411346.Google Scholar
Giddelo, C. S., Arndt, A. D. and Volckaert, F. A. M. (2002). Impact of rifting and hydrography on the genetic structure of Clarias gariepinus in eastern Africa. Journal of Fish Biology 60, 12521266.CrossRefGoogle Scholar
Goudie, A. S. (2005). The drainage of Africa since the Cretaceous. Geomorphology 67, 437456.Google Scholar
Hewitt, G. M. (2004). The structure of biodiversity – insights from molecular phylogeography. Frontiers in Zoology 1, 116. doi:10.1186/1742-9994-1-4.CrossRefGoogle ScholarPubMed
Huyse, T., Webster, B. L., Geldof, S., Stothard, R. J., Diaw, O. T., Polman, K. and Rollinson, D. (2009). Bidirectional introgressive hybridization between a cattle and human schistosome species. PLOS Pathogens 5, e100057.CrossRefGoogle ScholarPubMed
Jansen, G., Devaere, S., Weekers, P. H. H. and Adriaens, D. (2006). Phylogenetic relationships and divergence time estimate of African anguilliform catfish (Siluriformes: Clariidae) inferred from ribosomal gene and spacer sequences. Molecular Phylogenetics and Evolution 38, 6578.CrossRefGoogle ScholarPubMed
Kearn, G. C. (1998). Parasitism and the Platyhelminths. Chapman and Hall, London, UK.Google Scholar
Khalil, L. F. and Mashego, S. N. (1998). The African monogenean gyrodactylid genus Macrogyrodactylus Malmberg, 1957, and the reporting of three species of the genus in Clarias gariepinus in South Africa. Onderstepoort Journal of Veterinary Research 65, 223231.Google Scholar
Khalil, L. F. and Polling, L. (1997). Checklist of the Helminth Parasites of African Freshwater Fishes. University of Limpopo, Sovenga, South Africa.Google Scholar
Kimura, M. (1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111120.Google Scholar
Klassen, G. J. and Beverly-Burton, M. (1988). North American freshwater ancyrocephalids (Monogenea) with articulating haptoral bars: Host-parasite coevolution. Systematic Zoology 37, 179189.CrossRefGoogle Scholar
Le Brun, N., Renaud, F., Berrebi, P. and Lambert, A. (1992). Hybrid zones and host-parasite relationships: Effect on the evolution of parasitic specificity. Evolution 46, 5661.CrossRefGoogle Scholar
Maddison, W. P. and Maddison, D. R. (2008). MacClade: Analysis of Phylogeny and Character Evolution. Version 4.0. Sinauer Associates, Sunderland, MA, USA.Google Scholar
Malmberg, G. (1998). On the evolution within the family Gyrodactylidae (Monogenea). International Journal for Parasitology 28, 16251635.CrossRefGoogle ScholarPubMed
Marshall, B. E. (1999). The fishes of Zimbabwe. A century of change. Zimbabwe Science News 33, 4552.Google Scholar
Matějusová, I., Gelnar, M., McBeath, A. J. A., Collins, C. M. and Cunningham, C. O. (2001). Molecular markers for gyrodactylids (Gyrodactylidae: Monogenea) from five fish families (Teleostei). International Journal for Parasitology 31, 738745.Google Scholar
Matějusová, I., Gelnar, M., Verneau, O., Cunningham, C. O. and Littlewood, D. T. J. (2003). Molecular phylogenetic analysis of the genus Gyrodactylus (Platyhelminthes: Monogenea) inferred from rDNA ITS region: subgenera versus species groups. Parasitology 127, 603611.Google Scholar
Mayr, E. (1963). Animal Species and Evolution. Belknap Press of Harvard University Press, Cambridge, MA, USA.Google Scholar
Moore, A. E., Cotteril, F. P. D., Broderick, T. and Plowes, D. (2009). Landscape evolution in Zimbabwe from the Permian to present, with implications for kimberlite prospecting. South African Journal of Geology 112, 6588.Google Scholar
N'Douba, V. and Lambert, A. (1999). A new Macrogyrodactylus (Monogenea, Gyrodactylidae) parasite of Heterobranchus longifilis Valenciennes, 1840 (Teleostei, Siluriformes) in Cote d'Ivoire. Zoosystema 21, 7–11. (In French.)Google Scholar
Paperna, I. (1979). Monogenea of inland water fish in Africa. Musee Royal de L'Afrique Centrale, Annales, Serie 8 (Zoology) 226, 1131.Google Scholar
Paperna, I. (1996). Parasites, Infections and Diseases of Fishes in Africa: an Update. CIFA Technical Paper 3l. Food and Agriculture Organization, Rome, Italy.Google Scholar
Pariselle, A. and Euzet, L. (1998). Five new species of Cichlidogyrus (Monogenea: Ancyrocephalidae) from Tilapia brevimanus, T. buttikoferi and T. cessiana from Guinea, Ivory Coast and Sierra Leone (West Africa). Folia Parasitologica 45, 275282.Google Scholar
Pariselle, A. and Euzet, L. (2003). Four new species of Cichlidogyrus (Monogenea: Ancyrocephalidae), gill parasites of Tilapia cabrae (Teleostei: Cichlidae), with discussion on relative length of haptoral sclerites. Folia Parasitologica 50, 195201.Google Scholar
Posada, D. and Crandall, K. A. (1998). ModelTest: Testing the model of DNA substitution. Bioinformatics 14, 817818.Google Scholar
Pouyaud, L., Desmarais, E., Deveney, M. and Pariselle, A. (2006). Phylogenetic relationships among monogenean gill parasites (Dactylogyridae, Ancyrocephalidae) infesting tilapiine hosts (Cichlidae): Systematic and evolutionary implications. Molecular Phylogenetics and Evolution 38, 241249.Google Scholar
Přikrylová, I. and Gelnar, M. (2008). The first record of Macrogyrodactylus species (Monogenea, Gyrodactylidae) on freshwater fishes in Senegal with the description of Macrogyrodactylus simentiensis sp. nov., a parasite of Polypterus senegalus Cuvier. Acta Parasitologica 53, 18.CrossRefGoogle Scholar
Rognon, X., Teugels, G. G., Guyomard, R., Galbusera, Q. P., Andriamanga, M., Volckaert, F. and Agnèse, J. F. (1998). Morphometric and allozyme variation in the African catfishes Clarias gariepinus and C. anguillaris. Journal of Fish Biology 53, 192207.Google Scholar
Sang, T., Crawford, D. J. and Stuessy, T. F. (1995). Documentation of reticulate evolution in peonies (Paeonia) using internal transcribed spacer sequences of nuclear ribosomal DNA: Implications for biogeography and concerted evolution. Proceedings of the National Academy of Sciences, USA 92, 68136817.Google Scholar
Shamsi, S., Norman, R., Gasser, R. and Beveridge, I. (2009). Genetic and morphological evidences for the existence of sibling species within Contracaecum rudolphii (Hartwich, 1964) (Nematoda: Anisakidae) in Australia. Parasitology Research 105, 529538.Google Scholar
Šimková, A. S. and Morand, S. (2008). Co-evolutionary patterns in congeneric monogeneans: a review of Dactylogyrus species and their cyprinid hosts. Journal of Fish Biology 73, 22102227.CrossRefGoogle Scholar
Sinnappah, N. D., Lim, L. H. S., Rohde, K., Tinsley, R., Combes, C. and Verneau, O. (2001). A paedomorphic parasite associated with a neotenic amphibian host: phylogenetic evidence suggests a revised systematic position for Sphyranuridae within anuran and turtle polystomatoineans. Molecular Phylogenetics and Evolution 18, 189201.CrossRefGoogle ScholarPubMed
Skelton, P. H. (1994). Diversity and distribution of freshwater fishes in East and Southern Africa. Annales – Musee Royal de l'Afrique Centrale. Sciences Zoologiques (Belgium) 275, 6591.Google Scholar
Stankiewicz, J. and de Wit, M. J. (2006). A proposed drainage evolution model for Central Africa – Did the Congo flow east? Journal of African Earth Sciences 44, 7584.CrossRefGoogle Scholar
Swofford, D. L. (2003). PAUP*: Phylogenetic Analysis using Parsimony (*and other Methods). Version 4. Sinauer Associates, Sunderland, MA, USA.Google Scholar
Tamura, K. D., Nei, J. M. and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 15961599.Google Scholar
Trapani, J. (2008). Quartenary fossil fish from the Kibish Formation, Omo Valley, Ethiopia. Journal of Human Evolution 55, 521530.CrossRefGoogle Scholar
Trauth, M. H., Larrasoan, J. C. and Mudelsee, M. (2009). Trends, rhythms and events in Plio-Pleistocene African climate. Quaternary Science Reviews 28, 399411.Google Scholar
Waters, E. R. and Schaal, B. A. (1996). Biased gene conversion is not occurring among rDNA repeats in the Brassica triangle. Genome 39, 150154.Google Scholar