Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-23T05:29:17.291Z Has data issue: false hasContentIssue false
  • English
  • Français

Schistosoma kisumuensis n. sp. (Digenea: Schistosomatidae) from murid rodents in the Lake Victoria Basin, Kenya and its phylogenetic position within the S. haematobium species group

Published online by Cambridge University Press:  02 July 2009

B. HANELT ,
S. V. BRANT ,
M. L. STEINAUER ,
G. M. MAINA ,
J. M. KINUTHIA ,
L. E. AGOLA ,
I. N. MWANGI ,
B. N. MUNGAI ,
M. W. MUTUKU  and
G. M. MKOJI
...Show all authors
B. HANELT*
Affiliation:
Department of Biology, University of New Mexico, MSC03 2020, Albuquerque, New Mexico, 87131-0001, USA
S. V. BRANT
Affiliation:
Department of Biology, University of New Mexico, MSC03 2020, Albuquerque, New Mexico, 87131-0001, USA
M. L. STEINAUER
Affiliation:
Department of Biology, University of New Mexico, MSC03 2020, Albuquerque, New Mexico, 87131-0001, USA
G. M. MAINA
Affiliation:
Centre for Biotechnology Research and Development, Kenya Medical Research Institute, Mbagathi Road, PO Box 54840-00200, City Square, Nairobi, Kenya
J. M. KINUTHIA
Affiliation:
Centre for Biotechnology Research and Development, Kenya Medical Research Institute, Mbagathi Road, PO Box 54840-00200, City Square, Nairobi, Kenya
L. E. AGOLA
Affiliation:
Centre for Biotechnology Research and Development, Kenya Medical Research Institute, Mbagathi Road, PO Box 54840-00200, City Square, Nairobi, Kenya
I. N. MWANGI
Affiliation:
Centre for Biotechnology Research and Development, Kenya Medical Research Institute, Mbagathi Road, PO Box 54840-00200, City Square, Nairobi, Kenya
B. N. MUNGAI
Affiliation:
Centre for Biotechnology Research and Development, Kenya Medical Research Institute, Mbagathi Road, PO Box 54840-00200, City Square, Nairobi, Kenya
M. W. MUTUKU
Affiliation:
Centre for Biotechnology Research and Development, Kenya Medical Research Institute, Mbagathi Road, PO Box 54840-00200, City Square, Nairobi, Kenya
G. M. MKOJI
Affiliation:
Centre for Biotechnology Research and Development, Kenya Medical Research Institute, Mbagathi Road, PO Box 54840-00200, City Square, Nairobi, Kenya
E. S. LOKER
Affiliation:
Department of Biology, University of New Mexico, MSC03 2020, Albuquerque, New Mexico, 87131-0001, USA
*
*Corresponding author: Department of Biology, University of New Mexico, MSC03 2020, Albuquerque, New Mexico, 87131-0001, USA. Tel: +505 2774589. Fax: +505 2770304. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Schistosoma kisumuensis n. sp. is described based on 6 adult males and 2 adult females collected from the circulatory system of 3 murid rodent species, Pelomys isseli, Mastomys natalensis, and Dasymys incomtus. Specimens were collected from a single location, Nyabera Swamp, in Kisumu, Kenya in the Lake Victoria Basin. This new species is morphologically similar to members of the S. haematobium group, currently represented by 8 species parasitizing artiodactyls and primates, including humans. Schistosoma kisumuensis differs from these species by producing relatively small Schistosoma intercalatum-like eggs (135·2×52·9 μm) with a relatively small length to width ratio (2·55). Comparison of approximately 3000-base-pair sequences of nuclear rDNA (partial 28S) and mtDNA (partial cox1, nad6, 12S) strongly supports the status of S. kisumuensis as a new species and as a sister species of S. intercalatum. The cox1 genetic distance between these two species (6·3%) is comparable to other pairwise comparisons within the S. haematobium group. Separation of the Congo River and Lake Victoria drainage basins is discussed as a possible factor favoring the origin of this species.

Keywords

DigeneaSchistosomatidaeSchistosomaSchistosoma kisumuensis n. sprodent parasiteKenya
Type
Research Article
Information
Parasitology , Volume 136 , Issue 9 , August 2009 , pp. 987 - 1001
Copyright
Copyright © Cambridge University Press 2009

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

Attwood, S. W., Panasoponkul, C., Upatham, E. S., Meng, X. H. and Southgate, V. R. (2002). Schistosoma ovuncatum n. sp. (Digenea: Schistosomatidae) from northwest Thailand and the historical biogeography of Southeast Asian Schistosoma Weinland, 1858. Systematic Parasitology 51, 1–19.Google Scholar
Brown, D. S. (1994). Freshwater Snails of Africa and their Medical Importance. 2nd Edn. Taylor & Francis, London.Google Scholar
Chesterman, C. C. (1923). Note sur la bilharziose dans la region de Stanleyville (Congo belge). Annales de la Societe Belge de Medecine Tropicale 3, 63–79.Google Scholar
De Bont, J. and Vercruysse, J. (1997). The epidemiology and control of cattle schistosomiasis. Parasitology Today 13, 255–262.Google Scholar
De Clercq, D. (1987). The malacological situation in Kinshasa and description of an autochthonous focus of schistosomiasis due to Schistosoma intercalatum. Annales de la Société Belge de Médecine Tropicale 67, 345–352.Google Scholar
de Heinzelin, J. (1962). Les formations du Western Rift et de la cuvette congolaise. Annales du Musée Royal de L'afrique Centrale 40, 219–243.Google Scholar
Farley, J. (1971). A review of the family Schistosomatidae: excluding the genus Schistosoma from mammals. Journal of Helminthology 45, 289–320.Google Scholar
Fisher, A. C. (1934). A study of the schistosomiasis of the Stanleyville district of the Belgian Congo. Transactions of the Royal Society of Tropical Medicine and Hygiene 18, 277–306.Google Scholar
Frandsen, F. (1977). Investigations of the unimiracidial infection of Schistosoma intercalatum in snails and the infection of the final host using cercariae of one sex. Journal of Helminthology 51, 5–10.Google Scholar
Huelsenbeck, J. P., Ronquist, F., Nielsen, R. and Bollback, J. P. (2001). Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294, 2310–2314.Google Scholar
Kane, R. A., Southgate, V. R., Rollinson, D., Littlewood, D. T., Lockyer, A. E., Pages, J. R., Tchuem Tchuente, L. A. and Jourdane, J. (2003). A phylogeny based on three mitochondrial genes supports the division of Schistosoma intercalatum into two separate species. Parasitology 127, 131–137.Google Scholar
Kumar, S., Tamura, K., Jakobsen, I. B. and Nei, M. (2001). MEGA2: Molecular Evolutionary Genetics Analysis Software. Arizona State University, Tempe, Arizona, USA.Google Scholar
Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J. and Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.Google Scholar
Lewis, F. (1998). Schistosomiasis. In Current Protocols in Immunology, Supplement 28, Animal Models for Infectious Diseases (ed. Coligan, J. E., Kruisbeek, A. M., Margulies, D. H., Shevach, E. M. and Strober, W.),pp. 19.11.11–19.11.28. John Wiley & Sons, Inc., New York, USA.Google Scholar
Li, L., Yu, L. Y., Zhu, X. Q., Wang, C. R., Zhai, Y. Q. and Zhao, J. P. (2008). Orientobilharzia turkestanicum is grouped within African schistosomes based on phylogenetic analyses using sequences of mitochondrial genes. Parasitology Research 102, 939–943.Google Scholar
Littlewood, D. T. and Johnston, D. A. (1995). Molecular phylogenetics of the four Schistosoma species groups determined with partial 28S ribosomal RNA gene sequences. Parasitology 111, 167–175.Google Scholar
Lockyer, A. E., Olson, P. D., Ostergaard, P., Rollinson, D., Johnston, D. A., Attwood, S. W., Southgate, V. R., Horak, P., Snyder, S. D., Le, T. H., Agatsuma, T., McManus, D. P., Carmichael, A. C., Naem, S. and Littlewood, D. T. (2003). The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126, 203–224.Google Scholar
Loker, E. S. (1983). A comparative study of the life-histories of mammalian schistosomes. Parasitology 87, 343–369.Google Scholar
Morgan, J. A., DeJong, R. J., Kazibwe, F., Mkoji, G. M. and Loker, E. S. (2003). A newly-identified lineage of Schistosoma. International Journal for Parasitology 33, 977–985.Google Scholar
Odongo-Aginya, E. I., Mueller, A., Loroni-Lakwo, T., Ndugwa, C. M., Southgate, V. R., Schweigmann, U., Seitz, H. M. and Doehring-Schwerdtfeger, E. (1994). Evidence for the occurrence of Schistosoma intercalatum at Albert Nile in northern Uganda. American Journal of Tropical Medicine and Hygiene 50, 723–726.Google Scholar
Pagès, J. R., Durand, P., Southgate, V. R., Tchuem Tchuente, L. A. and Jourdane, J. (2001). Molecular arguments for splitting of Schistosoma intercalatum, into two distinct species. Parasitolgy Research 87, 57–62.Google Scholar
Pagès, J. R., Jourdane, J., Southgate, V. R. and Tchuem Tchuente, L. A. (2003). Reconnaissance de deux espèces jumelles au sein du taxon Schistosoma intercalatum Fisher, 1934, agent de la schistosomose humaine rectale en frique. Description de Schistosoma guineensis n. sp. In Taxonomy, Ecology and Evolution of Metazoan Parasites (ed. Combes, C. and Jourdane, J.), pp. 139–146. Presses Universitaires de Perpignan, Perpignan, France.Google Scholar
Pickford, M., Senut, B. and Hadoto, D. (1993). Geology and palaeobiology of the Albertine Rift Valley Uganda-Zaire. Centre International pour la Formation et les Echanges Géologiques 1993/24, 1–180.Google Scholar
Pitchford, R. J. (1965). Differences in the egg morphology and certain biological characteristics of some African and Middle Eastern schistosomes, genus Schistosoma, with terminal-spined eggs. Bulletin of The World Health Organization 32, 105–120.Google Scholar
Pitchford, R. J. (1977). A check list of definitive hosts exhibiting evidence of the genus Schistosoma Weinland, 1858 acquired naturally in Africa and the Middle East. Journal of Helminthology 51, 229–252.Google Scholar
Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.Google Scholar
Pritchard, M. H. and Kruse, G. O. W. (1982). The Collection and Preservation of Animal Parasites. University of Nebraska Press, Lincoln, NB, USA.Google Scholar
Rollinson, D. and Southgate, V. R. (1987). The genus Schistosoma: a taxonomic appraisal. In The Biology of Schistosomes: from Genes to Latrines (ed. Rollinson, D. and Simpson, A. J. G.), pp. 1–49. Academic Press, London, UK.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.Google Scholar
Schwetz, J. (1956 a). Role of wild rats and domestic rats (Rattus rattus) in schistosomiasis in man. Transactions of the Royal Society of Tropical Medicine and Hygiene 50, 275–282.Google Scholar
Schwetz, J. (1956 b). Some new comparative investigations on three Physopsis borne schistosomes: Schistosoma haematobium, S. bovis and S. intercalatum. American Journal of Tropical Medicine and Hygiene 5, 1021–1085.Google Scholar
Snyder, S. D. (2004). Phylogeny and paraphyly among tetrapod blood flukes (Digenea: Schistosomatidae and Spirorchiidae). International Journal for Parasitology 34, 1385–1392.Google Scholar
Snyder, S. D. and Loker, E. S. (2000). Evolutionary relationships among the Schistosomatidae (Platyhelminthes: Digenea) and an Asian origin for Schistosoma. Journal of Parasitology 86, 283–288.Google Scholar
Steinauer, M., Mwangi, I., Maina, G., Kinuthia, J., Mutuku, M., Agola, E., Mungai, B., Mkoji, G. and Loker, E. S. (2008 a). Interactions between natural populations of human and rodent schistosomes in the Lake Victoria region of Kenya: A molecular epidemiological approach. PLoS Neglected Tropical Diseases 16, 1–11.Google Scholar
Steinauer, M. L., Agola, L. E., Mwangi, I. N., Mkoji, G. M. and Loker, E. S. (2008 b). Molecular epidemiology of Schistosoma mansoni: a robust, high-throughput method to assess multiple microsatellite markers from individual miracidia. Infection, Genetics and Evolution 8, 68–73.Google Scholar
Steinmann, P., Keiser, J., Bos, R., Tanner, M. and Utzinger, J. (2006). Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. The Lancet Infectious Diseases 6, 411–425.Google Scholar
Swofford, D. (2002). PAUP*. Phylogenetic Analysis Using Parsimony (*and other Methods), Version 4.0b10 (Alvitec). Sinauer Associates, Sunderland, MA, USA.Google Scholar
Tchuem Tchuente, L. A., Southgate, V. R., Jourdane, J., Webster, B. L. and Vercruysse, J. (2003). Schistosoma intercalatum: an endangered species in Cameroon? Trends in Parasitology 19, 389–393.Google Scholar
Tchuem Tchuente, L. A., Southgate, V. R., Vercruysse, J., Kaukas, A., Kane, R., Mulumba, M. P., Pages, J. R. and Jourdane, J. (1997). Epidemiological and genetic observations on human schistosomiasis in Kinshasa, Zaire. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 263–269.Google Scholar
Truett, G. E., Heeger, P., Mynatt, R. L., Truett, A. A., Walker, J. A. and Warman, M. L. (2000). Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). BioTechniques 29, 52–54.Google Scholar
Van Damme, D. and Pickford, M. (1999). The late Cenozoic Viviparidae (Mollusca, Gastropoda) of the Albertine Rift Valley (Uganda–Congo). Hydrobiologia 390, 171–217.Google Scholar
Wang, C. R., Li, L., Ni, H. B., Zhai, Y. Q., Chen, A. H., Chen, J. and Zhu, X. Q. (2009). Orientobilharzia turkestanicum is a member of Schistosoma genus based on phylogenetic analysis using ribosomal DNA sequences. Experimental Parasitology 121, 193–197.Google Scholar
Webster, B. L., Southgate, V. R. and Littlewood, D. T. (2006). A revision of the interrelationships of Schistosoma including the recently described Schistosoma guineensis. International Journal for Parasitology 36, 947–955.Google Scholar
Wright, C. A., Southgate, V. R. and Knowles, R. J. (1972). What is Schistosoma intercalatum Fisher, 1934? Transactions of the Royal Society of Tropical Medicine and Hygiene 66, 28–56.Google Scholar
Wright, C. A., Southgate, V. R. and Ross, G. C. (1979). Enzymes in Schistosoma intercalatum and the relative status of the Lower Guinea and Zaire strains of the parasite. International Journal for Parasitology 9, 523–528.Google Scholar