Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-18T19:43:51.907Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular epidemiology and phylogeography of Schistosoma mansoni around Lake Victoria

Published online by Cambridge University Press:  21 June 2010

C. J. STANDLEY ,
N. B. KABATEREINE ,
C. N. LANGE ,
N. J. S. LWAMBO  and
J. R. STOTHARD
C. J. STANDLEY*
Affiliation:
Institute of Genetics, School of Biology, University of Nottingham, Nottingham NG7 2RD, UK Biomedical Parasitology Division, Department of Zoology, Natural History museum, Cromwell Road, London SW7 5BD, UK
N. B. KABATEREINE
Affiliation:
Vector Control Division, Ministry of Health, Kampala, Uganda
C. N. LANGE
Affiliation:
Invertebrate Zoology Section, Nairobi National Museum, Museum Hill, P.O. Box 40658, Nairobi, Kenya
N. J. S. LWAMBO
Affiliation:
National Institute for medical Research, Mwanza, Tanzania
J. R. STOTHARD
Affiliation:
Biomedical Parasitology Division, Department of Zoology, Natural History museum, Cromwell Road, London SW7 5BD, UK
*
*Corresponding author: Institute of Genetics, School of Biology, University of Nottingham, Nottingham NG7 2RD, UK. Tel: +0207 942 5566. Fax: +0207 942 5054. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Intestinal schistosomiasis continues to be a major public health problem in sub-Saharan Africa, and is endemic in communities around Lake Victoria. Interest is growing in the molecular evolution and population genetic structure of Schistosoma mansoni and we describe a detailed analysis of the molecular epidemiology and phylogeography of S. mansoni from Lake Victoria. In total, 388 cytochrome oxidase 1 (COI) sequences were obtained from 25 sites along the Ugandan, Tanzanian and Kenyan shorelines of Lake Victoria, and 122 unique barcodes were identified; 9 corresponded to previously discovered barcodes from Lakes Victoria and Albert. A subset of the data, composed of COI sequences from miracidia from 10 individual children, was used for population genetics analyses; these results were corroborated by microsatellite analysis of 4 isolates of lab-passaged adult worms. Overall, 12 barcodes were found to be shared across all 3 countries, whereas the majority occurred singly and were locally restricted. The population genetics analyses were in agreement in revealing high diversity at the level of the human host and negligible population structuring by location. The lack of correlation between genetic distance and geographical distance in these data may be attributed to the confounding influence of high intra-individual diversity as well as human migration between communities.

Keywords

Schistosoma mansonibarcodingmicrosatellitesevolutiondisease control
Type
Research Article
Information
Parasitology , Volume 137 , Issue 13 , November 2010 , pp. 1937 - 1949
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

Agola, L. E., Mburu, D. N., DeJong, R. J., Mungai, B. N., Muluvi, G. M., Njagi, E. N. M., Loker, E. S. and Mkoji, G. M. (2006). Microsatellite typing reveals strong genetic structure of Schistosoma mansoni from localities in Kenya. Infection, Genetics and Evolution 6, 484–490.CrossRefGoogle ScholarPubMed
Balen, J., Stothard, J. R., Kabatereine, N. B., Tukahebwa, E. M., Kazibwe, F., Whawell, S., Webster, J. P., Utzinger, J. and Fenwick, A. (2006). Morbidity due to Schistosoma mansoni: an epidemiological assessment of distended abdomen syndrome in Ugandan school children with observations before and 1-year after anthelminthic chemotherapy. Transactions of the Royal Society of Tropical Medicine and Hygiene 100, 1039–1048.CrossRefGoogle ScholarPubMed
Blair, L., Webster, J. P. and Barker, G. C. (2001). Isolation and characterization of polymorphic microsatellite markers in Schistosoma mansoni from Africa. Molecular Ecology Notes 1, 93–95.CrossRefGoogle Scholar
Brooker, S., Kabatereine, N. B., Gyapong, J. O., Stothard, J. R. and Utzinger, J. (2009). Rapid mapping of schistosomiasis and other neglected tropical diseases in the context of integrated control programmes in Africa. Parasitology 136, 1707–1718.CrossRefGoogle ScholarPubMed
Brouwer, K. C., Ndhlovu, P. D., Wagatsuma, Y., Munatsi, A. and Shiff, C. J. (2003). Urinary tract pathology attributed to Schistosoma haematobium: Does parasite genetics play a role? American Journal of Tropical Medicine and Hygiene 68, 456–462.CrossRefGoogle ScholarPubMed
Criscione, C. D. and Blouin, M. S. (2004). Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evolution 58, 198–202.Google ScholarPubMed
Curtis, J., Sorensen, R. E. and Minchella, D. J. (2002). Schistosome genetic diversity: the implications of population structure as detected with microsatellite markers. Parasitology 125 (Suppl.), S51–S59.CrossRefGoogle ScholarPubMed
Devon, B. K., Tania, M. K., Diane, L. R. and Robert, P. (2009). Contrasting mtDNA diversity and population structure in a direct-developing marine gastropod and its trematode parasites. Molecular Ecology 18, 4591–4603.Google Scholar
Dumont, M., Mone, H., Mouahid, G., Idris, M. A., Shaban, M. and Boissier, J. (2007). Influence of pattern of exposure, parasite genetic diversity and sex on the degree of protection against reinfection with Schistosoma mansoni. Parasitology Research 101, 247–252.CrossRefGoogle ScholarPubMed
Excoffier, L., Laval, G. and Schneider, S. (2005). Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.Google Scholar
Feng, Z., Curtis, J. and Minchella, D. J. (2001). The influence of drug treatment on the maintenance of schistosome genetic diversity. Journal of Mathematical Biology 43, 52–68.CrossRefGoogle ScholarPubMed
Fu, Y. X. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.CrossRefGoogle ScholarPubMed
Gower, C. M., Shrivastava, J., Lamerton, P. H. L., Rollinson, D., Webster, B. L., Emery, A., Kabatereine, N. B. and Webster, J. P. (2007). Development and application of an ethically and epidemiologically advantageous assay for the multi-locus microsatellite analysis of Schistosoma mansoni. Parasitology 134, 523–536.CrossRefGoogle ScholarPubMed
Hanelt, B., Brant, S. V., Steinauer, M. L., Maina, G. M., Kinuthia, J. M., Agola, L. E., Mwangi, I. N., Mungai, B. N., Mutuku, M. W., Mkoji, G. M. and Loker, E. S. (2009). 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. Parasitology 136, 987–1001.CrossRefGoogle Scholar
Jorgensen, A., Kristensen, T. K. and Stothard, J. R. (2007). Phylogeny and biogeography of African Biomphalaria (Gastropoda: Planorbidae) with emphasis on endemic species of the great east African lakes. Zoological Journal of the Linnean Society 151, 337–349.CrossRefGoogle Scholar
Kabatereine, N. B., Fleming, F. M., Nyandindi, U., Mwanza, J. C. L. and Blair, L. (2006). The control of schistosomiasis and soil-transmitted helminths in East Africa. Trends in Parasitology 22, 332–339.CrossRefGoogle ScholarPubMed
Kumar, P. N., Patra, K. P., Hoti, S. L. and Das, P. K. (2002). Genetic variability of the human filarial parasite, Wuchereria bancrofti in South India. Acta Tropica 82, 67–76.CrossRefGoogle Scholar
Morgan, J. A. T., Dejong, R. J., Adeoye, G. O., Ansa, E. D. O., Barbosa, C. S., Bremond, P., Cesari, I. M., Charbonnel, N., Correa, L. R., Coulibaly, G., D'Andrea, P. S., De Souza, C. P., Doenhoff, M. J., File, S., Idris, M. A., Incani, R. N., Jarne, P., Karanja, D. M. S., Kazibwe, F., Kpikpi, J., Lwambo, N. J. S., Mabaye, A., Magalhaes, L. A., Makundi, A., Mone, H., Mouahid, G., Muchemi, G. M., Mungai, B. N., Sene, M., Southgate, V., Tchuente, L. A. T., Theron, A., Yousif, F., Magalhaes, E. M. Z., Mkoji, G. M. and Loker, E. S. (2005). Origin and diversification of the human parasite Schistosoma mansoni. Molecular Ecology 14, 3889–3902.CrossRefGoogle ScholarPubMed
Rodrigues, N. B., Coura, P., de Souza, C. P., Passos, L. K. J., Dias-Neto, E. and Romanha, A. J. (2002). Populational structure of Schistosoma mansoni assessed by DNA microsatellites. International Journal for Parasitology 32, 843–851.CrossRefGoogle ScholarPubMed
Rollinson, D., Webster, J. P., Webster, B., Nyakaana, S., Jorgensen, A. and Stothard, J. R. (2009). Genetic diversity of schistosomes and snails: implications for control. Parasitology 136, 1801–1811.CrossRefGoogle ScholarPubMed
Shrivastava, J., Qian, B. and Webster, J. P. (2005). An insight into the genetic variation of Schistosoma japonicum in mainland China using DNA microsatellite markers. Molecular Ecology 14, 839–849.CrossRefGoogle ScholarPubMed
Smithers, S. R. and Terry, R. J. (1965). The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of the adult worms. Parasitology 55, 695–700.CrossRefGoogle ScholarPubMed
Standley, C. J., Adriko, M., Alinaitwe, M., Kazibwe, F., Kabatereine, N. B. and Stothard, J. R. (2009). Intestinal schistosomiasis and soil-transmitted helminthiasis in Ugandan schoolchildren: a rapid mapping assessment. Geospatial Health 4, 39–53.CrossRefGoogle ScholarPubMed
Steinauer, M. L., Hanelt, B., Agola, L. E., Mkoji, G. M. and Loker, E. S. (2009). Genetic structure of Schistosoma mansoni in western Kenya: the effects of geography and host sharing. International Journal for Parasitology 39, 1353–1362.CrossRefGoogle ScholarPubMed
Stohler, R. A., Curtis, J. and Minchella, D. J. (2004). A comparison of microsatellite polymorphism and heterozygosity among field and laboratory populations of Schistosoma mansoni. International Journal for Parasitology 34, 595–601.CrossRefGoogle ScholarPubMed
Stothard, J. R., Chitsulo, L., Kristensen, T. K. and Utzinger, J. (2009 a). Control of schistosomiasis in sub-Saharan Africa: progress made, new opportunities and remaining challenges. Parasitology 136, 1665–1675.CrossRefGoogle ScholarPubMed
Stothard, J. R. and Rollinson, D. (1996). An evaluation of random amplified polymorphic DNA (RAPD) for the identification and phylogeny of freshwater snails of the genus Bulinus (Gastropoda: Planorbidae). Journal of Molluscan Studies 62, 165–176.CrossRefGoogle Scholar
Stothard, J. R. and Rollinson, D. (1997). Partial DNA sequences from the mitochondrial cytochrome oxidase subunit I (COI) gene can differentiate the intermediate snail hosts Bulinus globosus and B. nasutus (Gastropoda: Planorbidae). Journal of Natural History 31, 727–737.CrossRefGoogle Scholar
Stothard, J. R., Webster, B. L., Weber, T., Nyakaana, S., Webster, J. P., Kazibwe, F., Kabatereine, N. B. and Rollinson, D. (2009 b). Molecular epidemiology of Schistosoma mansoni in Uganda: DNA barcoding reveals substantive genetic diversity within Lake Albert and Lake Victoria populations. Parasitology 136, 1813–1824.CrossRefGoogle Scholar
Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.CrossRefGoogle ScholarPubMed
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.CrossRefGoogle ScholarPubMed
Utzinger, J., Raso, G., Brooker, S., De Savigny, D., Tanner, M., Ornbjerg, N., Singer, B. H. and N'Goran, E. K. (2009). Schistosomiasis and neglected tropical diseases: towards integrated and sustainable control and a word of caution. Parasitology 136, 1859–1874.CrossRefGoogle Scholar