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Random mating in a natural population of the malaria parasite Plasmodium falciparum

Published online by Cambridge University Press:  06 April 2009

H. A. Babiker ,
L. C. Ranford-Cartwright ,
D. Currie ,
J. D. Charlwood ,
P. Billingsley ,
T. Teuscher  and
D. Walliker
H. A. Babiker
Affiliation:
Institute of Cell, Animal and Population Biology, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK
L. C. Ranford-Cartwright
Affiliation:
Institute of Cell, Animal and Population Biology, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK
D. Currie
Affiliation:
Institute of Cell, Animal and Population Biology, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK
J. D. Charlwood
Affiliation:
National Institute for Medical Research, Ifakara Centre, Box 53, Ifakara, Tanzania
P. Billingsley
Affiliation:
Department of Biology, Imperial College, Prince Consort Road, London SW7 2BB, UK
T. Teuscher
Affiliation:
National Institute for Medical Research, Ifakara Centre, Box 53, Ifakara, Tanzania
D. Walliker
Affiliation:
Institute of Cell, Animal and Population Biology, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK
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Summary

The genetic structure of a population of the malaria parasite Plasmodium falciparum has been examined in a village in Tanzania. Seventeen alleles of the merozoite surface protein MSP-1 and 23 of MSP-2 were detected by the polymerase chain reaction (PCR) among the blood parasites of the inhabitants. Most infections contained mixtures of genetically distinct parasite clones. PCR was then used to examine individual P. falciparum oocysts, the products of fertilization events, in wild-caught mosquitoes. Forty-five out of 71 oocysts were heterozygous for one or both genes, showing that crossing between clones was taking place frequently, following uptake of mixtures of gametocytes by the mosquitoes. The frequency of heterozygous forms showed that random mating events probably occurred within mosquito bloodmeals between gametes belonging to different parasite clones.

Keywords

cross-fertilizationPlasmodium falciparummalariaoocysts
Type
Research Article
Information
Parasitology , Volume 109 , Issue 4 , November 1994 , pp. 413 - 421
Copyright
Copyright © Cambridge University Press 1994

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References

REFERENCES

Aley, S. B., Barnwell, J. W., Wendell, D. & Howard, R. J. (1984). Identification of parasite proteins in a membrane preparation enriched for surface membrane of erythrocytes infected with Plasmodium knowlesi. Molecular and Biochemical Parasitology 12, 69–84.CrossRefGoogle Scholar
Babiker, H. A., Creasey, A. M., Fenton, B., Bayoumi, R. A. L., Arnot, D. E. & Walliker, D. (1991). Genetic diversity of Plasmodium falciparum in a village in eastern Sudan. 1. Diversity of enzymes, 2D-PAGE proteins and antigens. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 572–7.CrossRefGoogle Scholar
Babiker, H., Ranford-Cartwright, L., Sultan, A., Satti, G. & Walliker, D. (1994). Genetic evidence that R1 chloroquine resistance of Plasmodium falciparum is caused by recrudescence of resistant parasites. Transactions of the Royal Society of Tropical Medicine and Hygiene (in the Press).CrossRefGoogle Scholar
Boreham, P. F. L., Lenehan, J. K., Boulzaguet, R., Storey, J., Ashkar, T. S., Nambiar, R. & Matsushima, T. (1979). Studies on multiple feeding by Anopheles gambiae s.l. in a Sudan savanna area of north Nigeria. Transactions of the Royal Society of Tropical Medicine and Hygiene 73, 418–23.CrossRefGoogle Scholar
Carter, R. & Voller, A. (1975). The distribution of enzyme variation in populations of Plasmodium falciparum in Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 69, 371–6.CrossRefGoogle ScholarPubMed
Conway, D. J. & McBride, J. S. (1991). Population genetics of Plasmodium falciparum within a malaria hyperendemic area. Parasitology 103, 7–16.CrossRefGoogle ScholarPubMed
Creasey, A., Fenton, B., Walker, A., Thaithong, S., Oliveira, S., Mutambu, S. & Walliker, D. (1990). Genetic diversity of Plasmodium falciparum shows geographical variation. American Journal of Tropical Medicine and Hygiene 42, 403–13.CrossRefGoogle ScholarPubMed
Day, K. P., Koella, J. C., Nee, S., Gupta, S. & Read, A. F. (1992). Population genetics and dynamics of Plasmodium falciparum: an ecological view. Parasitology 104, S35–S52.CrossRefGoogle ScholarPubMed
Dye, C. (1991). Population genetics of nonclonal nonrandomly mating malaria parasites. Parasitology Today 7, 237–40.CrossRefGoogle ScholarPubMed
Fenton, B., Clark, J. T., Anjam Khan, C. M., Robinson, J. V., Walliker, D., Ridley, R., Scaife, J. G. & McBride, J. S. (1991). Structural and antigenic polymorphism of the 35- to 48-kilodalton merozoite surface antigen (MSA-2) of the malaria parasite Plasmodium falciparum. Molecular and Cellular Biology 11, 963–71.Google ScholarPubMed
Foley, M., Ranford-Cartwright, L. C. & Babiker, H. A. (1992). Rapid and simple method for isolating malaria DNA from fingerprick samples of blood. Molecular and Biochemical Parasitology 53, 241–4.CrossRefGoogle ScholarPubMed
Fowler, J. & Cohen, L. (1990). Practical Statistics for Field Biology. Chichester: John Wiley and Sons Ltd.Google Scholar
Kilombero Malaria Project (1992). The level of antisporozoite antibodies in a highly endemic malaria area and its relationship with exposure to mosquitoes. Transactions of the Royal Society of Tropical Medicine and Hygiene 86, 499–504.CrossRefGoogle Scholar
Kimura, E., Mattel, D., di Santi, S. M. & Scherf, A. (1990). Genetic diversity in the major merozoite surface antigen of Plasmodium falciparum: high prevalence of a third polymorphic form detected in strains derived from malaria patients. Gene 91, 57–62.CrossRefGoogle ScholarPubMed
Lyimo, E. O. & Koella, J. C. (1992). Relationship between body size of adult Anopheles gambiae s.l. and infection with the malaria parasite Plasmodium falciparum. Parasitology 104, 233–7.CrossRefGoogle ScholarPubMed
Marshall, V. M., Coppel, R. L., Martin, R. K., Oduola, A. M. J., Anders, R. F. & Kemp, D. J. (1991). A Plasmodium falciparum MSA-2 gene apparently generated by intragenic recombination between the two allelic families. Molecular and Biochemical Parasitology 45, 349–52.CrossRefGoogle ScholarPubMed
Molineaux, L., Muir, D. A., Spencer, H. C. & Wernsdorfer, W. H. (1988). The epidemiology of malaria and its measurement. In Malaria: Principles and Practice of Malariology (ed. Wernsdorfer, W. H. & McGregor, I. A.), pp. 999–1089. Edinburgh: Churchill Livingstone.Google Scholar
Pinswasdi, C., Thaithong, S., Beale, G. H., Fenton, B., Webster, H. K. & Panavand, K. (1987). Polymorphism of proteins in malaria parasites following mefloquine treatment. Molecular and Biochemical Parasitology 23, 159–64.CrossRefGoogle ScholarPubMed
Ranford-Cartwright, L. C., Balfe, P., Carter, R. & Walliker, D. (1991). Genetic hybrids of Plasmodium falciparum identified by amplification of genomic DNA from single oocysts. Molecular and Biochemical Parasitology 49, 239–44.CrossRefGoogle ScholarPubMed
Ranford-Cartwright, L. C., Balfe, P., Carter, R. & Walliker, D. (1993). Frequency of cross-fertilization in the human malaria parasite Plasmodium falciparum. Parasitology 107, 11–18.CrossRefGoogle ScholarPubMed
Rosenberg, R., Rungsiwongse, J., Kangsadalampai, S., Sattabongkot, J., Suwanabun, N., Chaiyaroj, S. & Mongkolsuk, S. (1992). Random mating of natural Plasmodium populations demonstrated from individual oocysts. Molecular and Biochemical Parasitology 53, 129–34.CrossRefGoogle ScholarPubMed
Saiki, R. K., Gelfand, D. H., Stoffel, S., Scharf, S. J., Higuchi, R., Horn, G. T., Mullis, K. B. & Ehrlicfi, H. A. (1988). Primer-directed enzyme amplification of DNA with a thermostable DNA polymerase. Science 239, 487–91.CrossRefGoogle ScholarPubMed
Smith, T., Charlwood, J. D., Kihonda, J., Mwankusye, S., Billingsley, P., Meuwissen, J., Lyimo, E., Takken, W., Teuscher, T. &Tanner, M. (1993). Absence of seasonal variation in malaria parasitaemia in an area of intense seasonal transmission. Acta Tropica 54, 55–72.CrossRefGoogle Scholar
Smythe, J. A., Coppel, R. L., Day, K. P., Martin, R. K., Oduola, A. M. J., Kemp, D. J. & Anders, R. F. (1991). Structural diversity in the Plasmodium falciparum merozoite surface antigen 2. Proceedings of the National Academy of Sciences, USA 88, 1751–5.CrossRefGoogle ScholarPubMed
Snewin, V. A.Herrera, S. (1991). Polymorphism of alleles of the merozoite surface antigens MSAI and MSA2 in Plasmodium falciparum wild isolates from Colombia. Molecular and Biochemical Parasitology 49, 265–76.CrossRefGoogle Scholar
Thaithong, S., Beale, G. H., Fenton, B., McBride, J., Rosario, V., Walker, A. & Walliker, D. (1984). Clonal diversity in a single isolate of the malaria parasite Plasmodium falciparum. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 242–5.CrossRefGoogle Scholar
Tibayrenc, M., Kjellberg, F. & Ayala, F. J. (1990). A clonal theory of parasitic protozoa: the population structures of Entamoeba, Giardia, Leishmania, Naegleria, Plasmodium, Trichomonas and Trypanosoma, and their medical and taxonomical consequences. Proceedings of the National Academy of Sciences, USA 87, 2414–18.CrossRefGoogle ScholarPubMed
Tibayrenc, M., Kjellberg, F., Arnaud, J., Oury, B., Breniere, S. F., Darde, M.-L. & Ayala, F. J. (1991). Are eukaryotic microorganisms clonal or sexual ? A population genetics vantage. Proceedings of the National Academy of Sciences, USA 88, 5129–33.CrossRefGoogle ScholarPubMed
Triglia, T., Wellems, T. E. & Kemp, D. J. (1992). Towards a high resolution map of the Plasmodium falciparum genome. Parasitology Today 8, 225–9.CrossRefGoogle ScholarPubMed
Walliker, D., Quakyi, I. A., Wellems, T. E., McCutchan, T. F., Szarfman, A., London, W. T., Corcoran, L. M., Burkot, T. R. & Carter, R. (1987). Genetic analysis of the human malaria parasite Plasmodium falciparum. Science 236, 1661–6.CrossRefGoogle ScholarPubMed
Weir, B. S. (1992). Independence of VNTR alleles defined as fixed bins. Genetics 130, 873–87.CrossRefGoogle ScholarPubMed
Wellems, T. E., Panton, L. J., Gluzman, I. Y., do Rosario, V. E., Gwadz, R. W., Walker-Jonah, A. & Krogstad, D. J. (1990). Chloroquine resistance not linked to mdr-like genes in a Plasmodium falciparum cross. Nature, London 345, 253–5.CrossRefGoogle ScholarPubMed