Population genetics and dynamics of Plasmodium falciparum: an ecological view | Parasitology | Cambridge Core (original) (raw)

Summary

Molecular characterization of the Plasmodium falciparum genome has led to identification of polymorphic loci and the mechanisms generating genetic diversity in this parasite. This information has resulted in the development of molecular methods to type parasite diversity in the field. Consequently, we are now in a position to describe the population genetics and dynamics of P. falciparum. The limited number of field studies that have been conducted to date have revealed an extraordinary degree of genetic diversity in natural parasite populations. Heterozygous recombination which occurs during meiosis appears to be one mechanism for generating genetic diversity. The rate at which such recombination occurs in natural parasite populations defines the genetic structure of the parasite population and can influence the ability of the parasite to respond to selection pressure. The high frequency of single genotype infections and the female-biased gametocyte sex ratios found in hyperendemic malaria areas suggest that self-fertilization occurs frequently. Population- wide surveys of allele frequencies in endemic areas have, however, shown no evidence of linkage disequilibrium and are consistent with a panmictic population structure. We argue that these studies have only sampled symptomatic infections, within which rare or recombinant genotypes may be disproportionately represented. They also take no account of the spatial structure of P. falciparum populations. Systematic investigations of the amount of heterozygosity in small areas as part of population-wide surveys are required to define the genetic structure of P. falciparum populations. Population dynamic studies which consider genetic heterogeneity of P. falciparum have shown fluctuations of different serotypes in space and time. The host immune response appears to play an important role in generating these dynamics. Integrated field and laboratory studies, which consider the interaction between population genetics and dynamics, will be necessary to describe the population biology of P. falciparum.

References

Allison, A. C. (1964). Polymorphism and natural selection in human populations. Cold Spring Harbor Symposium on Quantitative Biology 29, 137–49.CrossRefGoogle ScholarPubMed

Anders, R. F. (1986). Multiple cross-reactivities amongst antigens of Plasmodium falciparum impair the development of protective immunity against malaria. Parasite Immunology 8, 529–39.CrossRefGoogle ScholarPubMed

Anders, R. F., Brown, G. V. & Edwards, A. E. (1983). Characterization of an S-antigen synthesized by several isolates of Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA 80, 6652–6.CrossRefGoogle ScholarPubMed

Aron, J. L. & May, R. M. (1982). The population dynamics of malaria. In The Population Dynamics of Infectious Diseases: Theory and Applications (ed. Anderson, R. M.), pp. 139–79. London: Chapman and Hall.CrossRefGoogle Scholar

Babiker, H. A., Creasey, A. M., Fenton, B., Bayoumi, H. 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

Biggs, B. A., Gooze, L., Wycherley, K., Wollish, W., Southwell, B., Leech, J. H. & Brown, C. V. (1991). Antigenic variation in Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA (in the Press.)CrossRefGoogle ScholarPubMed

Boreham, P. F. L., Lenahan, J. K., Boulzaquet, R., Storey, J., Ashkar, T. S., Nambier, R. & Matsushima, T. (1979). Studies on multiple feeding by Anopheles gambiae s1. in Garki District, northern Nigeria. Transactions of the Royal Society of Tropical Medicine and Hygiene 73, 418–23.CrossRefGoogle Scholar

Brown, K. N. (1990). The parasitology of malaria and the study of protective immunity. Immunology Letters 25, 97–100.CrossRefGoogle Scholar

Burkot, T. R., Craves, P. M., Paru, R. & Lagog, M. (1988). Mixed blood feeding by the malaria vectors in the Anopheles punctulatus complex (Diptera: Culicidae). Journal of Medical Entomology 25, 205–13.CrossRefGoogle ScholarPubMed

Carter, R. & McGregor, I. A. (1973). Enzyme variation in Plasmodium falciparum in The Gambia. Transactions of the Royal Society of Tropical Medicine and Hygiene 67, 830–7.CrossRefGoogle ScholarPubMed

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

Cattani, J. A., Tulloch, J. L., Vebova, H., Jolley, D., Gibson, F. D., Moir, J. S., Heywood, P. F., Alpers, M. P., Stevenson, A. & Clancy, R. (1986). The epidemiology of malaria in a population surrounding Madang, Papua New Guinea. American Journal of Tropical Medicine and Hygiene 35, 3–15.CrossRefGoogle Scholar

Charlwood, J. D., Graves, P. M. & Birley, M. H. (1986). Capture–recapture studies of Anopheles punctulatus Donitz (Diptera: Culicidae) from Papua New Guinea. Bulletin of Entomological Research 76, 211–27.CrossRefGoogle Scholar

Charnov, E. L. (1982). The Theory of Sex Allocation, Princeton: Princeton University Press.Google ScholarPubMed

Conway, D. J., Greenwood, B. M. & McBride, J. S. (1991). The epidemiology of multiple-clone Plasmodium falciparum infections in Gambian patients. Parasitology 103, 1–6.CrossRefGoogle ScholarPubMed

Conway, D. J. & McBRIDE, J. S. (1991 a). Population genetics of Plasmodium falciparum within a malaria hyperendemic area. Parasitology 103, 7–16.CrossRefGoogle ScholarPubMed

Conway, D. J. & McBride, J. S. (1991 b). Genetic evidence for the importance of interrupted feeding by mosquitos in the transmission of malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 454–6.CrossRefGoogle ScholarPubMed

Cowman, A. F., Saint, R. B., Coppel, R. L., Brown, G. V., Anders, R. F. & Kemp, D. J. (1985). Conserved sequences flank variable tandem repeats in two S-antigen genes of Plasmodium falciparum. Cell 40, 775–83.CrossRefGoogle ScholarPubMed

Cowman, A. F., Morry, M. J., Biggs, B. A., Cross, C. A. M. & Foote, S. J. (1988). Identification of amino acids linked to pyrimethamine resistance in dihydrofolate reductase thymidylate-synthase gene of Plassnodium falciparum. Proceedings of the National Academy of Sciences, USA 85, 9109–13.CrossRefGoogle Scholar

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

Crow, J. F. & Kimura, M. (1962). The number of alleles that can be maintained in a finite population. Genetics 49, 725–38.Google Scholar

Dame, J. B., Williams, J. L., McCutchan, T. F., Weber, J. L., Wirtz, H., Hockmeyer, A., Maloy, W. T., Haynes, J. D., Schneider, I., Roberts, D., Sanders, C. S., Reddy, E. P., Diggs, C. L. & Miller, L. H. (1984). Structure of the gene encoding the immunodominant surface antigen on the sporozoite of the human malaria parasite Plasmodium falciparum. Science 225, 593–9.CrossRefGoogle ScholarPubMed

Day, K. P. & Marsh, K. (1990). Naturally acquired immunity to Plasmodium falciparum. Parasitology Today 6, 68–71.Google Scholar

Dye, C. (1991). Population genetics of nonclonal, nonrandomly mating malaria parasites. Parasitology Today 7, 236–40.CrossRefGoogle ScholarPubMed

Flint, J., Hill, A. V. S., Bowden, D. K., Oppenheimer, S. J., Sill, P. H., Serjeantson, S. W., Bana-Koiri, J., Bhatla, K., Alpers, H. P., Boyce, A. J., Weatherall, D. J. & Clegg, J. B. (1986). High frequencies of α-thalassaemia are the result of natural selection by malaria. Nature, London 321, 744–50.CrossRefGoogle ScholarPubMed

Foote, S. J., Kyle, D. E., Martin, R. K., Oduola, A. M. J., Forsyth, K. P., Kemp, D. J. & Cowman, A. F. (1990). Several alleles of the multi-drug resistance gene are closely linked to chloroquine resistance in Plasmodium falciparum. Nature, London 345, 255–8.CrossRefGoogle ScholarPubMed

Forsyth, K. P., Philip, G., Smith, T., Klim, E., Southwell, B. & Brown, G. V. (1989 a). Diversity of antigens expressed on the surface of erythrocytes infected with mature Plasmodium falciparum parasites in Papua New Guinea. American Journal of Tropical Medicine and Hygiene 41, 259–65.CrossRefGoogle ScholarPubMed

Forsyth, K. P., Anders, R. F., Cattani, J. & Alpers, M. A. (1989 b). Small area variation in prevalence of an S-antigen serotype of Plasmodium falciparum in villages of Madang, Papua New Guinea. American Journal of Tropical Medicine and Hygiene 40, 344–50.CrossRefGoogle ScholarPubMed

Frank, S. A. (1990). Sex allocation theory for birds and mammals. Annual Review of Ecology and Systematics 21, 13–55.CrossRefGoogle Scholar

Graves, P. M., Burkot, T. B., Carter, R., Cattani, J. A., Lagog, M., Parker, J., Brabin, B. J., Gibson, F. D., BRADLEY, D. J. & Alpers, M. A. (1988). Measurement of malarial infectivity of human populations to mosquitos in the Madang region, Papua New Guinea. Parasitology 96, 251–63.CrossRefGoogle ScholarPubMed

Herbert, P. D. N. (1987). The comparative evidence. In The Evolution of Sex and its Consequences (ed. Stearns, S. C.), pp. 192–4. Basel: Birkhäuser Verlag.Google Scholar

Hill, A. V. S., Allsopp, C. E. M., Kwiatkowski, D., Anstey, N. M., Twumasi, P., Rowe, P. A., Bennett, S., Brewster, D., McMichael, A. J. & Greenwood, B. M. (1991). Common West African HLA antigens are associated with protection from severe malaria. Nature, London 352, 595–600.CrossRefGoogle ScholarPubMed

Howard, R. J. (1988). Malarial proteins at the membrane of Plasmodium falciparum infected ervthrocytes and their involvement in cytoadherence to endothelial cells. Progress in Allergy 41, 98–147.Google ScholarPubMed

Joshi, H., Subbarao, S. K., Raghavendra, K. & Sharma, V. P. (1989). Plasmodium vivax: enzyme polymorphism in isolates of Indian origin. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 179–81.CrossRefGoogle ScholarPubMed

Kemp, D. J., Cowman, A. F. & Walliker, D. (1990). Genetic diversity in Plasmodium falciparum. Advances in Parasitology 29, 75–149.CrossRefGoogle ScholarPubMed

Lockyer, M. J. & Schwartz, R. T. (1987). Strain variation in the circumsporozoite gene of Plasmodium falciparum. Molecular and Biochemical Parasitology 22, 101–8.CrossRefGoogle ScholarPubMed

McBride, J. S., Walliker, D. & Morgan, G. (1985). Antigenic diversity in the human malaria parasite Plasmodium falciparum. Science 217, 254–7.CrossRefGoogle Scholar

McConkey, G. A., Waters, A. P. & McCutchan, T. F. (1990). The generation of genetic diversity in malaria parasites. Annual Review of Microbiology 44, 479–98.CrossRefGoogle ScholarPubMed

McCutchan, T. S. & Waters, A. P. (1990). Mutations with multiple independent origins in surface antigens mark the targets of biological selection pressures. Immunology Letters 25, 23–6.CrossRefGoogle Scholar

MacDonald, G. (1957). The Epidemiology and Control of Malaria. London: Oxford University Press.Google Scholar

Marsh, K. & Howard, R. J. (1986). Antigens induced in the circumsporozoite gene of Plasmodium falciparum: expression of diverse and Conserved determinants. Science 231, 150–3.CrossRefGoogle Scholar

Marsh, K., Otoo, L., Hayes, R. J., Carson, D. C. & Greenwood, B. M. (1989). Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 293–303.CrossRefGoogle ScholarPubMed

Pascala, S. W., Hassell, M. P. & May, R. M. (1990). Host–parasite associations in patchy environments. Nature, London 344, 150–3.CrossRefGoogle Scholar

Peterson, D., Walliker, D. & Wellems, T. (1988 a). Evidence that a point mutation in dihydro-folate reductase thymidylate synthase gene confers pyrimethamine resistance in falciparum malaria. Proceedings of the National Academy of Sciences, USA 85, 9114–18.CrossRefGoogle Scholar

Peterson, M. G., Coppel, R. L., McIntyre, P., Langford, C. J., Woodrow, G., Brown, G. V., Anders, R. F. & Kemp, D. J. (1988 b). Variation in the precursor to the major merozoite surface antigens of Plasmodium falciparum. Molecular and Biochemical Parasitology 27, 291–302.CrossRefGoogle Scholar

Port, G. R., Boreham, P. F. L. & Bryan, J. H. (1980). The relationship of host size to feeding of mosquitos of the Anopheles gambiae Giles complex (Diptera: CuliCidae). Bulletin of Entomological Research 70, 133–44.CrossRefGoogle Scholar

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

Read, A. F., Narara, A., Nee, S., Keymer, A. E. & Day, K. (1992). Gametocyte sex ratios as indirect measures of outcrossing rates in malaria. Parasitology 104, (in the Press).CrossRefGoogle ScholarPubMed

Rosenberg, R., Wirtz, R. A., Schneider, I. & Burge, H. (1990). An estimation of the number of malaria sporozoites ejected by a feeding mosquito. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 209–12.CrossRefGoogle ScholarPubMed

Sadun, E. H., Hickman, R. L., Welloe, B. T., Moon, A. D. & Udeozo, I. D. R. (1966). Active and passive immunization of chimpanzees infected with West African and Southeast Asian strains of Plasmodium falciparum. Military Medicine 131 (Suppl.), 1250–62.CrossRefGoogle ScholarPubMed

Saul, A., Myler, P., Schofield, L. & Kidson, C. (1984). A high molecular weight antigen in Plasmodium falciparum recognised by inhibitory monoclonal antibodies. Parasite Immunology 6, 39.CrossRefGoogle ScholarPubMed

Scherf, A., Mattel, D. & Southou, J. L. (1991). Multiple infections and unusual distribution of block 2 of MSA I gene of Plasmodium falciparum detected in West African clinical isolates by polymerase chain reaction analysis. Molecular and Biochemical Parasitology 44, 297–300.CrossRefGoogle Scholar

Schoen, D. J. & Brown, A. H. D. (1991). Intraspecific variation in population gene diversity and effective population size correlates with mating system in plants. Proceedings of the National Academy of Sciences, USA 88, 4494–7.CrossRefGoogle ScholarPubMed

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., England, S. M., Sims, P. F. G. & Hyde, J. E. (1989). Characterization of the dihydrofolate reductase thymidylate synthetase gene from human malaria parasites highly resistant to pyrirnethamine. Gene 76, 41–52.CrossRefGoogle Scholar

Tanabe, K., MacKay, M., Goman, M. & Scaife, J. G. (1987). Allelic dimorphism in a surface antigen gene of the malaria parasite Plasmodium falciparum. Journal of Molecular Biology 195, 273–87.CrossRefGoogle Scholar

Thaithong, S., Sueblinwong, T. & Beale, G. H. (1981). Enzyme typing of some isolates of Plasmodium falciparum from Thailand. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 268–70.CrossRefGoogle ScholarPubMed

Tibayrenc, M. & Ayala, F. J. (1991). Towards a population genetics of micro-organisms: the clonal theory of parasitic protozoa. Parasitology Today 7, 228–32.CrossRefGoogle Scholar

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

Tibayrenc, M., Kjellberg, F. & Ayala, F. J. (1990). A clonal theory of parasitic protozoa: the population structures of Entamoeba, Giardia, Leishmania, Plasmodium, Trichomonas and Trypanosoma and their medical and taxonomic consequences. Proceedings of the National Academy of Sciences, USA 87, 2414–18.CrossRefGoogle Scholar

Walliker, D. (1991). Malaria parasites: randomly interbreeding or ‘clonal’ populations? Parasitology Today 7, 232–5.CrossRefGoogle ScholarPubMed

Walliker, D., Quakyi, L. 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

Wellems, T. E., Walker-Jonah, A. & Panton, L. J. (1991). Genetic mapping of the chloroquine-resistance locus on Plasmodium falciparum chromosome 7. Proceedings of the National Academy of Sciences, USA 88, 3382–6.CrossRefGoogle ScholarPubMed

Wilson, R. J. M., McGregor, I. A. & Hall, P. J. (1975). Persistence and recurrence of S-antigens in Plasmodium falciparum infections in man. Transactions of the Royal Society of Tropical Medicine and Hygiene 69, 461–7.Google ScholarPubMed

Wilson, R. J. M., McGregor, I. A., Hall, P., Williams, K. & Bartholomew, R. (1969). Antigens associated with Plasmodium falciparum infections in man. Lancet ii, 201–5.CrossRefGoogle Scholar