Skip to main content
NCBI home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 1997 Jun 22;264(1383):927–935. doi: 10.1098/rspb.1997.0128

Mixed-genotype infections of malaria parasites: within-host dynamics and transmission success of competing clones.

L H Taylor 1, D Walliker 1, A F Read 1
PMCID: PMC1688430  PMID: 9225482

Abstract

Mixed-genotype infections of microparasites are common, but almost nothing is known about how competitive interactions within hosts affect the subsequent transmission success of individual genotypes. We investigated changes in the composition of mixed-genotype infections of the rodent malaria Plasmodium chabaudi clones CR and ER by monoclonal antibody analysis of the asexual infection in mice, and by PCR amplification of clone-specific alleles in oocysts sampled from mosquitoes which had fed on these mice. Mixed-clone infections were initiated with a 9:1 ratio of the two clones, with ER as the minority in the first experiment and CR as the minority in the second experiment. When beginning as the majority, clones achieved parasite densities in mice comparable to those achieved in control (single-clone) infections. When they began as the minority, clones were suppressed to less than 10% of control parasitaemias during the early part of the infections. However, in mosquitoes, the frequency of the initially rare clone was substantially greater than it was in mice at the start of the infection or four days prior to the feed. In both experiments, the minority clone in the inocula produced as many, or more, oocysts than it did as a single-clone infection. These experiments show that asexual dominance during most of the infection is poorly correlated to transmission probability, and therefore that the assumption that within-host population size correlates to transmission probability may not be warranted. They also raise the fundamental question of why transmission rates of individual genotypes are often higher from mixed than single-clone infections.

Full Text

The Full Text of this article is available as a PDF (386.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Antia R., Nowak M. A., Anderson R. M. Antigenic variation and the within-host dynamics of parasites. Proc Natl Acad Sci U S A. 1996 Feb 6;93(3):985–989. doi: 10.1073/pnas.93.3.985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Boyle D. B., Newbold C. I., Smith C. C., Brown K. N. Monoclonal antibodies that protect in vivo against Plasmodium chabaudi recognize a 250,000-dalton parasite polypeptide. Infect Immun. 1982 Oct;38(1):94–102. doi: 10.1128/iai.38.1.94-102.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bremermann H. J., Pickering J. A game-theoretical model of parasite virulence. J Theor Biol. 1983 Feb 7;100(3):411–426. doi: 10.1016/0022-5193(83)90438-1. [DOI] [PubMed] [Google Scholar]
  4. Bremermann H. J., Thieme H. R. A competitive exclusion principle for pathogen virulence. J Math Biol. 1989;27(2):179–190. doi: 10.1007/BF00276102. [DOI] [PubMed] [Google Scholar]
  5. Bruce M. C., Alano P., Duthie S., Carter R. Commitment of the malaria parasite Plasmodium falciparum to sexual and asexual development. Parasitology. 1990 Apr;100(Pt 2):191–200. doi: 10.1017/s0031182000061199. [DOI] [PubMed] [Google Scholar]
  6. Buckling A. G., Taylor L. H., Carlton J. M., Read A. F. Adaptive changes in Plasmodium transmission strategies following chloroquine chemotherapy. Proc Biol Sci. 1997 Apr 22;264(1381):553–559. doi: 10.1098/rspb.1997.0079. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cornelissen A. W., Walliker D. Gametocyte development of Plasmodium chabaudi in mice and rats: evidence for host induction of gametocytogenesis. Z Parasitenkd. 1985;71(3):297–303. doi: 10.1007/BF00928331. [DOI] [PubMed] [Google Scholar]
  8. Creasey A., Fenton B., Walker A., Thaithong S., Oliveira S., Mutambu S., Walliker D. Genetic diversity of Plasmodium falciparum shows geographical variation. Am J Trop Med Hyg. 1990 May;42(5):403–413. doi: 10.4269/ajtmh.1990.42.403. [DOI] [PubMed] [Google Scholar]
  9. Daubersies P., Sallenave-Sales S., Magne S., Trape J. F., Contamin H., Fandeur T., Rogier C., Mercereau-Puijalon O., Druilhe P. Rapid turnover of Plasmodium falciparum populations in asymptomatic individuals living in a high transmission area. Am J Trop Med Hyg. 1996 Jan;54(1):18–26. doi: 10.4269/ajtmh.1996.54.18. [DOI] [PubMed] [Google Scholar]
  10. Day K. P., Koella J. C., Nee S., Gupta S., Read A. F. Population genetics and dynamics of Plasmodium falciparum: an ecological view. Parasitology. 1992;104 (Suppl):S35–S52. doi: 10.1017/s0031182000075235. [DOI] [PubMed] [Google Scholar]
  11. Deleersnijder W., Hendrix D., Hamers R. Analysis of MSA-1 diversity in Plasmodium chabaudi chabaudi strains. Mol Biochem Parasitol. 1991 Jun;46(2):315–317. doi: 10.1016/0166-6851(91)90057-d. [DOI] [PubMed] [Google Scholar]
  12. Ebert D., Herre E. A. The evolution of parasitic diseases. Parasitol Today. 1996 Mar;12(3):96–101. doi: 10.1016/0169-4758(96)80668-5. [DOI] [PubMed] [Google Scholar]
  13. Frank S. A. Models of parasite virulence. Q Rev Biol. 1996 Mar;71(1):37–78. doi: 10.1086/419267. [DOI] [PubMed] [Google Scholar]
  14. Gautret P., Miltgen F., Gantier J. C., Chabaud A. G., Landau I. Enhanced gametocyte formation by Plasmodium chabaudi in immature erythrocytes: pattern of production, sequestration, and infectivity to mosquitoes. J Parasitol. 1996 Dec;82(6):900–906. [PubMed] [Google Scholar]
  15. Gravenor M. B., McLean A. R., Kwiatkowski D. The regulation of malaria parasitaemia: parameter estimates for a population model. Parasitology. 1995 Feb;110(Pt 2):115–122. doi: 10.1017/s0031182000063861. [DOI] [PubMed] [Google Scholar]
  16. Hellriegel B. Modelling the immune response to malaria with ecological concepts: short-term behaviour against long-term equilibrium. Proc Biol Sci. 1992 Dec 22;250(1329):249–256. doi: 10.1098/rspb.1992.0156. [DOI] [PubMed] [Google Scholar]
  17. Hetzel C., Anderson R. M. The within-host cellular dynamics of bloodstage malaria: theoretical and experimental studies. Parasitology. 1996 Jul;113(Pt 1):25–38. doi: 10.1017/s0031182000066245. [DOI] [PubMed] [Google Scholar]
  18. Holt R. D. Predation, apparent competition, and the structure of prey communities. Theor Popul Biol. 1977 Oct;12(2):197–129. doi: 10.1016/0040-5809(77)90042-9. [DOI] [PubMed] [Google Scholar]
  19. Landau I., Chabaud A. Plasmodium species infecting Thamnomys rutilans: a zoological study. Adv Parasitol. 1994;33:49–90. doi: 10.1016/s0065-308x(08)60411-x. [DOI] [PubMed] [Google Scholar]
  20. Langhorne J., Simon-Haarhaus B., Meding S. J. The role of CD4+ T cells in the protective immune response to Plasmodium chabaudi in vivo. Immunol Lett. 1990 Aug;25(1-3):101–107. doi: 10.1016/0165-2478(90)90099-c. [DOI] [PubMed] [Google Scholar]
  21. May R. M., Anderson R. M. Parasite-host coevolution. Parasitology. 1990;100 (Suppl):S89–101. doi: 10.1017/s0031182000073042. [DOI] [PubMed] [Google Scholar]
  22. McKean P. G., O'Dea K., Brown K. N. Nucleotide sequence analysis and epitope mapping of the merozoite surface protein 1 from Plasmodium chabaudi chabaudi AS. Mol Biochem Parasitol. 1993 Dec;62(2):199–209. doi: 10.1016/0166-6851(93)90109-b. [DOI] [PubMed] [Google Scholar]
  23. McLean A. P., Lainson F. A., Sharkey A. M., Walliker D. Genetic studies on a major merozoite surface antigen of the malaria parasite of rodents, Plasmodium chabaudi. Parasite Immunol. 1991 Jul;13(4):369–378. doi: 10.1111/j.1365-3024.1991.tb00290.x. [DOI] [PubMed] [Google Scholar]
  24. Nakamura T., Konishi T., Kawaguchi H., Imose J. Estimation of relative fecundity in Eimeria tenella strains by a mixed infection method. Parasitology. 1992 Feb;104(Pt 1):11–17. doi: 10.1017/s0031182000060741. [DOI] [PubMed] [Google Scholar]
  25. Nowak M. A., May R. M. Superinfection and the evolution of parasite virulence. Proc Biol Sci. 1994 Jan 22;255(1342):81–89. doi: 10.1098/rspb.1994.0012. [DOI] [PubMed] [Google Scholar]
  26. Ranford-Cartwright L. C., Balfe P., Carter R., Walliker D. Frequency of cross-fertilization in the human malaria parasite Plasmodium falciparum. Parasitology. 1993 Jul;107(Pt 1):11–18. doi: 10.1017/s003118200007935x. [DOI] [PubMed] [Google Scholar]
  27. Ranford-Cartwright L. C., Balfe P., Carter R., Walliker D. Genetic hybrids of Plasmodium falciparum identified by amplification of genomic DNA from single oocysts. Mol Biochem Parasitol. 1991 Dec;49(2):239–243. doi: 10.1016/0166-6851(91)90067-g. [DOI] [PubMed] [Google Scholar]
  28. Read A. F. The evolution of virulence. Trends Microbiol. 1994 Mar;2(3):73–76. doi: 10.1016/0966-842x(94)90537-1. [DOI] [PubMed] [Google Scholar]
  29. Richie T. L. Interactions between malaria parasites infecting the same vertebrate host. Parasitology. 1988 Jun;96(Pt 3):607–639. doi: 10.1017/s0031182000080227. [DOI] [PubMed] [Google Scholar]
  30. Rosenberg R., Rungsiwongse J., Kangsadalampai S., Sattabongkot J., Suwanabun N., Chaiyaroj S. C., Mongkolsuk S. Random mating of natural Plasmodium populations demonstrated from individual oocysts. Mol Biochem Parasitol. 1992 Jul;53(1-2):129–133. doi: 10.1016/0166-6851(92)90015-c. [DOI] [PubMed] [Google Scholar]
  31. Seed J. R. Competition among serologically different clones of Trypanosoma brucei gambiense in vivo. J Protozool. 1978 Nov;25(4):526–529. doi: 10.1111/j.1550-7408.1978.tb04179.x. [DOI] [PubMed] [Google Scholar]
  32. Snounou G., Bourne T., Jarra W., Viriyakosol S., Wood J. C., Brown K. N. Assessment of parasite population dynamics in mixed infections of rodent plasmodia. Parasitology. 1992 Dec;105(Pt 3):363–374. doi: 10.1017/s0031182000074539. [DOI] [PubMed] [Google Scholar]
  33. Stevenson M. M., Lyanga J. J., Skamene E. Murine malaria: genetic control of resistance to Plasmodium chabaudi. Infect Immun. 1982 Oct;38(1):80–88. doi: 10.1128/iai.38.1.80-88.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Taylor L. H., Read A. F. Why so few transmission stages? Reproductive restraint by malaria parasites. Parasitol Today. 1997 Apr;13(4):135–140. doi: 10.1016/s0169-4758(97)89810-9. [DOI] [PubMed] [Google Scholar]
  35. Yap G. S., Stevenson M. M. Blood transfusion alters the course and outcome of Plasmodium chabaudi AS infection in mice. Infect Immun. 1994 Sep;62(9):3761–3765. doi: 10.1128/iai.62.9.3761-3765.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES