Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-03T05:05:02.979Z Has data issue: false hasContentIssue false
  • English
  • Français

Rodent malaria parasites suffer from the presence of conspecific clones in three-clone Plasmodium chabaudi infections

Published online by Cambridge University Press:  17 October 2003

J. C. DE ROODE ,
A. F. READ ,
B. H. K. CHAN  and
M. J. MACKINNON
J. C. DE ROODE
Affiliation:
Institute of Cell, Animal and Population Biology, University of Edinburgh, Ashworth Laboratories, King's Buildings, West Mains Road, Edinburgh EH9 3JT, Scotland, UK
A. F. READ
Affiliation:
Institute of Cell, Animal and Population Biology, University of Edinburgh, Ashworth Laboratories, King's Buildings, West Mains Road, Edinburgh EH9 3JT, Scotland, UK
B. H. K. CHAN
Affiliation:
Institute of Cell, Animal and Population Biology, University of Edinburgh, Ashworth Laboratories, King's Buildings, West Mains Road, Edinburgh EH9 3JT, Scotland, UK
M. J. MACKINNON
Affiliation:
Institute of Cell, Animal and Population Biology, University of Edinburgh, Ashworth Laboratories, King's Buildings, West Mains Road, Edinburgh EH9 3JT, Scotland, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

We studied infection dynamics of Plasmodium chabaudi in mice infected with 3 genetically distinct clones – 1 less virulent than the other 2 – either on their own or in mixtures. During the acute phase of infection, total numbers of asexual parasites in mixed-clone infections were equal to those produced by the 3 clones alone, suggesting strong in-host competition among clones. During the chronic phase of the infection, mixed-clone infections produced more asexual parasites than single-clone infections, suggesting lower levels of competition than during the acute phase, and indicating that a genetically diverse infection is harder to control by the host immune system. Transmission potential over the whole course of infection was lower from mixed-clone infections than from the average of the 3 single-clone infections. These results suggest that in-host competition reduces both growth rate and probability of transmission for individual parasite clones.

Keywords

malariaPlasmodium chabaudivirulenceevolutioncompetitionmixed infections
Type
Research Article
Information
Parasitology , Volume 127 , Issue 5 , November 2003 , pp. 411 - 418
Copyright
2003 Cambridge University Press

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

ARNOT, D. ( 1998). Clone multiplicity of Plasmodium falciparum infections in individuals exposed to variable levels of disease transmission. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 580–585.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, 572–577.CrossRefGoogle Scholar
BABIKER, H. A., RANFORD-CARTWRIGHT, L. C. & WALLIKER, D. ( 1999). Genetic structure and dynamics of Plasmodium falciparum infections in the Kilombero region of Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, S11–S14.CrossRefGoogle Scholar
BEALE, G. H., CARTER, R. & WALLIKER, D. ( 1978). Genetics. In Rodent Malaria (ed. Killick Kendrick, R. & Peters, W.), pp. 213–246. Academic Press, London.CrossRef
BIGGS, B.-A., GOOZÉ, L., WYCHERLEY, K., WOLLISH, W., SOUTHWELL, B., LEECH, J. H. & BROWN, G. V. ( 1991). Antigenic variation in Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA 88, 9171–9174.CrossRefGoogle Scholar
BROWN, K. N. & BROWN, I. N. ( 1965). Immunity to malaria: antigenic variation in chronic infections of Plasmodium knowlesi. Nature, London 208, 1286–1288.CrossRefGoogle Scholar
BRUCE, M. C., DONNELLY, C. A., ALPERS, M. P., GALINSKI, M. R., BARNWELL, J. W., WALLIKER, D. & DAY, K. P. ( 2000). Cross-species interactions between malaria parasites in humans. Science 287, 845–848.CrossRefGoogle Scholar
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 Scholar
COX, F. E. G. (1988). Major models in malaria research: rodent. In Malaria: Principles and Practice of Malariology (ed. Wernsdorfer, W. H. & McGregor, I.), pp. 1503–1543. Churchill Livingstone, Edinburgh.
FELGER, I., SMITH, T., EDOH, D., KITUA, A., ALONSO, P., TANNER, M. & BECK, H. P. ( 1999). Multiple Plasmodium falciparum infections in Tanzanian infants. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, S29–S34.CrossRefGoogle Scholar
FERGUSON, H. M. & READ, A. F. ( 2002). Genetic and environmental determinants of malaria parasite virulence in mosquitoes. Proceedings of the Royal Society of London, Series B 269, 1217–1224.CrossRefGoogle Scholar
JACOBS, R. L. ( 1964). Role of p-aminobenzoic acid in Plasmodium berghei infection in the mouse. Experimental Parasitology 15, 213–225.CrossRefGoogle Scholar
JAKEMAN, G. N., SAUL, A., HOGARTH, W. L. & COLLINS, W. E. ( 1999). Anaemia of acute malaria infections in non-immune patients primarily results from destruction of uninfected erythrocytes. Parasitology 119, 127–133.CrossRefGoogle Scholar
JARRA, W. & BROWN, K. N. ( 1989). Protective immunity to malaria: studies with cloned lines of rodent malaria in CBA/Ca mice. IV. The specificity of mechanisms resulting in crisis and resolution of the primary acute phase parasitaemia of Plasmodium chabaudi chabaudi and P. yoelii yoelii. Parasite Immunology 11, 1–13.Google Scholar
LI, C., SEIXAS, E. & LANGHORNE, J. ( 2001). Rodent malarias: the mouse as a model for understanding immune responses and pathology induced by the erythrocytic stages of the parasite. Medical Microbiology and Immunology 189, 115–126.CrossRefGoogle Scholar
MACKINNON, M. J., GAFFNEY, D. J. & READ, A. F. ( 2002). Virulence of malaria parasites: host genotype by parasite genotype interactions. Infection, Genetics and Evolution 1, 287–296.CrossRefGoogle Scholar
MACKINNON, M. J. & READ, A. F. ( 1999). Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution 53, 689–703.CrossRefGoogle Scholar
McLEAN, S. A., MACDOUGALL, L. M. & PHILLIPS, R. S. ( 1990). Early appearance of variant parasites in Plasmodium chabaudi infections. Parasite Immunology 12, 97–103.CrossRefGoogle Scholar
McLEAN, S. A., PEARSON, C. D. & PHILLIPS, R. S. ( 1982). Plasmodium chabaudi: evidence of antigenic variation during recrudescent parasitaemias in mice. Experimental Parasitology 54, 296–300.CrossRefGoogle Scholar
MENENDEZ, C., FLEMING, A. F. & ALONSO, P. L. ( 2000). Malaria-related anaemia. Parasitology Today 16, 469–476.CrossRefGoogle Scholar
MOTA, M. M., NEIL BROWN, K., HOLDER, A. A. & JARRA, W. ( 1998). Acute Plasmodium chabaudi chabaudi malaria infection induces antibodies which bind to the surfaces of parasitized erythrocytes and promote their phagocytosis by macrophages in vitro. Infection and Immunity 66, 4080–4086.Google Scholar
PHILLIPS, R. S., BRANNAN, L. R., BALMER, P. & NEUVILLE, P. ( 1997). Antigenic variation during malaria infection – the contribution from the murine parasite Plasmodium chabaudi. Parasite Immunology 19, 427–434.CrossRefGoogle Scholar
READ, A. F. & TAYLOR, L. H. ( 2001). The ecology of genetically diverse infections. Science 292, 1099–1102.CrossRefGoogle Scholar
ROBERTS, D. J., CRAIG, A. G., BERENDT, A. R., PINCHES, R., NASH, G., MARSH, K. & NEWBOLD, C. I. ( 1992). Rapid switching to multiple antigenic and adhesive phenotypes in malaria. Nature, London 357, 689–692.CrossRefGoogle Scholar
SAS/STAT. (1990). User's Guide (Version 6.0). SAS Institute, Cary, NC, USA.
SMITH, T., BECK, H. P., KITUA, A., MWANKUSYE, S., FELGER, I., FRASER-HURT, N., IRION, A., ALONSO, P., TEUSCHER, T. & TANNER, M. ( 1999). Age dependence of the multiplicity of Plasmodium falciparum infections and of other malariological indices in an area of high endemicity. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, S15–S20.CrossRefGoogle Scholar
SNOUNOU, G., JARRA, W., VIRIYAKOSOL, S., WOOD, J. C. & BROWN, K. N. ( 1989). Use of a DNA probe to analyse the dynamics of infection with rodent malaria parasites confirms that parasite clearance during crisis is predominantly strain- and species-specific. Molecular and Biochemical Parasitology 37, 37–46.CrossRefGoogle Scholar
TAYLOR, L. H., MACKINNON, M. J. & READ, A. F. ( 1998). Virulence of mixed-clone and single-clone infections of the rodent malaria Plasmodium chabaudi. Evolution 52, 583–591.CrossRefGoogle Scholar
TAYLOR, L. H., WALLIKER, D. & READ, A. F. ( 1997). Mixed-genotype infections of malaria parasites: within-host dynamics and transmission success of competing clones. Proceedings of the Royal Society of London, Series B 264, 927–935.CrossRefGoogle Scholar
TAYLOR, L. H., WALLIKER, D. & READ, A. F. ( 1997). Mixed-genotype infections of the rodent malaria Plasmodium chabaudi are more infectious to mosquitoes than single-genotype infections. Parasitology 115, 121–132.CrossRefGoogle Scholar
TAYLOR-ROBINSON, A. W. ( 1995). Regulation of immunity to malaria: valuable lessons learned from murine models. Parasitology Today 11, 334–342.CrossRefGoogle Scholar
TIMMS, R. (2001). The ecology and evolution of virulence in mixed infections of malaria parasites. Ph.D. thesis, University of Edinburgh.
YAP, G. S. & STEVENSON, M. M. ( 1994). Blood transfusion alters the course and outcome of Plasmodium chabaudi AS infection in mice. Infection and Immunity 62, 3761–3765.Google Scholar