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Sex ratios in the rodent malaria parasite, Plasmodium chabaudi

Published online by Cambridge University Press:  17 October 2003

S. E. REECE ,
A. B. DUNCAN ,
S. A. WEST  and
A. F. READ
S. E. REECE
Affiliation:
Institute of Cell, Animal and Population Biology, Ashworth Laboratories, West Mains Road, University of Edinburgh, Edinburgh EH9 3JT, UK
A. B. DUNCAN
Affiliation:
Institute of Cell, Animal and Population Biology, Ashworth Laboratories, West Mains Road, University of Edinburgh, Edinburgh EH9 3JT, UK
S. A. WEST
Affiliation:
Institute of Cell, Animal and Population Biology, Ashworth Laboratories, West Mains Road, University of Edinburgh, Edinburgh EH9 3JT, UK
A. F. READ
Affiliation:
Institute of Cell, Animal and Population Biology, Ashworth Laboratories, West Mains Road, University of Edinburgh, Edinburgh EH9 3JT, UK
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Abstract

The sex ratios of malaria and related Apicomplexan parasites play a major role in transmission success. Here, we address 2 fundamental issues in the sex ratios of the rodent malaria parasite, Plasmodium chabaudi. First we test the accuracy of empirical methods for estimating sex ratios in malaria parasites, and show that sex ratios made with standard thin smears may overestimate the proportion of female gametocytes. Secondly, we test whether the mortality rate differs between male and female gametocytes, as assumed by sex ratio theory. Conventional application of sex ratio theory to malaria parasites assumes that the primary sex ratio can be accurately determined from mature gametocytes circulating in the peripheral circulation. We stopped gametocyte production with chloroquine in order to study a cohort of gametocytes in vitro. The mortality rate was significantly higher for female gametocytes, with an average half-life of 8 h for female gametocytes and 16 h for male gametocytes.

Keywords

sex allocation theorygametocytemortalityblood smears
Type
Research Article
Information
Parasitology , Volume 127 , Issue 5 , November 2003 , pp. 419 - 425
Copyright
2003 Cambridge University Press

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References

REFERENCES

AIKAWA, M., RENER, J., CARTER, R. & MILLER, L. H. ( 1981). An electron microscopical study of the interaction of monoclonal antibodies with gametes of the malaria parasite Plasmodium gallinaceum. Journal of Protozoology 28, 383–388.CrossRefGoogle Scholar
BENNETT, G. F. & PEIRCE, M. A. ( 1992). Leucocytozoids of 7 old world passeriform families. Journal of Natural History 26, 693–707.CrossRefGoogle Scholar
BILLKER, O., SHAW, M. K., MARGOS, G. & SINDEN, R. E. ( 1997). The roles of temperature, pH and mosquito factors as triggers of male and female gametogenesis of Plasmodium berghei in vitro. Parasitology 114, 1–7.CrossRefGoogle Scholar
BURKOT, T., WILLIAMS, J. L. & SCHNEIDER, I. (1984). Infectivity to mosquitoes of Plasmodium falciparum clones grown in vitro from the same isolate. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 339–341.CrossRefGoogle Scholar
CARTER, R. & WALLIKER, D. (1975). New observations on the malaria parasites of rodents of the Central African Republic – Plasmodium vinckei petteri subsp. nov. and Plasmodium chabaudi Landau, 1965. Annals of Tropical Medicine and Parasitology 69, 187–196.Google Scholar
DEARSLY, A. L., SINDEN, R. E. & SELF, I. A. ( 1990). Sexual development in malarial parasites: gametocyte production, fertility and infectivity to the mosquito vector. Parasitology 3, 359–368.CrossRefGoogle Scholar
DYE, C. & GODFRAY, H. J. C. ( 1993). On sex ratio and inbreeding in malaria parasite populations. Journal of Theoretical Biology 161, 131–134.CrossRefGoogle Scholar
EKSI, S. & WILLIAMSON, K. C. ( 2002). Male-specific expression of the paralog of malaria transmission blocking target antigen Pfs230, PfB0400w. Molecular and Biochemical Parasitology 122, 127–130.CrossRefGoogle Scholar
FALLIS, A. M. & DESSER, S. S. ( 1974). On species of Leucocytozoan. Advances in Parasitology 12, 1–67.Google Scholar
GARDNER, A., REECE, S. E. & WEST, S. A. ( 2003). Even more extreme fertility insurance and the sex ratios of protozoan blood parasites. Journal of Theoretical Biology ( in the Press).CrossRefGoogle Scholar
JANSE, C. J., BOORSMA, E. G., RAMESAR, J., VANVIANEN, P., VANDERMEER, R., ZENOBI, P., CASAGLIA, O., MONS, B. & VANDERBERG, F. M. ( 1989). Plasmodium berghei – gametocyte production, DNA content, and chromosome-size polymorphisms during asexual multiplication in vivo. Experimental Parasitology 68, 274–282.CrossRefGoogle Scholar
JANSE, C. J., VANDERKLOOSTER, P. F. J., VANDERKAAY, H. J., VANDERPLOEG, M. & OVERDULVE, J. P. ( 1986). Rapid repeated DNA-replication during microgametogenesis and DNA-synthesis in young zygotes of Plasmodium berghei. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 154–157.CrossRefGoogle Scholar
KAWAMOTO, F., KIDO, N., HANAICHI, T., DJAMGOZ, M. B. A. & SINDEN, R. E. ( 1992). Gamete development in Plasmodium berghei regulated by ionic exchange mechanisms. Parasitology Research 78, 277–284.CrossRefGoogle Scholar
LANDAU, I. & BOULARD, Y. (1978). Life cycles and morphology. In Rodent Malaria (ed. Killick-Kendrick, R. & Peters, W.), pp. 53–84. Academic Press, London.CrossRef
MACOMBER, P. B., O'BRIEN, R. L. & HAHN, F. E. ( 1966). Chloroquine: physiological basis of drug resistance in Plasmodium berghei. Science 152, 1374–1375.CrossRefGoogle Scholar
MICKS, D. W., de CAIRES, P. F. & FRANCO, L. B. (1948). The relationship of exflagellation in avian Plasmodia to pH and immunity in the mosquito. American Journal of Hygiene 48, 182–190.Google Scholar
NEE, S., WEST, S. A. & READ, A. F. ( 2002). Inbreeding and parasite sex ratios. Proceedings of the Royal Society of London, Series B 269, 755–760.CrossRefGoogle Scholar
OGWAN'G, R. A., MWANGI, J. K., GITHURE, J., WERE, J. B. O., ROBERTS, C. R. & MARTIN, S. K. ( 1993). Factors affecting exflagellation of in vitro cultivated Plasmodium falciparum gametocytes. American Journal of Tropical Medicine and Hygiene 49, 25–29.CrossRefGoogle Scholar
OWENS, I. P. F. ( 2002). Sex differences in mortality rate. Science 297, 2008–2009.CrossRefGoogle Scholar
PAUL, R. E. L., BREY, P. T. & ROBERT, V. ( 2002). Plasmodium sex determination and transmission to mosquitoes. Trends in Parasitology 18, 32–38.CrossRefGoogle Scholar
PAUL, R. E. L., COULSON, T. N., RAIBAUD, A. & BREY, P. T. ( 2000). Sex determination in malaria parasites. Science 287, 128–131.CrossRefGoogle Scholar
PETERS, W. ( 1970). The pharmacology and mode of action of antimalarial drugs with especial reference to drug resistance. In Chemotherapy and Drug resistance in Malaria. Academic Press, London.
PICKERING, J., READ, A. F., GUERRERO, S. & WEST, S. A. ( 2000). Sex ratio and virulence in two species of lizard malaria parasites. Evolutionary Ecology Research 2, 171–184.Google Scholar
RANFORD-CARTWRIGHT, L. C., BALFE, P., CARTER, R. & WALLIKER, D. ( 1993). Frequency of cross fertilisation in the human malaria parasite Plasmodium falciparum. Parasitology 107, 11–18.CrossRefGoogle Scholar
READ, A. F., NARARA, A., NEE, S., KEYMER, A. E. & DAY, K. P. ( 1992). Gametocyte sex ratios as indirect measures of outcrossing rates in malaria. Parasitology 104, 387–395.CrossRefGoogle Scholar
READ, A. F., SMITH, T. G., NEE, S. & WEST, S. A. ( 2002). Sex ratios of malaria parasites and related protozoa. In Sex Ratios: Concepts and Research Methods (ed. Hardy, I. C. W.), pp. 314–332. Cambridge University Press, Cambridge.CrossRef
REECE, S. E. & READ, A. (2000). Malaria sex ratios. Trends in Ecology and Evolution 15, 259–260.CrossRefGoogle Scholar
ROBERT, V., READ, A. F., ESSONG, J., TCHUINKAM, T., MULDER, B., VERHAVE, J. P. & CARNEVALE, P. ( 1996). Effect of gametocyte sex ratio on infectivity of Plasmodium falciparum to Anopheles gambiae. Transactions of the Royal Society of Tropical Medicine and Hygiene 90, 621–624.CrossRefGoogle Scholar
SCHALL, J. J. ( 1989). The sex ratio of Plasmodium gametocytes. Parasitology 98, 343–350.CrossRefGoogle Scholar
SCHALL, J. J. ( 2000). Transmission success of the malaria parasite Plasmodium mexicanum into its vector: role of gametocyte density and sex ratio. Parasitology 121, 575–580.CrossRefGoogle Scholar
SEVERINI, C., SILVESTRINI, F., SANNELLA, A., BARCA, S., GRADONI, L. & ALANO, P. ( 1999). The production of the osmiophillic body protein Pfg377 is associated with state of maturation and sex in Plasmodium falciparum gametocytes. Molecular and Biochemical Parasitology 100, 247–252.CrossRefGoogle Scholar
SILVESTRINI, F., ALANO, P. & WILLIAMS, J. L. (2000). Commitment to the production of male and female gametocytes in the human malaria parasite Plasmodium falciparum. Parasitology 121, 465–471.CrossRefGoogle Scholar
SINDEN, R. E. (1975). Microgametogenesis in Plasmodium yoeli nigeriensis: a scanning electron microscope investigation. Protistologica 11, 263–268.Google Scholar
SINDEN, R. E. ( 1983). Sexual development of malarial parasites. Advances in Parasitology 22, 153–216.CrossRefGoogle Scholar
SINDEN, R. E., CANNING, E. U., BRAY, R. S. & SMALLEY, M. E. ( 1978). Gametocyte and gamete development in Plasmodium falciparum. Proceedings of the Royal Society of London, Series B 201, 375–399.CrossRefGoogle Scholar
SINDEN, R. E., CANNING, E. U. & SPAIN, B. ( 1976). Gametogenesis and fertilisation in Plasmodium yoeli nigeriensis: a transmission electron microscope study. Proceedings of the Royal Society of London, Series B 193, 55–76.CrossRefGoogle Scholar
SMALLEY, M. E. & SINDEN, R. E. ( 1977). Plasmodium falciparum gametocytes: their longevity and infectivity. Parasitology 74, 1–8.CrossRefGoogle Scholar
SMITH, T. G., LOURENCO, P., CARTER, R., WALLIKER, D. & RANFORD-CARTWRIGHT, L. ( 2000). Commitment to sexual differentiation in the human malaria parasite Plasmodium falciparum. Parasitology 121, 127–133.CrossRefGoogle Scholar
WEST, S. A., REECE, S. E. & READ, A. F. ( 2001). The evolution of gametocyte sex ratios in malaria and related apicomplexan (protozoan) parasites. Trends in Parasitology 17, 525–531.CrossRefGoogle Scholar
WEST, S. A., SMITH, T. G. & READ, A. F. ( 2000). Sex allocation and population structure in apicomplexan (protozoa) parasites. Proceedings of the Royal Society of London, Series B 267, 257–263.CrossRefGoogle Scholar
WEST, S. A., SMITH, T. G. & READ, A. F. ( 2002). Fertility insurance and the sex ratios of malaria and related Hemosporin blood parasites. Journal of Parasitology 88, 258–263.CrossRefGoogle Scholar