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Male gametocyte fecundity and sex ratio of a malaria parasite, Plasmodium mexicanum

Published online by Cambridge University Press:  15 July 2011

A. T. NEAL*
Affiliation:
Department of Biology, University of Vermont, Burlington, VT 05405, USA
*
*Corresponding author: Tel: 001 802 656 0702. Fax: 001 802 656 2914. E-mail: [email protected]

Summary

Evolutionary theory predicts that the sex ratio of Plasmodium gametocytes will be determined by the number of gametes produced per male gametocyte (male fecundity), parasite clonal diversity and any factor that reduces male gametes' ability to find and combine with female gametes. Despite the importance of male gametocyte fecundity for sex ratio theory as applied to malaria parasites, few data are available on gamete production by male gametocytes. In this study, exflagellating gametes, a measure of male fecundity, were counted for 866 gametocytes from 26 natural infections of the lizard malaria parasite, Plasmodium mexicanum. The maximum male fecundity observed was 8, but most gametocytes produced 2–3 gametes, a value consistent with the typical sex ratio observed for P. mexicanum. Male gametocytes in infections with higher gametocytaemia had lower fecundity. Male fecundity was not correlated with gametocyte size, but differed among infections, suggesting genetic variation for fecundity. Fecundity and sex ratio were correlated (more female gametocytes with higher fecundity) as predicted by theory. Results agree with evolutionary theory, but also suggest a possible tradeoff between production time and fecundity, which could explain the low fecundity of this species, the variation among infections, and the correlation with gametocytaemia.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Alano, P. and Billker, O. (2005). Gametocytes and gametes. In Molecular Approaches to Malaria (ed. Sherman, I. W.), pp. 191219. ASM Press, Washington D.C., USA.Google ScholarPubMed
Alano, P. and Carter, R. (1990). Sexual differentiation in malaria parasites. Annual Reviews of Microbiology 44, 429449.CrossRefGoogle ScholarPubMed
Anderson, T. J. C., Williams, J. T., Nair, S., Sudimack, D., Barends, M., Jaidee, A., Price, R. N. and Nosten, F. (2010). Inferred relatedness and heritability in malaria parasites. Proceedings of the Royal Society of London, B 277, 25312540. doi: 10.1098/rspb.2010.0196.Google ScholarPubMed
Burkot, T. R., Williams, J. L. and Schneider, I. (1984). Infectivity to mosquitoes of Plasmodium falciparum clones grown in vitro from same isolate. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 339341.CrossRefGoogle ScholarPubMed
Carter, R. and Graves, P. M. (1988). Gametocytes. In Malaria: Principles and Practice of Malariology (ed. Wernsdorfer, W. H. and McGregor, I.), pp. 253305. Churchill Livingstone, Edinburgh, UK.Google Scholar
Edwards, A. W. F. (1998). Natural selection and the sex ratio: Fisher's sources. The American Naturalist 151, 564569.CrossRefGoogle ScholarPubMed
Fricke, J. M., Vardo-Zalik, A. M. and Schall, J. J. (2010). Geographic genetic differentiation of a malaria parasite, Plasmodium mexicanum, and its lizard host, Sceloporus occidentalis. Journal of Parasitology 96, 308313.CrossRefGoogle ScholarPubMed
Garnham, P. C. C. (1966). Malaria Parasites and Other Haemosporidia, Blackwell Scientific Publications, Oxford, UK.Google Scholar
Godfray, H. C. J. and Werren, J. H. (1996). Recent developments in sex ratio studies. Trends in Ecology and Evolution 11, 5963.CrossRefGoogle ScholarPubMed
Hamilton, W. D. (1967). Extraordinary sex ratios. Nature, London 156, 477488.Google ScholarPubMed
Hoaglin, D. C., Mosteller, F. and Tukey, J. W. (1983). Introduction to more refined estimators. In Understanding Robust and Exploratory Data Analysis (ed. Hoaglin, D. C., Mosteller, F. and Tukey, J. W.), pp. 283296. John Wiley & Sons, Inc., New York, USA.Google Scholar
Lobo, C. A. and Kumar, N. (1998). Sexual differentiation and development in the malaria parasite. Parasitology Today 14, 146150.CrossRefGoogle ScholarPubMed
Martinsen, E. M., Perkins, S. L. and Schall, J. J. (2008). A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): Evolution of life-history traits and host switches. Molecular Phylogenetics and Evolution 47, 261273.CrossRefGoogle ScholarPubMed
Neal, A. T. and Schall, J. J. (2010). Gametocyte sex ratio in single clone infections of the malaria parasite Plasmodium mexicanum. Parasitology 137, 18511859.CrossRefGoogle ScholarPubMed
Paul, R. E. L., Raibaud, A. and Brey, P. T. (1999). Sex ratio adjustment in Plasmodium gallinaceum. Parassitologia 41, 153158.Google ScholarPubMed
Ranford-Cartwright, L. C. (1995). Fit for fertilization: mating in malaria parasites. Parasitology Today 11, 154157.CrossRefGoogle Scholar
Ranford-Cartwright, L. C., Balfe, P., Carter, R. and Walliker, D. (1993). Frequency of cross-fertilization in the human malaria parasite Plasmodium falciparum. Parasitology 107, 1118.CrossRefGoogle ScholarPubMed
Read, A. F., Narara, A., Nee, S., Keymer, A. E. and Day, K. P. (1992). Gametocyte sex ratios as indirect measures of outcrossing rates in malaria. Parasitology 104, 387395.CrossRefGoogle ScholarPubMed
Reece, S. E., Drew, D. R. and Gardner, A. (2008). Sex ratio adjustment and kin discrimination in malaria parasites. Nature, London 453, 609614. doi: 10.1038/nature06954.CrossRefGoogle ScholarPubMed
Reece, S. E., Duncan, A. B., West, S. A. and Read, A. F. (2003). Sex ratios in the rodent malaria parasite Plasmodium chabaudi. Parasitology 127, 419425.CrossRefGoogle ScholarPubMed
Schall, J. J. (1989). The sex ratio of Plasmodium gametocytes. Parasitology 98, 343350.CrossRefGoogle ScholarPubMed
Schall, J. J. (1990). Virulence of lizard malaria: The evolutionary ecology of an ancient parasite-host association. Parasitology 100 (Suppl.), S35S52.CrossRefGoogle ScholarPubMed
Schall, J. J. (2008). Sex ratios writ small. Nature, London 453, 605606.CrossRefGoogle ScholarPubMed
Schall, J. J. (2009). Do malaria parasites follow the algebra of sex ratio theory? Trends in Parasitology 25, 120123. doi: 10.1016/j.pt.2008.12.006.CrossRefGoogle ScholarPubMed
Schall, J. J. and Vardo, A. M. (2007). Identification of microsatellite markers in Plasmodium mexicanum, a lizard malaria parasite that infects nucleated erythrocytes. Molecular Ecology Notes 7, 227229.CrossRefGoogle Scholar
Sinden, R. E. (1983). Sexual development of malaria parasites. Advances in Parasitology 22, 154216.Google Scholar
Sinden, R. E. (1985). Gametocytogenesis in Plasmodium spp. and observations on the meiotic division. Annales de la Societe bélgé de médecine tropicale 65 (Suppl. 2), 2123.Google ScholarPubMed
Sinden, R. E., Canning, E. U., Bray, R. S. and Smalley, M. E. (1978). Gametocyte and gamete development in Plasmodium falciparum. Proceedings of the Royal Society of London, B 201, 375399.Google ScholarPubMed
Vardo-Zalik, A. M. (2009). Clonal diversity of a malaria parasite, Plasmodium mexicanum, and its transmission success from its vertebrate-to-insect host. International Journal for Parasitology 39, 15731579.CrossRefGoogle ScholarPubMed
Vardo-Zalik, A. M. and Schall, J. J. (2008). Clonal diversity within infections and the virulence of a malaria parasite, Plasmodium mexicanum. Parasitology 135, 13631372.CrossRefGoogle ScholarPubMed
West, S. A., Reece, S. E. and Read, A. F. (2001). Evolution of gametocyte sex ratios in malaria and related apicomplexan (protozoan) parasites. Trends in Parasitology 17, 525531.CrossRefGoogle ScholarPubMed