Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-24T02:42:40.150Z Has data issue: false hasContentIssue false
  • English
  • Français

Gametocyte sex ratio in single-clone infections of the malaria parasite Plasmodium mexicanum

Published online by Cambridge University Press:  12 July 2010

A.T. NEAL  and
J.J. SCHALL
A.T. NEAL*
Affiliation:
Department of Biology, University of Vermont, Burlington, Vermont 05405, USA
J.J. SCHALL
Affiliation:
Department of Biology, University of Vermont, Burlington, Vermont 05405, USA
*
*Corresponding author: Department of Biology, University of Vermont, Burlington, Vermont, 05405, USA. Tel: 001 802 656 0702. Fax: 001 802 656 2914. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Sex ratio theory predicts that malaria parasites should bias gametocyte production toward female cells in single-clone infections because they will experience complete inbreeding of parasite gametes within the vector. A higher proportion of male gametocytes is favoured under conditions that reduce success of male gametes at reaching females such as low gametocyte density or attack of the immune system later in the infection. Recent experimental studies reveal genetic variation for gametocyte sex ratio in single-clone infections. We examined these issues with a study of experimental single-clone infections for the lizard malaria parasite Plasmodium mexicanum in its natural host. Gametocyte sex ratios of replicate single-clone infections were determined over a period of 3–4 months. Sex ratios were generally female biased, but not as strongly as expected under simple sex ratio theory. Gametocyte density was not related to sex ratio, and male gametocytes did not become more common later in infections. The apparent surplus of male gametocytes could be explained if male fecundity is low in this parasite, or if rapid clotting of the lizard blood reduces male gamete mobility. There was also a significant clone effect on sex ratio, suggesting genetic variation for some life-history trait, possibly male fecundity.

Keywords

sex ratioPlasmodiummalariasex allocationPlasmodium mexicanumgametocyteLocal Mate Competitionfertility insurancesingle-clone infections
Type
Research Article
Information
Parasitology , Volume 137 , Issue 13 , November 2010 , pp. 1851 - 1859
Copyright
Copyright © Cambridge University Press 2010

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

Alano, P. and Billker, O. (2005). Gametocytes and gametes. In Molecular Approaches to Malaria (ed. Sherman, I. W.), pp. 191–219. ASM Press, Washington DC, USA.Google ScholarPubMed
Bromwich, C. R. and Schall, J. J. (1986). Infection dynamics of Plasmodium mexicanum, a malarial parasite of lizards. Ecology 67, 1227–1235.CrossRefGoogle Scholar
Burkot, T. R., Williams, J. L. and 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 ScholarPubMed
Carter, R., Gwadz, R. W. and McAuliffe, F. M. (1979). Plasmodium gallinaceum: Transmission-blocking immunity in chickens. I. Comparative immunogenicity of gametocyte- and gamete-containing preparations. Experimental Parasitology 47, 185–193.CrossRefGoogle ScholarPubMed
Charnov, E. L. (1982). The Theory of Sex Allocation. Princeton University Press, Princeton, NJ, USA.Google ScholarPubMed
Eisen, R. J. and Schall, J. J. (2000). Life history of a malaria parasite (Plasmodium mexicanum): independent traits and basis for variation. Proceedings of the Royal Society of London, B 267, 793–799.CrossRefGoogle ScholarPubMed
Fialho, R. F. and Schall, J. J. (1995). Thermal ecology of a malarial parasite and its insect vector: Consequences for the parasite's transmission success. Journal of Animal Ecology 64, 553–562.CrossRefGoogle Scholar
Gardner, A., Reece, S. E. and West, S. A. (2003). Even more extreme fertility insurance and the sex ratios of protozoan blood parasites. Journal of Theoretical Biology 223, 515–521.CrossRefGoogle ScholarPubMed
Garnham, P. C. C. (1966). Malaria Parasites and other Hemosporidia. Blackwell Scientific Publications, Oxford, UK.Google Scholar
Hamilton, W. D. (1967). Extraordinary sex ratios. Nature, London 156, 477–488.Google ScholarPubMed
Osgood, S. M., Eisen, R. J., Wargo, A. R. and Schall, J. J. (2003). Manipulation of the vertebrate host's testosterone does not affect gametocyte sex ratio of a malaria parasite. Journal of Parasitology 89, 190–192.CrossRefGoogle Scholar
Osgood, S. M. and Schall, J. J. (2004). Gametocyte sex ratio of a malaria parasite: response to experimental manipulation of parasite clonal diversity. Parasitology 128, 23–29.CrossRefGoogle ScholarPubMed
Paul, R. E. L., Coulson, T. N., Raibaud, A. and Brey, P. T. (2000). Sex determination in malaria parasites. Science 287, 128–131.CrossRefGoogle ScholarPubMed
Paul, R. E., Raibaud, A. and Brey, P. T. (1999). Sex ratio adjustment in Plasmodium gallinaceum. Parassitologia 41, 153–158.Google ScholarPubMed
Pickering, J., Read, A. F., Guerrero, S. and West, S. A. (2000). Sex ratio and virulence in two species of lizard malaria parasites. Evolutionary Ecology Research 2, 171–184.Google Scholar
Pleass, R. J. (2009). Platelet power: sticky problems for sticky parasites? Trends in Parasitology 25, 296–299.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, 387–395.CrossRefGoogle ScholarPubMed
Reece, S. E., Drew, D. R. and Gardner, A. (2008). Sex ratio adjustment and kin discrimination in malaria parasites. Nature, London 453, 609–614. doi:10.1038/nature06954CrossRefGoogle 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, 419–425.CrossRefGoogle ScholarPubMed
Robert, V., Sokhana, C. S., Rogier, C., Ariey, F. and Trape, J.-F. (2003). Sex ratio of Plasmodium falciparum gametocytes in inhabitants of Dielmo, Senegal. Parasitology 127, 1–8.CrossRefGoogle ScholarPubMed
Schall, J. J. (1996). Malarial parasites of lizards: diversity and ecology. Advances in Parasitology 37, 255–333.CrossRefGoogle ScholarPubMed
Schall, J. J. (1989). The sex ratio of Plasmodium gametocytes. Parasitology 98, 343–350.CrossRefGoogle ScholarPubMed
Schall, J. J. (1990). Virulence of lizard malaria: the evolutionary ecology of an ancient parasite-host association. Parasitology 100, S35–S52.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Schall, J. J. (2002). Parasite virulence. In The Behavioural Ecology of Parasites (ed. Lewis, , Campbell, E., Sukhdeo, J., , M.), pp. 283–313. CAB International, Oxon, UK.CrossRefGoogle Scholar
Schall, J. J. (2009). Do malaria parasites follow the algebra of sex ratio theory? Trends in Parasitology 25, 120–123.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, 227–229.CrossRefGoogle Scholar
Taylor, L. H. and Read, A. F. (1997). Why so few transmission stages? Reproductive restraint by malaria parasites. Parasitology Today 13, 135–140.CrossRefGoogle ScholarPubMed
Vardo, A. M. and Schall, J. J. (2007). Clonal diversity of a lizard malaria parasite, Plasmodium mexicanum, in its vertebrate host, the western fence lizard: role of variation in transmission intensity over time and space. Molecular Ecology 13, 2712–2720.CrossRefGoogle Scholar
Vardo-Zalik, A. M. and Schall, J. J. (2008). Clonal diversity within infections and the virulence of a malaria parasite, Plasmodium mexicanum. Parasitology 135, 1363–1372.CrossRefGoogle ScholarPubMed
Vardo-Zalik, A. M. and Schall, J. J. (2009). Clonal diversity alters the infection dynamics of a malaria parasite (Plasmodium mexicanum) in its vertebrate host. Ecology 90, 529–536.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, 525–531.CrossRefGoogle ScholarPubMed
West, S. A., Smith, T. G., Nee, S. and Read, A. F. (2002). Fertility insurance and the sex ratios of malaria and related hemosporin blood parasites. Journal of Parasitology 88, 258–263.CrossRefGoogle ScholarPubMed