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Sex ratio adjustment and kin discrimination in malaria parasites

Abstract

Malaria parasites and related Apicomplexans are the causative agents of the some of the most serious infectious diseases of humans, companion animals, livestock and wildlife. These parasites must undergo sexual reproduction to transmit from vertebrate hosts to vectors, and their sex ratios are consistently female-biased. Sex allocation theory, a cornerstone of evolutionary biology, is remarkably successful at explaining female-biased sex ratios in multicellular taxa, but has proved controversial when applied to malaria parasites. Here we show that, as predicted by theory, sex ratio is an important fitness-determining trait and Plasmodium chabaudi parasites adjust their sex allocation in response to the presence of unrelated conspecifics. This suggests that P. chabaudi parasites use kin discrimination to evaluate the genetic diversity of their infections, and they adjust their behaviour in response to environmental cues. Malaria parasites provide a novel way to test evolutionary theory, and support the generality and power of a darwinian approach.

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Figure 1: The fitness consequences of sex ratio variation.
Figure 2: Genetic variation in patterns of sex allocation.
Figure 3: Explaining sex ratio variation throughout infections.
Figure 4: Sex ratio varies with the genetic diversity of P. chabaudi infections.
Figure 5: Sex ratios of focal genotypes during the growth phase of infections.
Figure 6: Sex ratios of focal genotypes during the post-peak phase of infections.

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Acknowledgements

We thank A. P. Waters, C. Janse and M. R. van Dijk for the genetically modified parasites, and D. H. Nussey, S. A. West, A. F. Read and A. Buckling for discussions. The Wellcome Trust, NERC, BBSRC and Royal Society provided funding.

Author Contributions S.E.R. conceived and designed the experiments, carried out the fitness consequences experiment, analysed sex ratio data and prepared the manuscript. D.R.D. developed the PCR assays, carried out the sex ratio experiments and data collection. A.G. analysed the fitness data and contributed to discussions and manuscript preparation.

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Correspondence to Sarah E. Reece.

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Reece, S., Drew, D. & Gardner, A. Sex ratio adjustment and kin discrimination in malaria parasites. Nature 453, 609–614 (2008). https://doi.org/10.1038/nature06954

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