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Attraction between sexes: male–female gametocyte behaviour within a Leucocytozoon toddi (Haemosporida)

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Abstract

Understanding the breeding systems of Plasmodium, and the closely related Haemoproteus and Leucocytozoon (Apicomplexa: Haemosporida), is fundamental to virulence and transmission research. We report an unusual binding behaviour between gametocytes of Leucocytozoon toddi. This aggregative behaviour was notably characterised by a disparity in the likelihood of clustering by female and male gametocytes. Thus, indicating a possible difference in the ‘stickiness’ of gametocytes per sex. Overall, 12% of gametocytes in this high-parasitaemia infection (0.269 gametocytes per 100 red blood cells (RBCs)) were incorporated into aggregations involving substantial contact. The gametocyte sexual combinations within aggregations varied significantly from expected according to the background 0.49 sex ratio within this sample, with female–female contacts occurring more and male–male contacts occurring less frequently than expected. A second L. toddi (identical for 709 bp of the cyt b mitochondrial gene) with lower parasitemia (0.035 gametocytes per 100 RBCs) showed no significant binding. Interestingly, the ratios of male gametocytes in both of these parasites were greater than expected under sex-ratio theory and similar to the 50% observed in species with syzygy breeding strategies. We discuss the ramifications of this observation in terms of sex-ratio theory and breeding strategies and provide speculative explanations for this unusual gametocyte behaviour.

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Acknowledgements

The authors thank Rachel Fewster for her input into the current manuscript. Steven M. Goodman was responsible for many of the avian hematozoa surveys from 1994 to 2004 and provided equipment and support for this field work. Attale Ravaoarimalala provided field assistance during the Réserve Spéciale d’Ambohitantely survey. The authors recognize Philippe Grellier and Geneviève Milon for their critical comments on a previous version of the manuscript. All research complied with Malagasy laws: Eaux et Forêt and l'Association Nationale pour la Gestion des Aires Protégées provided a research permit for the protected area of Madagascar (271-MINENV.EF/SG/DGEF/DPB/SCBLF du 16 Décembre 2003), and we thank the staff of Réserve Spéciale d’Ambohitantely for their support.

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Correspondence to Rosemary K. Barraclough.

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Research funding was provided by the Institut de Recherche pour le Développement, l’Institut Pasteur, Grand Programme Horizontal Anophèles de l’Institut Pasteur and World Wide Fund for Nature.

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Barraclough, R.K., Duval, L., Talman, A.M. et al. Attraction between sexes: male–female gametocyte behaviour within a Leucocytozoon toddi (Haemosporida). Parasitol Res 102, 1321–1327 (2008). https://doi.org/10.1007/s00436-008-0913-8

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  • DOI: https://doi.org/10.1007/s00436-008-0913-8

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