Malaria and mosquitoes: Parasite-induced apoptosis reduces vector reproductive fitness and may enhance transmission

H. Hurd, J. A. Hopwood, A. Polwart & G. T. Williams

Centre for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Staffordshire, ST5 5BG, UK

Anopheline mosquitoes become infected with, and transmit, malaria parasites during the process of bloodfeeding. This is a risky feeding strategy during which the mosquito obtains a proteinaceous meal for egg production but, in the process she is vulnerable to host defence behaviour. Thus a trade-off exists between reproductive success and mosquito longevity. Strategies adopted by a mosquito during a gonotrophic cycle will also affect the survival and transmission success of pathogens that infect her. In particular, malaria parasites will only be transmitted if their host survives 3 or more gonotrophic cycles post-infection, because they take 1-2 weeks to develop as oocysts on the mosquito midgut before sporozoites are formed and salivary gland infections occur. Infection affects both feeding behaviour and nutritional resource management such that feeding persistence and egg production are reduced during the period of malaria sporogony. These strategies may improve the chances of parasite transmission by increasing mosquito longevity. Several aspects of vitellogenesis are affected by infection including the uptake of vitellogenin into ovarian terminal follicles. In infected females, many follicles undergo atresia and are resorbed. Using the rodent malaria, Plasmodium yoelii nigeriensis infection of Anopheles stephensi, we have shown that follicle resorption is associated with programmed cell death or apoptosis. DNA fragmentation was identified using TUNEL and shown to occur in the follicular epithelial cells and nurse cells of terminal follicles at 16 and 18h post infection. Using acridine orange staining of whole follicles, apoptotic nuclei were visualised in 11-15% of follicles per ovary between 20 and 24h post infection. In addition, examination of ultrathin sections showed that some follicles contained epithelial cells that were not developing patency and that contained nuclei with condensed chromatin typical of apoptosis. Oocytes in these follicles did not contain developing yolk spheres. Apoptosis and follicle resorption may be induced directly by the malaria parasite or as the indirect result of a vector’s response to infection. However, by reducing nutrient invested in egg production, a better environment may be provided for the developing parasite.

Index terms: Anopheles stephensi, Plasmodium yoelii nigeriensis, follicular epithelium, reproductive fitness

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