Abstract
BackgroundIn female mosquitoes that transmit malaria, the benefits of being refractory to the Plasmodium parasite are balanced by the immunity costs in the absence of infection. Male mosquitoes, however, gain no advantage from being refractory to blood-transmitted parasites, so that any costs associated with an enhanced immune system in the males limit the evolution of female refractoriness and has practical implications for the release of transgenic males.MethodsAspects of the male cost of carrying Plasmodium-refractory genes were estimated by comparing the males' immune response and reproductive success among strains of Anopheles gambiae that had been selected for refractoriness or extreme susceptibility to the rodent malaria parasite, Plasmodium yoelii nigeriensis. The refractory males had a stronger melanization response than males from the susceptible line. Four traits were used as correlates of a male's reproductive success: the proportion of females that were inseminated by a fixed number of males in a cage within a fixed time frame, the proportion of females with motile sperm in their spermathecae, the proportion of ovipositing females, and the mean number of eggs per batch.ResultsAlthough there were significant differences among groups of males in sperm motility and oviposition success, these differences in male reproductive success were not associated with the refractory or susceptible male genotypes. Contrary to expectation, females mated to early emerging refractory males laid significantly more eggs per batch than females mated to later emerging susceptible males. Sperm motility and oviposition success were strongly correlated suggesting that variation in sperm motility influences female oviposition and ultimately male reproductive success.ConclusionAn increased melanization response in male A. gambiae does not diminish male reproductive success under the experimental protocol used in this study. That refractory males induced ovipositing females to lay more eggs than susceptible males is an interesting result for any strategy considering the release of transgenic males. That sperm motility influences female oviposition is also important for the release of transgenic males.
Highlights
In female mosquitoes that transmit malaria, the benefits of being refractory to the Plasmodium parasite are balanced by the immunity costs in the absence of infection
Examples of costs incurred by insects include larvae of Drosophila melanogaster selected for parasitoid resistance that are less competitive than unselected controls [2] and Aedes aegypti mosquitoes selected for early pupation that have a weaker immune response to foreign objects (Sephadex beads) than mosquitoes selected for late pupation [3]
The present study suggests that refractory genes are neutral with respect to male fitness in a laboratory setting and that males are unlikely to affect the evolution of Plasmodium-refractoriness in female mosquitoes
Summary
In female mosquitoes that transmit malaria, the benefits of being refractory to the Plasmodium parasite are balanced by the immunity costs in the absence of infection. Species of Plasmodium that cause malaria in man and other vertebrate hosts impose fitness costs on their mosquito vectors because they reduce fecundity [5,6,7] and, in some cases, lifespan [8,9]. That laboratory colonies of mosquitoes respond readily to artificial selection for refractoriness to Plasmodium [13,14] demonstrates that there is genetic variation for this trait. Anopheles gambiae selected for refractoriness to Plasmodium yoelii nigeriensis produced fewer offspring when fed on an uninfected blood meal than susceptible mosquitoes after nine generations of selection This difference was observed in only one of the three replicate selection experiments and the effect was not observed after 12 generations of selection [14]. There is some evidence suggesting that in the absence of infection, increased immunity to Plasmodium may be costly for female mosquitoes
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