Impact of mating on Anopheles coluzzii in response to infection

Abstract

Mating causes dramatic changes of female physiology, behaviour, and immunity in many insects, often inducing oogenesis, oviposition, and refractoriness to further mating. Females from the Anopheles gambiae species complex typically mate only once in their lifetime during which they receive sperm and seminal fluid proteins as well as a mating plug that contains the steroid hormone 20E. This hormone, also induced by bloodfeeding, plays a major role in activating vitellogenesis for egg production. In this thesis, I present data showing that the mating status of an Anopheles coluzzii female influences her midgut bacterial load and bacterial composition. Furthermore, I show that her susceptibility to Plasmodium falciparum infection is also enhanced upon mating especially when infection intensity is high. I find that mating status has a major impact on the midgut transcriptome, but only under sugar-fed conditions; once females have bloodfed, the transcriptional changes that are still observable as induced by mating are masked. To determine whether increased susceptibility to parasites could be driven by the additional 20E that mated females receive from males, I mimicked mating by injecting 20E into virgin females, finding that these females have significantly increased infection intensity compared to controls. I carried out further RNAseq to examine whether the genes that change upon 20E injection in the midgut are similar to those that change upon mating. I find that 11% of the genes upregulated by 20E are in common with genes upregulated by mating. Together, these findings suggest that male Anopheles mosquitoes might contribute to malaria transmission by influencing female midgut bacterial loads and by potentially increasing P. falciparum susceptibility in females.