Impact of vertebrate host parasitaemia on Plasmodium development within mosquitoes

Abstract

Background: In vector-borne diseases, invertebrate hosts are exposed to highly variable quantities of parasites during their blood meal. This heterogeneity may partly explain the overdispersed distribution of parasites within the vector population, as well as the variability in the extrinsic incubation period (EIP) of the parasite. Indeed, the quantity of parasites ingested is often considered as a good predictor of the quantity of parasites that will develop within the vectors, as well as the speed at which they will develop (EIP). However, density-dependent processes can strongly influence the relationship between parasite burden in the vertebrate host and in vectors, making this relationship not always clear. Methods: Here, we used the avian malaria system to investigate whether the proportion of red blood cells infected by sexual and/or asexual stages of malaria parasite influences the intensity of malaria infection and the EIP of Plasmodium within the invertebrate vectors. For this purpose, we have experimentally infected twelve vertebrate hosts in order to generate a range of intensity of infection. More than a thousand mosquitoes took a blood meal on these hosts and the development of Plasmodium within the vectors was followed for more than 20 days. Results: The main finding presented in this study reveals a negative relationship between the intensity of infection in the vertebrate host and the EIP. Four days were sufficient for 10% of infected mosquitoes fed on the most infected hosts to become infectious. However, the number of transmissible stages did not significantly vary according to the vertebrate host intensity of infection. Conclusion: While the quantity of ingested parasites had no impact on the density of transmissible stages in infectious mosquitoes, the EIP was affected. Studies have demonstrated that small changes in the EIP can have a significant effect on the number of mosquitoes living long enough to transmit parasites. Here, we observed a difference of 4-6 days in the detection of the first transmissible stages, depending on the intensity of infection of the bitten vertebrate host. Considering that a gonotrophic cycle lasts 3-4 days, the shortened EIP observed here may have significant effects on Plasmodium transmission. Keywords: Avian malaria, Plasmodium, Extrinsic Incubation Period, EIP, Transmission, Overdispersion