Multiple blood feeding in mosquitoes shortens the Plasmodium falciparum incubation period and increases malaria transmission potential

Abstract

Many mosquito species, including the major malaria vector Anopheles gambiae, naturally undergo multiple reproductive cycles of blood feeding, egg development and egg laying in their lifespan. Such complex mosquito behavior is regularly overlooked when mosquitoes are experimentally infected with malaria parasites, limiting our ability to accurately describe potential effects on transmission. Here, we examine how Plasmodium falciparum development and transmission potential is impacted when infected mosquitoes feed an additional time. We measured P. falciparum oocyst size and performed sporozoite time course analyses to determine the parasite’s extrinsic incubation period (EIP), i.e. the time required by parasites to reach infectious sporozoite stages, in An. gambiae females blood fed either once or twice. An additional blood feed at 3 days post infection drastically accelerates oocyst growth rates, causing earlier sporozoite accumulation in the salivary glands, thereby shortening the EIP (reduction of 2.3 ± 0.4 days). Moreover, parasite growth is further accelerated in transgenic mosquitoes with reduced reproductive capacity, which mimic genetic modifications currently proposed in population suppression gene drives. We incorporate our shortened EIP values into a measure of transmission potential, the basic reproduction number R0, and find the average R0 is higher (range: 10.1%–12.1% increase) across sub-Saharan Africa than when using traditional EIP measurements. These data suggest that malaria elimination may be substantially more challenging and that younger mosquitoes or those with reduced reproductive ability may provide a larger contribution to infection than currently believed. Our findings have profound implications for current and future mosquito control interventions.

Frequency matters: How successive feeding episodes by blood-feeding insect vectors influences disease transmission

“…In addition to the impacts on immune recognition of Plasmodium oocysts associated with an additional blood meal, several recent studies have demonstrated that an additional feeding can also influence parasite growth [ 26 , 32 , 33 ]. In mosquitoes receiving an additional blood meal, P .…”

Antimalarials in mosquitoes overcomeAnophelesandPlasmodiumresistance to malaria control strategies

“…Regardless of the inhibitory mechanism, these results demonstrate that P. falciparum can be targeted via LLINs, IRS or ATSB throughout their development in the mosquito. This considerably increases the effective window of opportunity for a mosquito-targeted antimalarial intervention, given that even relatively modest increases in oocyst development time can significantly reduce the probability of parasite transmission due to the short mosquito lifespan (25, 45). Furthermore, slowing or preventing oocyst development could interact synergistically with both the transmission blocking effect of pre-infection antimalarial exposure, and with the life-shortening effects of insecticides.…”

Non-immune Traits Triggered by Blood Intake Impact Vectorial Competence

“…Shaw et al (2020) proved that previously infected An. gambiae females, when provided a second uninfected blood meal, present an increase in oocyst growth rates and faster accumulation of sporozoites in the salivary glands, which can indeed amplify local malaria transmission potential (Shaw et al, 2020). Therefore, this previously overlooked multiple feeding behavior is a justifiable current trend of investigation in vector-borne pathogen transmission.…”

“…Recently, it was shown that transgenic An. gambiae mosquitoes with reduced reproductive capacity have a significantly higher malaria transmission potential, due to an increase in parasite growth rates (Shaw et al, 2020). Due to the direct implications in currently proposed control strategies (e.g., eggless mosquitoes for population suppression) and the vacancy of descriptions of resource reallocation mechanisms in other insect vector species, this subject deserves a greater deal of attention in the field.…”

“…Interestingly, the development of the malaria parasite seems to equally affect and be affected by frequent blood meals, which accelerate oocyst maturation and sporozoite development (Beier et al, 1989;Ponnudurai et al, 1989), and are induced by pathogen-vector manipulation to further enhance transmission (Cator et al, 2012). Shaw et al (2020) proved that previously infected An. gambiae females, when provided a second uninfected blood meal, present an increase in oocyst growth rates and faster accumulation of sporozoites in the salivary glands, which can indeed amplify local malaria transmission potential (Shaw et al, 2020).…”