Abstract
The efficiency of malaria parasite development within mosquito vectors (sporogony) is a critical determinant of transmission. Sporogony is thought to be controlled by environmental conditions and mosquito/parasite genetic factors, with minimal contribution from mosquito behaviour during the period of parasite development. We tested this assumption by investigating whether successful sporogony of Plasmodium falciparum parasites through to human-infectious transmission stages is influenced by the host species upon which infected mosquitoes feed. Studies were conducted on two major African vector species that generally are found to differ in their innate host preferences: Anopheles arabiensis and An. gambiae sensu stricto. We show that the proportion of vectors developing transmissible infections (sporozoites) was influenced by the source of host blood consumed during sporogony. The direction of this effect was associated with the innate host preference of vectors: higher sporozoite prevalences were generated in the usually human-specialist An. gambiae s.s. feeding on human compared to cow blood, whereas the more zoophilic An. arabiensis had significantly higher prevalences after feeding on cow blood. The potential epidemiological implications of these results are discussed.
Highlights
In the host feeding patterns of these vector species, overall the general trend of a high preference for humans by An. gambiae s.s. and An. coluzzii, and for cattle by An. arabiensis, holds across a broad range of settings
The potential impact of mosquito host choice on malaria parasite sporogony is unknown. This study addressed these knowledge gaps by investigating if: (1) the host species from which malaria-infected mosquitoes feed influences parasite sporogonic success; and (2) the efficiency of P. falciparum malaria parasite sporogony varies between An. arabiensis (Ifakara) and An. gambiae s.s. (Keele)
Of the 1440 mosquitoes fed on malaria-infected blood (720 for each vector species; Supplementary Table S1), the proportion infected with oocysts across replicates ranged from 71–86% in An. arabiensis, and 54–71% in An. gambiae s.s. (Fig. 1a)
Summary
In the host feeding patterns of these vector species (e.g. an An. gambiae s.s. population which prefers feeding on dogs[29], an An. arabiensis population that feeds exclusively on people28), overall the general trend of a high preference for humans by An. gambiae s.s. and An. coluzzii, and for cattle by An. arabiensis, holds across a broad range of settings. Variation in feeding behaviour within these malaria vectors has potential to influence malaria transmission in another way: the type of host blood consumed by infected mosquitoes could influence the quality and quantity of resources available to developing parasites, and their likelihood of onward transmission. Prediction of the epidemiological consequences of shifts in vector species composition will require an understanding of both how vectors differ in their innate susceptibility to infection, and how their subsequent behaviour and fitness during sporogony influences their likelihood of developing transmission stage parasites. The potential impact of mosquito host choice on malaria parasite sporogony is unknown This study addressed these knowledge gaps by investigating if: (1) the host species from which malaria-infected mosquitoes feed (human or cattle) influences parasite sporogonic success; and (2) the efficiency of P. falciparum malaria parasite sporogony varies between An. arabiensis (Ifakara) and An. gambiae s.s. Assessing the contribution of mosquito host choice and vector species to parasite sporogony has particular relevance for understanding the potential epidemiological consequences of recently reported changes in the ecology of African malaria vectors
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