Abstract
Malaria parasites alter mosquito feeding behaviour in a way that enhances parasite transmission. This is widely considered a prime example of manipulation of host behaviour to increase onward transmission, but transient immune challenge in the absence of parasites can induce the same behavioural phenotype. Here, we show that alterations in feeding behaviour depend on the timing and dose of immune challenge relative to blood ingestion and that these changes are functionally linked to changes in insulin signalling in the mosquito gut. These results suggest that altered phenotypes derive from insulin signalling-dependent host resource allocation among immunity, blood feeding, and reproduction in a manner that is not specific to malaria parasite infection. We measured large increases in mosquito survival and subsequent transmission potential when feeding patterns are altered. Leveraging these changes in physiology, behaviour and life history could promote effective and sustainable control of female mosquitoes responsible for transmission.
Highlights
Clarify the role of the parasite in driving the behavioural response and reveal potential novel targets for genetic manipulation of mosquito host-seeking behaviour
When we investigated the mechanism of this dynamic relationship between bloodmeal and immune challenge, we found that both heat-killed E. coli and the human malaria parasite, P. falciparum, trigger changes in insulin signaling in the mosquito midgut which are functionally linked to feeding propensity
We challenged female Anopheles stephensi by injecting heat-killed E. coli immediately following the first bloodmeal[2]. This technique has been shown to generate both the behavioural and neurophysiological phenotypes associated with malaria parasite infection[2], and represents a more tractable experimental approach for evaluating mosquito behaviour in the lab
Summary
We began by dissecting the relationship between immune challenge and bloodfeeding. As in previous work, we challenged female Anopheles stephensi by injecting heat-killed E. coli immediately following the first bloodmeal[2]. Behavioural change depended on both the dose and timing of immune challenge relative to the bloodmeal, suggesting possible trade-offs or constraints between immune response, digestion, and potentially reproduction With this new insight, we set out to characterize the regulation of the altered host-seeking behaviour. To confirm whether insulin signalling plays a role in the Plasmodium parasite-triggered behavioural changes, we measured expression levels of ILP3 and ILP4 in the midguts of P. falciparum-infected An. stephensi at times consistent with altered host-seeking behaviour. Previous work in mosquitoes has demonstrated that ILPs have been shown to play a role in the regulation of vitellogenesis and bloodmeal digestion[22,23] It appears that in An. stephensi there is an inhibition of insulin signalling activity in the migut in association with immune activation and that this suppression dramatically alters mosquito life history and transmission potential. Insulin signalling pathways may be used to target the parasite both directly via mosquito immunity and indirectly by altering mosquito feeding behaviour to curtail transmission potential
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