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Immune response and insulin signalling alter mosquito feeding behaviour to enhance malaria transmission potential.

Cator LJ, Pietri JE, Murdock CC, Ohm JR, Lewis EE, Read AF, Luckhart S, Thomas MB - Sci Rep (2015)

Bottom Line: 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.Leveraging these changes in physiology, behaviour and life history could promote effective and sustainable control of female mosquitoes responsible for transmission.

View Article: PubMed Central - PubMed

Affiliation: Grand Challenges in Ecosystem and Environment, Department of Life Sciences, Imperial College London, Silwood Park.

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.

No MeSH data available.


Related in: MedlinePlus

Effects of timing and dose of immune challenge on host-seeking behaviour.A. Immune challenge coinciding with the bloodmeal generates the mosquito host-seeking patterns associated with malaria parasite infection. The previously described ‘manipulation’ phenotype is only recapitulated when females are challenged immediately following the bloodmeal (HK-0, n = 163). Immune challenge alone (HK, n = 156) or occurring later (HK-2 days, n = 145 and HK-4 days, n = 148) do not generate the same phenotype. Controls included unmanipulated females (UC, n = 78) and females which only received a bloodmeal (BC, n = 157) This experiment was replicated twice. B. The effect of dose of heat-killed E. coli on behaviour. Dose had no effect on the duration or time of decreased response period (Fig. S2). Control, n = 391, Low, n = 227, Medium, n = 209, High, n = 221. This experiment was replicated three times. Error bars represent 1 SE and * indicates P < 0.05 between first and second test period within a treatment.
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f1: Effects of timing and dose of immune challenge on host-seeking behaviour.A. Immune challenge coinciding with the bloodmeal generates the mosquito host-seeking patterns associated with malaria parasite infection. The previously described ‘manipulation’ phenotype is only recapitulated when females are challenged immediately following the bloodmeal (HK-0, n = 163). Immune challenge alone (HK, n = 156) or occurring later (HK-2 days, n = 145 and HK-4 days, n = 148) do not generate the same phenotype. Controls included unmanipulated females (UC, n = 78) and females which only received a bloodmeal (BC, n = 157) This experiment was replicated twice. B. The effect of dose of heat-killed E. coli on behaviour. Dose had no effect on the duration or time of decreased response period (Fig. S2). Control, n = 391, Low, n = 227, Medium, n = 209, High, n = 221. This experiment was replicated three times. Error bars represent 1 SE and * indicates P < 0.05 between first and second test period within a treatment.

Mentions: First, we examined possible interactions between the timing of immune challenge and the bloodmeal. Female mosquitoes were given an uninfected bloodmeal and were then challenged with 200,000 heat-killed E. coli administered either immediately following the bloodmeal, 2 days, or 4 days post-bloodmeal2. The behavioural response of these mosquitoes to human host cues was compared with mosquitoes that received either a bloodmeal or immune challenge alone, or were completely unmanipulated. Behaviour was assayed at two time points coinciding with non-infectious (6–8 days post infection) and infectious (14–16 days post infection) stages of parasite development in malaria-infected mosquitoes. Behavioural changes only occurred when the bloodmeal and immune challenge were synchronous (treatment x test period, Wald χ2 = 11.753, d.f. = 5, P = 0.04, Fig. 1a). Neither immune challenge alone nor a bloodmeal alone altered host-seeking propensity compared to unmanipulated controls, and only females challenged directly after the bloodmeal exhibited a significantly different phenotype from bloodfed control females (Fig. 1a, Wald χ2 = 10.91, d.f. = 11, P < 0.01).


Immune response and insulin signalling alter mosquito feeding behaviour to enhance malaria transmission potential.

Cator LJ, Pietri JE, Murdock CC, Ohm JR, Lewis EE, Read AF, Luckhart S, Thomas MB - Sci Rep (2015)

Effects of timing and dose of immune challenge on host-seeking behaviour.A. Immune challenge coinciding with the bloodmeal generates the mosquito host-seeking patterns associated with malaria parasite infection. The previously described ‘manipulation’ phenotype is only recapitulated when females are challenged immediately following the bloodmeal (HK-0, n = 163). Immune challenge alone (HK, n = 156) or occurring later (HK-2 days, n = 145 and HK-4 days, n = 148) do not generate the same phenotype. Controls included unmanipulated females (UC, n = 78) and females which only received a bloodmeal (BC, n = 157) This experiment was replicated twice. B. The effect of dose of heat-killed E. coli on behaviour. Dose had no effect on the duration or time of decreased response period (Fig. S2). Control, n = 391, Low, n = 227, Medium, n = 209, High, n = 221. This experiment was replicated three times. Error bars represent 1 SE and * indicates P < 0.05 between first and second test period within a treatment.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4495552&req=5

f1: Effects of timing and dose of immune challenge on host-seeking behaviour.A. Immune challenge coinciding with the bloodmeal generates the mosquito host-seeking patterns associated with malaria parasite infection. The previously described ‘manipulation’ phenotype is only recapitulated when females are challenged immediately following the bloodmeal (HK-0, n = 163). Immune challenge alone (HK, n = 156) or occurring later (HK-2 days, n = 145 and HK-4 days, n = 148) do not generate the same phenotype. Controls included unmanipulated females (UC, n = 78) and females which only received a bloodmeal (BC, n = 157) This experiment was replicated twice. B. The effect of dose of heat-killed E. coli on behaviour. Dose had no effect on the duration or time of decreased response period (Fig. S2). Control, n = 391, Low, n = 227, Medium, n = 209, High, n = 221. This experiment was replicated three times. Error bars represent 1 SE and * indicates P < 0.05 between first and second test period within a treatment.
Mentions: First, we examined possible interactions between the timing of immune challenge and the bloodmeal. Female mosquitoes were given an uninfected bloodmeal and were then challenged with 200,000 heat-killed E. coli administered either immediately following the bloodmeal, 2 days, or 4 days post-bloodmeal2. The behavioural response of these mosquitoes to human host cues was compared with mosquitoes that received either a bloodmeal or immune challenge alone, or were completely unmanipulated. Behaviour was assayed at two time points coinciding with non-infectious (6–8 days post infection) and infectious (14–16 days post infection) stages of parasite development in malaria-infected mosquitoes. Behavioural changes only occurred when the bloodmeal and immune challenge were synchronous (treatment x test period, Wald χ2 = 11.753, d.f. = 5, P = 0.04, Fig. 1a). Neither immune challenge alone nor a bloodmeal alone altered host-seeking propensity compared to unmanipulated controls, and only females challenged directly after the bloodmeal exhibited a significantly different phenotype from bloodfed control females (Fig. 1a, Wald χ2 = 10.91, d.f. = 11, P < 0.01).

Bottom Line: 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.Leveraging these changes in physiology, behaviour and life history could promote effective and sustainable control of female mosquitoes responsible for transmission.

View Article: PubMed Central - PubMed

Affiliation: Grand Challenges in Ecosystem and Environment, Department of Life Sciences, Imperial College London, Silwood Park.

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.

No MeSH data available.


Related in: MedlinePlus