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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

The effect of blood feeding on the cumulative proportional survival of female mosquitoes challenged with heat-killed E. coli.Control females received bloodmeals every 4 days while treatment females skipped the 2nd and 3rd bloodmeals during the period associated with down-regulated feeding behaviour. When not on bloodmeals, females were maintained on 2.5% sugar solution. Female survival was individually tracked. Each treatment group contained 100 females and the experiment was replicated twice (mean shown for total of 400 females, 200 females per treatment group). Red shading indicates the extrinsic incubation period of P. falciparum at 27 °C36. Stars below control and above treatment line indicate that treatment received a bloodmeal. Error bars represent 1 SE. Survival was compared using a Cox Proportional Hazards Test.
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f3: The effect of blood feeding on the cumulative proportional survival of female mosquitoes challenged with heat-killed E. coli.Control females received bloodmeals every 4 days while treatment females skipped the 2nd and 3rd bloodmeals during the period associated with down-regulated feeding behaviour. When not on bloodmeals, females were maintained on 2.5% sugar solution. Female survival was individually tracked. Each treatment group contained 100 females and the experiment was replicated twice (mean shown for total of 400 females, 200 females per treatment group). Red shading indicates the extrinsic incubation period of P. falciparum at 27 °C36. Stars below control and above treatment line indicate that treatment received a bloodmeal. Error bars represent 1 SE. Survival was compared using a Cox Proportional Hazards Test.

Mentions: These conclusions do not alter the fact that the malaria parasites might benefit from these changes. Therefore, we quantified the potential impact of altered feeding behaviour for malaria transmission potential. Specifically, we examined the significance of reduced mosquito feeding and associated mortality during the early, non-infectious stages for malaria transmission potential. Bloodfeeding is known to be costly to uninfected mosquitoes1516, but its effect on infected or immune challenged mosquitoes remains unexplored. Immune-challenged females were split into two groups, one that was bloodfed at a regular 4-day cycle and one that was not offered bloodmeals during the second and third cycles (days 4 and 8, consistent with the ‘manipulation’ phenotype). We found that skipping bloodmeals led to a significant increase in survival (Cox Regression, z = 2.37, P = 0.02), doubling the number of mosquitoes alive at the fourth and fifth feeding cycles when, in infected mosquitoes, parasites would have completed development and could potentially be transmitted (Fig. 3). Given that feeding and reproductive costs (e.g. feeding-associated mortality from defensive host behaviour and flights to shuttle between hosts and oviposition sites) are likely higher in the field than under benign laboratory conditions, these results confirm the potential importance of the altered feeding phenotype for malaria transmission. Future work quantifying the effect of altered feeding using local vector-parasite pairings under field conditions, will further clarify effect on transmission. However, this simple experiment demonstrates the need to better understand this phenomenon and its mechanisms.


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)

The effect of blood feeding on the cumulative proportional survival of female mosquitoes challenged with heat-killed E. coli.Control females received bloodmeals every 4 days while treatment females skipped the 2nd and 3rd bloodmeals during the period associated with down-regulated feeding behaviour. When not on bloodmeals, females were maintained on 2.5% sugar solution. Female survival was individually tracked. Each treatment group contained 100 females and the experiment was replicated twice (mean shown for total of 400 females, 200 females per treatment group). Red shading indicates the extrinsic incubation period of P. falciparum at 27 °C36. Stars below control and above treatment line indicate that treatment received a bloodmeal. Error bars represent 1 SE. Survival was compared using a Cox Proportional Hazards Test.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f3: The effect of blood feeding on the cumulative proportional survival of female mosquitoes challenged with heat-killed E. coli.Control females received bloodmeals every 4 days while treatment females skipped the 2nd and 3rd bloodmeals during the period associated with down-regulated feeding behaviour. When not on bloodmeals, females were maintained on 2.5% sugar solution. Female survival was individually tracked. Each treatment group contained 100 females and the experiment was replicated twice (mean shown for total of 400 females, 200 females per treatment group). Red shading indicates the extrinsic incubation period of P. falciparum at 27 °C36. Stars below control and above treatment line indicate that treatment received a bloodmeal. Error bars represent 1 SE. Survival was compared using a Cox Proportional Hazards Test.
Mentions: These conclusions do not alter the fact that the malaria parasites might benefit from these changes. Therefore, we quantified the potential impact of altered feeding behaviour for malaria transmission potential. Specifically, we examined the significance of reduced mosquito feeding and associated mortality during the early, non-infectious stages for malaria transmission potential. Bloodfeeding is known to be costly to uninfected mosquitoes1516, but its effect on infected or immune challenged mosquitoes remains unexplored. Immune-challenged females were split into two groups, one that was bloodfed at a regular 4-day cycle and one that was not offered bloodmeals during the second and third cycles (days 4 and 8, consistent with the ‘manipulation’ phenotype). We found that skipping bloodmeals led to a significant increase in survival (Cox Regression, z = 2.37, P = 0.02), doubling the number of mosquitoes alive at the fourth and fifth feeding cycles when, in infected mosquitoes, parasites would have completed development and could potentially be transmitted (Fig. 3). Given that feeding and reproductive costs (e.g. feeding-associated mortality from defensive host behaviour and flights to shuttle between hosts and oviposition sites) are likely higher in the field than under benign laboratory conditions, these results confirm the potential importance of the altered feeding phenotype for malaria transmission. Future work quantifying the effect of altered feeding using local vector-parasite pairings under field conditions, will further clarify effect on transmission. However, this simple experiment demonstrates the need to better understand this phenomenon and its mechanisms.

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