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Sugar-sensitive neurone responses and sugar feeding preferences influence lifespan and biting behaviours of the Afrotropical malaria mosquito, Anopheles gambiae

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Abstract

Floral nectar is the main source of carbohydrates for many insects including mosquitoes. Nonetheless, the physiological mechanisms underlying feeding on carbohydrates by the Afrotropical malaria mosquito Anopheles gambiae remain poorly understood. Here, we tested whether sugar sensitivity and sugar feeding preferences correlate with longevity in A. gambiae. We also tested whether feeding females on different sugar diets influences their biting behaviours. Electrophysiological recordings show that sugar neurones on the labella of females are most sensitive to sucrose, mixtures of glucose and fructose, and to melezitose; other sugars tested, including glucose and fructose presented alone, only weakly activate these taste neurones. Mosquitoes survive longest on sucrose, the most preferred sugar. Whereas feeding on a mixture of glucose and fructose is preferred over fructose or glucose alone, fructose supports higher longevity than either glucose or the mixture of the two hexoses. Females that had previously fed on glucose show a stronger biting response than those fed on sucrose, perhaps in an effort to compensate for their lower energetic state. These findings contribute to our understanding of the physiological basis of sugar feeding in A. gambiae and indicate how the sugar diet can affect laboratory-reared A. gambiae biting behaviours.

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Acknowledgments

Radu Slobodeanu, Institute of Mathematics, University of Neuchâtel, is cordially acknowledged for his help with statistics. Our gratitude is also extended to Thomas Kröber, Animal Physiology Laboratory, University of Neuchâtel, for improvements to the biting assay in collaboration with Virgile Rumo, HE-ARC, Neuchâtel and Daniel Varidel, Technical Service, University of Neuchâtel. All members of the Animal Physiology Laboratory are acknowledged, particularly Martine Bourquin, for her help in mosquito rearing and Charles Chappuis, Alexandre Gurba as well as two anonymous reviewers for their worthwhile suggestions for improvements to the manuscript. The authors wish to thank Geraldine Wright, Institute of Neuroscience, Newcastle University, and Andrew McMullin, Institute of Biology, University of Neuchâtel for help with a revision of the manuscript. The Guinea pigs used for the mosquito rearing were maintained in an animal house under permit, in compliance with Swiss Federal Regulations. This research was funded by the Swiss National Science Foundation [Grant no. 138207].

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Correspondence to Patrick M. Guerin.

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359_2015_978_MOESM1_ESM.pdf

Supplementary material 1 Mean ± s.e.m. feeding preferences by male A. gambiae offered sugar solutions in paired choice tests: 584 mM fructose versus 584 mM glucose; 584 mM glucose or 584 mM fructose versus water; 292 mM glucose with 292 mM fructose versus 584 mM glucose or 584 mM fructose; 292 mM sucrose versus 292 mM melezitose, 584 mM glucose or 584 mM fructose; 292 mM sucrose versus 292 mM glucose with 292 mM fructose or the same solution of 292 mM sucrose. Each choice test consisted of 4–7 replicates with 19 ± 3 males in each. Percentages of mosquitoes tested that fed on both solutions are in grey (PDF 16 kb)

359_2015_978_MOESM2_ESM.pdf

Supplementary material 2 Survival curves in days for male A. gambiae (between 82 and 99 mosquitoes tested per treatment) fed on 584 mM fructose, 584 mM glucose, 292 mM glucose with 292 mM fructose, 292 mM sucrose or water (PDF 19 kb)

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Kessler, S., Vlimant, M. & Guerin, P.M. Sugar-sensitive neurone responses and sugar feeding preferences influence lifespan and biting behaviours of the Afrotropical malaria mosquito, Anopheles gambiae . J Comp Physiol A 201, 317–329 (2015). https://doi.org/10.1007/s00359-015-0978-7

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