Sensory Discrimination of Blood and Floral Nectar by Aedes aegypti Mosquitoes

Blood-feeding mosquitoes survive by feeding on nectar for metabolic energy but require a blood meal to develop eggs. Aedes aegypti females must accurately discriminate blood and nectar because each meal promotes mutually exclusive feeding programs with distinct sensory appendages, meal sizes, digest...

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Published inNeuron (Cambridge, Mass.) Vol. 108; no. 6; pp. 1163 - 1180.e12
Main Authors Jové, Veronica, Gong, Zhongyan, Hol, Felix J.H., Zhao, Zhilei, Sorrells, Trevor R., Carroll, Thomas S., Prakash, Manu, McBride, Carolyn S., Vosshall, Leslie B.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 23.12.2020
Elsevier Limited
Elsevier
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Summary:Blood-feeding mosquitoes survive by feeding on nectar for metabolic energy but require a blood meal to develop eggs. Aedes aegypti females must accurately discriminate blood and nectar because each meal promotes mutually exclusive feeding programs with distinct sensory appendages, meal sizes, digestive tract targets, and metabolic fates. We investigated the syringe-like blood-feeding appendage, the stylet, and discovered that sexually dimorphic stylet neurons taste blood. Using pan-neuronal calcium imaging, we found that blood is detected by four functionally distinct stylet neuron classes, each tuned to specific blood components associated with diverse taste qualities. Stylet neurons are insensitive to nectar-specific sugars and respond to glucose only in the presence of additional blood components. The distinction between blood and nectar is therefore encoded in specialized neurons at the very first level of sensory detection in mosquitoes. This innate ability to recognize blood is the basis of vector-borne disease transmission to millions of people worldwide. •Neurons in the syringe-like stylet are the first to detect blood as mosquitoes bite•The taste of blood is integrated across taste qualities and stylet neuron subsets•Subsets are tuned to distinct blood components and insensitive to floral sugars•Polymodal taste quality integration assigns a blood-specific context to glucose Jové et al. characterize specialized blood-feeding sensory neurons in female Aedes aegypti mosquitoes and demonstrate that they encode the distinction between blood and floral nectar. Polymodal integrator neurons respond to glucose only in the presence of additional blood components, allowing mosquitoes to discriminate these two appetizing food sources.
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AUTHOR CONTRIBUTIONS
V.J. performed all experiments in the paper with the following exceptions: F.J.H.H. (Figure 2, Video 1); Z.G. (Figure 1E,F,J, Figure S1D, Figure 7B,C); T.R.S. (Figure 6C–F; Figure S7C,D; Video 6); T.S.C. wrote the live imaging analysis pipeline code and performed statistical analyses in Figure S5. Z.G. and V.J. together created the Ir7a-QF2, Gr4-QF2, QUAS-TRPV1 strains and performed experiments in Figure 1I, Figure S1A–C, Figure 3A,B, Figure S2B,C,F,G, Figure 6A,B, and Figure 7E; Z.Z. and C.S.M. shared their unpublished Brp-QF2w strain. M.P. supervised and collaborated with F.J.H.H. V.J. and L.B.V. together conceived the study, designed the figures, and wrote the paper with input from all authors.
These authors contributed equally
ISSN:0896-6273
1097-4199
DOI:10.1016/j.neuron.2020.09.019