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The olfactory basis of orchid pollination by mosquitoes

Mosquitoes are important vectors of disease and require sources of carbohydrates for reproduction and survival. Unlike host-related behaviors of mosquitoes, comparatively less is understood about the mechanisms involved in nectar-feeding decisions, or how this sensory information is processed in the...

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Autores principales: Lahondère, Chloé, Vinauger, Clément, Okubo, Ryo P., Wolff, Gabriella H., Chan, Jeremy K., Akbari, Omar S., Riffell, Jeffrey A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6955360/
https://www.ncbi.nlm.nih.gov/pubmed/31871198
http://dx.doi.org/10.1073/pnas.1910589117
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author Lahondère, Chloé
Vinauger, Clément
Okubo, Ryo P.
Wolff, Gabriella H.
Chan, Jeremy K.
Akbari, Omar S.
Riffell, Jeffrey A.
author_facet Lahondère, Chloé
Vinauger, Clément
Okubo, Ryo P.
Wolff, Gabriella H.
Chan, Jeremy K.
Akbari, Omar S.
Riffell, Jeffrey A.
author_sort Lahondère, Chloé
collection PubMed
description Mosquitoes are important vectors of disease and require sources of carbohydrates for reproduction and survival. Unlike host-related behaviors of mosquitoes, comparatively less is understood about the mechanisms involved in nectar-feeding decisions, or how this sensory information is processed in the mosquito brain. Here we show that Aedes spp. mosquitoes, including Aedes aegypti, are effective pollinators of the Platanthera obtusata orchid, and demonstrate this mutualism is mediated by the orchid’s scent and the balance of excitation and inhibition in the mosquito’s antennal lobe (AL). The P. obtusata orchid emits an attractive, nonanal-rich scent, whereas related Platanthera species—not visited by mosquitoes—emit scents dominated by lilac aldehyde. Calcium imaging experiments in the mosquito AL revealed that nonanal and lilac aldehyde each respectively activate the LC2 and AM2 glomerulus, and remarkably, the AM2 glomerulus is also sensitive to N,N-diethyl-meta-toluamide (DEET), a mosquito repellent. Lateral inhibition between these 2 glomeruli reflects the level of attraction to the orchid scents. Whereas the enriched nonanal scent of P. obtusata activates the LC2 and suppresses AM2, the high level of lilac aldehyde in the other orchid scents inverts this pattern of glomerular activity, and behavioral attraction is lost. These results demonstrate the ecological importance of mosquitoes beyond operating as disease vectors and open the door toward understanding the neural basis of mosquito nectar-seeking behaviors.
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spelling pubmed-69553602020-01-14 The olfactory basis of orchid pollination by mosquitoes Lahondère, Chloé Vinauger, Clément Okubo, Ryo P. Wolff, Gabriella H. Chan, Jeremy K. Akbari, Omar S. Riffell, Jeffrey A. Proc Natl Acad Sci U S A PNAS Plus Mosquitoes are important vectors of disease and require sources of carbohydrates for reproduction and survival. Unlike host-related behaviors of mosquitoes, comparatively less is understood about the mechanisms involved in nectar-feeding decisions, or how this sensory information is processed in the mosquito brain. Here we show that Aedes spp. mosquitoes, including Aedes aegypti, are effective pollinators of the Platanthera obtusata orchid, and demonstrate this mutualism is mediated by the orchid’s scent and the balance of excitation and inhibition in the mosquito’s antennal lobe (AL). The P. obtusata orchid emits an attractive, nonanal-rich scent, whereas related Platanthera species—not visited by mosquitoes—emit scents dominated by lilac aldehyde. Calcium imaging experiments in the mosquito AL revealed that nonanal and lilac aldehyde each respectively activate the LC2 and AM2 glomerulus, and remarkably, the AM2 glomerulus is also sensitive to N,N-diethyl-meta-toluamide (DEET), a mosquito repellent. Lateral inhibition between these 2 glomeruli reflects the level of attraction to the orchid scents. Whereas the enriched nonanal scent of P. obtusata activates the LC2 and suppresses AM2, the high level of lilac aldehyde in the other orchid scents inverts this pattern of glomerular activity, and behavioral attraction is lost. These results demonstrate the ecological importance of mosquitoes beyond operating as disease vectors and open the door toward understanding the neural basis of mosquito nectar-seeking behaviors. National Academy of Sciences 2020-01-07 2019-12-23 /pmc/articles/PMC6955360/ /pubmed/31871198 http://dx.doi.org/10.1073/pnas.1910589117 Text en Copyright © 2020 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle PNAS Plus
Lahondère, Chloé
Vinauger, Clément
Okubo, Ryo P.
Wolff, Gabriella H.
Chan, Jeremy K.
Akbari, Omar S.
Riffell, Jeffrey A.
The olfactory basis of orchid pollination by mosquitoes
title The olfactory basis of orchid pollination by mosquitoes
title_full The olfactory basis of orchid pollination by mosquitoes
title_fullStr The olfactory basis of orchid pollination by mosquitoes
title_full_unstemmed The olfactory basis of orchid pollination by mosquitoes
title_short The olfactory basis of orchid pollination by mosquitoes
title_sort olfactory basis of orchid pollination by mosquitoes
topic PNAS Plus
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6955360/
https://www.ncbi.nlm.nih.gov/pubmed/31871198
http://dx.doi.org/10.1073/pnas.1910589117
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