Dual mechanism for bitter avoidance in Drosophila.
In flies and humans, bitter chemicals are known to inhibit sugar detection, but the adaptive role of this inhibition is often overlooked. At best, this inhibition is described as contributing to the rejection of potentially toxic food, but no studies have addressed the relative importance of the direct pathway that involves activating bitter-sensitive cells versus the indirect pathway represented by the inhibition of sugar detection. Using toxins to selectively ablate or inactivate populations of bitter-sensitive cells, we assessed the behavioral responses of flies to sucrose mixed with strychnine (which activates bitter-sensitive cells and inhibits sugar detection) or with L-canavanine (which only activates bitter-sensitive cells). As expected, flies with ablated bitter-sensitive cells failed to detect L-canavanine mixed with sucrose in three different feeding assays (proboscis extension responses, capillary feeding, and two-choice assays). However, such flies were still able to avoid strychnine mixed with sucrose. By means of electrophysiological recordings, we established that bitter molecules differ in their potency to inhibit sucrose detection and that sugar-sensing inhibition affects taste cells on the proboscis and the legs. The optogenetic response of sugar-sensitive cells was not reduced by strychnine, thus suggesting that this inhibition is linked directly to sugar transduction. We postulate that sugar-sensing inhibition represents a mechanism in insects to prevent ingesting harmful substances occurring within mixtures.
Institut National de la Recherche Agronomique, Unité Mixte de Recherche (UMR) Institut d'Ecologie et des Sciences de l'Environnement de Paris, F-78026 Versailles, France, AgroParisTech, Département Sciences de la Vie et Santé, F-75231 Paris, France, CNRS, Unité mixte de Recherches UMR 9191, Evolution, Génomes, Comportement, Ecologie F-91198 Gif-sur-Yvette, France.
Alice Sarah
AS
French
Institut National de la Recherche Agronomique, Unité Mixte de Recherche (UMR) Institut d'Ecologie et des Sciences de l'Environnement de Paris, F-78026 Versailles, France, AgroParisTech, Département Sciences de la Vie et Santé, F-75231 Paris, France.
Marie-Jeanne
MJ
Sellier
Institut National de la Recherche Agronomique, Unité Mixte de Recherche (UMR) Institut d'Ecologie et des Sciences de l'Environnement de Paris, F-78026 Versailles, France, CNRS, Unité mixte de Recherches UMR 9191, Evolution, Génomes, Comportement, Ecologie F-91198 Gif-sur-Yvette, France.
Moutaz
M
Ali Agha
Institut National de la Recherche Agronomique, Unité Mixte de Recherche (UMR) Institut d'Ecologie et des Sciences de l'Environnement de Paris, F-78026 Versailles, France, CNRS, Unitmixte de Recherches UMR 9191, Evolution, Génomes, Comportement, Ecologie F-91198 Gif-sur-Yvette, France.
Ali Agha
AA
Moutaz
Institut National de la Recherche Agronomique, Unité Mixte de Recherche (UMR) Institut d'Ecologie et des Sciences de l'Environnement de Paris, F-78026 Versailles, France, AgroParisTech, Département Sciences de la Vie et Santé, F-75231 Paris, France.
Alexandra
A
Guigue
Institut National de la Recherche Agronomique, Unité Mixte de Recherche (UMR) Institut d'Ecologie et des Sciences de l'Environnement de Paris, F-78026 Versailles, France.
Marie-Ange
http://orcid.org/0000-0003-4122-2091
MA
Chabaud
Universidad Nacional del Comahue, Facultad de Ciencias Agrarias, Departamento de Estadistica, RA-8303 Cinco Saltos, Argentina.
Pablo D
http://orcid.org/0000-0003-0577-5545
PD
Reeb
CNRS, Unité mixte de Recherches UMR 9191, Evolution, Génomes, Comportement, Ecologie F-91198 Gif-sur-Yvette, France.
Aniruddha
A
Mitra
Centre National de la Recherche Scientifique (CNRS), UMR 5203, Institut de Génomique Fonctionnelle, F-34094 Montpellier, France, Institut National de la Santé et de la Recherche Médicale, U661, F-34094 Montpellier, France, Universités de Montpellier 1 and 2, UMR 5203, F-34094 Montpellier, France, and.
Yves
Y
Grau
Centre National de la Recherche Scientifique (CNRS), UMR 5203, Institut de Génomique Fonctionnelle, F-34094 Montpellier, France, Institut National de la Santé et de la Recherche Médicale, U661, F-34094 Montpellier, France, Universités de Montpellier 1 and 2, UMR 5203, F-34094 Montpellier, France, and.
Laurent
http://orcid.org/0000-0003-1034-2955
L
Soustelle
Institut National de la Recherche Agronomique, Unité Mixte de Recherche (UMR) Institut d'Ecologie et des Sciences de l'Environnement de Paris, F-78026 Versailles, France, AgroParisTech, Département Sciences de la Vie et Santé, F-75231 Paris, France, CNRS, Unité mixte de Recherches UMR 9191, Evolution, Génomes, Comportement, Ecologie F-91198 Gif-sur-Yvette, France frederic.marion-poll@legs.cnrs-gif.fr.
Frédéric
http://orcid.org/0000-0001-6824-0180
F
Marion-Poll
D000818:Animals; D001362:Avoidance Learning / Q000502:physiology*; D001522:Behavior, Animal / Q000502:physiology; D004331:Drosophila melanogaster / Q000502:physiology*; D005121:Extremities / Q000294:innervation / Q000502:physiology; D005260:Female; D062308:Optogenetics; D012243:Rhodopsin / Q000502:physiology; D058618:Sensilla / Q000502:physiology; D011984:Sensory Receptor Cells / Q000502:physiology; D013268:Stimulation, Chemical; D013649:Taste / Q000502:physiology*
D012243:Rhodopsin
Drosophila; behavior; bitter; electrophysiology; mixture interaction; sweet