Drosophila Tracks Carbon Dioxide in Flight

• Published in: Current biology 2013-02, Vol.23 (4), p.301-306
• Main Authors: Wasserman, Sara, Salomon, Alexandra, Frye, Mark A.
• Format: Article
• Language: English
• Subjects: adults; Animals; Arthropod Antennae - physiology; Behavior, Animal - physiology; Carbon Dioxide; Cues; Culicidae; Drosophila melanogaster; Drosophila melanogaster - metabolism; Drosophila melanogaster - physiology; Drosophila Proteins - genetics; Drosophila Proteins - metabolism; Environment; flight; Flight, Animal - physiology; host seeking; Magnetic Fields; mutation; neurons; octopamine; Octopamine - metabolism; Olfactory Pathways - metabolism; Receptors, Ionotropic Glutamate - genetics; Receptors, Ionotropic Glutamate - metabolism; Receptors, Odorant; Smell - physiology; walking
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2012.12.038

Carbon dioxide (CO2) elicits an attractive host-seeking response from mosquitos [1–3] yet is innately aversive to Drosophila melanogaster [4, 5] despite being a plentiful byproduct of attractive fermenting food sources. Prior studies used walking flies exclusively, yet adults track distant food sources on the wing [6]. Here we show that a fly tethered within a magnetic field allowing free rotation about the yaw axis [7] actively seeks a narrow CO2 plume during flight. Genetic disruption of the canonical CO2-sensing olfactory neurons does not alter in-flight attraction to CO2; however, antennal ablation and genetic disruption of the Ir64a acid sensor do. Surprisingly, mutation of the obligate olfactory coreceptor (Orco [8]) does not abolish CO2 aversion during walking [4] yet eliminates CO2 tracking in flight. The biogenic amine octopamine regulates critical physiological processes during flight [9–11], and blocking synaptic output from octopamine neurons inverts the valence assigned to CO2 and elicits an aversive response in flight. Combined, our results suggest that a novel Orco-mediated olfactory pathway that gains sensitivity to CO2 in flight via changes in octopamine levels, along with Ir64a, quickly switches the valence of a key environmental stimulus in a behavioral-state-dependent manner. ► During flight, flies actively orient toward a narrow CO2 plume ► CO2 tracking requires both Ir64a and the olfactory coreceptor Orco ► Synaptic output from octopamine neurons mediates CO2 tracking in flight