Flying insects are well known for airborne odour tracking and have evolved diverse chemoreceptors. While ionotropic receptors (IRs) are found across protostomes, insect odorant receptors (ORs) have only been identified in winged insects. We therefore hypothesized that the unique signal transduction of ORs offers an advantage for odour localization in flight. Using Drosophila, we found expression and increased activity of the intracellular signalling protein PKC in antennal sensilla following odour stimulation. Odour stimulation also enhanced phosphorylation of the OR co-receptor Orco in vitro, while site-directed mutation of Orco or mutations in PKC subtypes reduced the sensitivity and dynamic range of OR-expressing neurons in vivo, but not IR-expressing neurons. We ultimately show that these mutations reduce competence for odour localization of flies in flight. We conclude that intracellular regulation of OR sensitivity is necessary for efficient odour localization, which suggests a mechanistic advantage for the evolution of the OR complex in flying insects.
The authors declare no competing or financial interests.
M.N.G., S.L.-L., S.B.O., D.W. and B.S.H. conceived and designed the study; M.N.G. performed the experiments and analysed the data; M.N.G., S.B.O. and I.K. performed and analysed the wind-tunnel experiments; M.N.G., S.B.O., D.W. and B.S.H. wrote the manuscript; M.T. and M.K. performed and analysed the Flywalk experiment; R.A.F. helped with western blotting. All authors discussed and agreed on the content of the paper.
This study was supported by the Max Planck Society.
Supplementary information available online at http://jeb.biologists.org/lookup/doi/10.1242/jeb.143396.supplemental
- Received May 17, 2016.
- Accepted August 22, 2016.
- © 2016. Published by The Company of Biologists Ltd