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A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone

Nature volume 446, pages 542–546 (2007)Cite this article

Abstract

Insects, like many other animals, use sex pheromones to coordinate their reproductive behaviours1. Volatile pheromones are detected by odorant receptors expressed in olfactory receptor neurons (ORNs). Whereas fruit odours typically activate multiple ORN classes2, pheromones are thought to act through single dedicated classes of ORN3. This model predicts that activation of such an ORN class should be sufficient to trigger the appropriate behavioural response. Here we show that the Drosophila melanogaster male-specific pheromone 11-cis-vaccenyl acetate (cVA) acts through the receptor Or67d to regulate both male and female mating behaviour. Mutant males that lack Or67d inappropriately court other males, whereas mutant females are less receptive to courting males. These data suggest that cVA has opposite effects in the two sexes: inhibiting mating behaviour in males but promoting mating behaviour in females. Replacing Or67d with moth pheromone receptors renders these ORNs sensitive to the corresponding moth pheromones. In such flies, moth pheromones elicit behavioural responses that mimic the normal response to cVA. Thus, activation of a single ORN class is both necessary and sufficient to mediate behavioural responses to the Drosophila sex pheromone cVA.

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Figure 1: Or67d mediates physiological responses to cVA.
Figure 2: Or67d functions in male and female mating behaviours.
Figure 3: Or67d mediates cVA-induced courtship suppression.
Figure 4: Artificial activation of Or67d ORNs mimics cVA responses.

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Acknowledgements

We thank A. Couto and M. Alenius for the initial identification of Or67d expression in the T1 ORNs and for the images in Fig. 1b, c; K. Golic for targeting stocks; Y. Banno for the Bombyx mori genomic DNA; J. Krieger for the HR13 cDNA and the supply of bombykol used in our initial experiments; R. Fuchs and Azra Kurtovic for technical assistance; G. Jefferis, A. Keene and M. Leyssen for comments on the manuscript; and G. Jefferis and L. Luo for communicating unpublished data. A.W. was supported in part by a postdoctoral fellowship from the Swiss National Science Foundation. This work was funded by Boehringer Ingelheim GmbH.

Author Contributions A.K. and B.J.D. generated the Or67d knock-in alleles. A.K. performed the behavioural analysis with assistance from A.W., who also carried out all the electrophysiological experiments. All three authors contributed to the experimental design and preparation of the manuscript.

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  1. Amina Kurtovic and Alexandre Widmer: These authors contributed equally to this work.

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  1. Research Institute of Molecular Pathology (IMP), Dr Bohr-gasse 7, A-1030 Vienna, Austria,

    Amina Kurtovic, Alexandre Widmer & Barry J. Dickson

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Correspondence to Barry J. Dickson.

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Kurtovic, A., Widmer, A. & Dickson, B. A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446, 542–546 (2007). https://doi.org/10.1038/nature05672

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