Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Hierarchical chemosensory regulation of male-male social interactions in Drosophila

Abstract

Pheromones regulate male social behaviors in Drosophila, but the identities and behavioral role(s) of these chemosensory signals, and how they interact, are incompletely understood. We found that (z)-7-tricosene, a male-enriched cuticular hydrocarbon that was previously shown to inhibit male-male courtship, was essential for normal levels of aggression. The mechanisms by which (z)-7-tricosene induced aggression and suppressed courtship were independent, but both required the gustatory receptor Gr32a. Sensitivity to (z)-7-tricosene was required for the aggression-promoting effect of 11-cis-vaccenyl acetate (cVA), an olfactory pheromone, but (z)-7-tricosene sensitivity was independent of cVA. (z)-7-tricosene and cVA therefore regulate aggression in a hierarchical manner. Furthermore, the increased courtship caused by depletion of male cuticular hydrocarbons was suppressed by a mutation in the olfactory receptor Or47b. Thus, male social behaviors are controlled by gustatory pheromones that promote aggression and suppress courtship, and whose influences are dominant to olfactory pheromones that enhance these behaviors.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Male cuticular hydrocarbons are important for the normal balance of male-male social behaviors.
Figure 2: (z)-7-tricosene reciprocally regulates male-male aggression and courtship.
Figure 3: Gr32a mediates the behavioral effects of (z)-7-tricosene and permits the aggression-promoting effect of cVA.
Figure 4: Or47b is required for elevated male-male courtship caused by depletion of male cuticular hydrocarbons.

Similar content being viewed by others

References

  1. Vrontou, E., Nilsen, S.P., Demir, E., Kravitz, E.A. & Dickson, B.J. fruitless regulates aggression and dominance in Drosophila. Nat. Neurosci. 9, 1469–1471 (2006).

    Article  CAS  Google Scholar 

  2. Dankert, H., Wang, L., Hoopfer, E.D., Anderson, D.J. & Perona, P. Automated monitoring and analysis of social behavior in Drosophila. Nat. Methods 6, 297–303 (2009).

    Article  CAS  Google Scholar 

  3. Krstic, D., Boll, W. & Noll, M. Sensory integration regulating male courtship behavior in Drosophila. PLoS One 4, e4457 (2009).

    Article  Google Scholar 

  4. Miyamoto, T. & Amrein, H. Suppression of male courtship by a Drosophila pheromone receptor. Nat. Neurosci. 11, 874–876 (2008).

    Article  CAS  Google Scholar 

  5. Moon, S.J., Lee, Y., Jiao, Y. & Montell, C. A Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship. Curr. Biol. 19, 1623–1627 (2009).

    Article  CAS  Google Scholar 

  6. Billeter, J.-C., Atallah, J., Krupp, J.J., Millar, J.G. & Levine, J.D. Specialized cells tag sexual and species identity in Drosophila melanogaster. Nature 461, 987–991 (2009).

    Article  CAS  Google Scholar 

  7. Savarit, F., Sureau, G., Cobb, M. & Ferveur, J.-F. Genetic elimination of known pheromones reveals the fundamental chemical bases of mating and isolation in Drosophila. Proc. Natl. Acad. Sci. USA 96, 9015–9020 (1999).

    Article  CAS  Google Scholar 

  8. Ferveur, J.-F. Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav. Genet. 35, 279–295 (2005).

    Article  Google Scholar 

  9. Fernández, M.P. et al. Pheromonal and behavioral cues trigger male-to-female aggression in Drosophila. PLoS Biol. 8, e1000541 (2010).

    Article  Google Scholar 

  10. Kurtovic, A., Widmer, A. & Dickson, B.J. A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446, 542–546 (2007).

    Article  CAS  Google Scholar 

  11. Ha, T.S. & Smith, D.P. A pheromone receptor mediates 11-cis-vaccenyl acetate-induced responses in Drosophila. J. Neurosci. 26, 8727–8733 (2006).

    Article  CAS  Google Scholar 

  12. van der Goes van Naters, W. & Carlson, J.R. Receptors and neurons for fly odors in Drosophila. Curr. Biol. 17, 606–612 (2007).

    Article  CAS  Google Scholar 

  13. Wang, L. & Anderson, D.J. Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 463, 227–231 (2010).

    Article  CAS  Google Scholar 

  14. Krupp, J.J. et al. Social experience modifies pheromone expression and mating behavior in male Drosophila melanogaster. Curr. Biol. 18, 1373–1383 (2008).

    Article  CAS  Google Scholar 

  15. Everaerts, C., Farine, J.-P., Cobb, M. & Ferveur, J.-F. Drosophila cuticular hydrocarbons revisited: mating status alters cuticular profiles. PLoS One 5, e9607 (2010).

    Article  Google Scholar 

  16. Jallon, J.M. A few chemical words exchanged by Drosophila during courtship and mating. Behav. Genet. 14, 441–478 (1984).

    Article  CAS  Google Scholar 

  17. Butterworth, F.M. Lipids of Drosophila: a newly detected lipid in the male. Science 163, 1356–1357 (1969).

    Article  CAS  Google Scholar 

  18. Chen, S., Lee, A.Y., Bowens, N.M., Huber, R. & Kravitz, E.A. Fighting fruit flies: a model system for the study of aggression. Proc. Natl. Acad. Sci. USA 99, 5664–5668 (2002).

    Article  CAS  Google Scholar 

  19. Dow, M.A. & von Schilcher, F. Aggression and mating success in Drosophila melanogaster. Nature 254, 511–512 (1975).

    Article  CAS  Google Scholar 

  20. Lacaille, F. et al. An inhibitory sex pheromone tastes bitter for Drosophila males. PLoS One 2, e661 (2007).

    Article  Google Scholar 

  21. Wang, Z., Singhvi, A., Kong, P. & Scott, K. Taste representations in the Drosophila brain. Cell 117, 981–991 (2004).

    Article  CAS  Google Scholar 

  22. Thorne, N., Chromey, C., Bray, S. & Amrein, H. Taste perception and coding in Drosophila. Curr. Biol. 14, 1065–1079 (2004).

    Article  CAS  Google Scholar 

  23. Weiss, L.A., Dahanukar, A., Kwon, J.Y., Banerjee, D. & Carlson, J.R. The molecular and cellular basis of bitter taste in Drosophila. Neuron 69, 258–272 (2011).

    Article  CAS  Google Scholar 

  24. Marella, S. et al. Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49, 285–295 (2006).

    Article  CAS  Google Scholar 

  25. Lee, Y., Kim, S.H. & Montell, C. Avoiding DEET through insect gustatory receptors. Neuron 67, 555–561 (2010).

    Article  CAS  Google Scholar 

  26. Koganezawa, M., Haba, D., Matsuo, T. & Yamamoto, D. The shaping of male courtship posture by lateralized gustatory inputs to male-specific interneurons. Curr. Biol. 20, 1–8 (2010).

    Article  CAS  Google Scholar 

  27. Lee, Y., Moon, S.J. & Montell, C. Multiple gustatory receptors required for the caffeine response in Drosophila. Proc. Natl. Acad. Sci. USA 106, 4495–4500 (2009).

    Article  CAS  Google Scholar 

  28. Yew, J.Y. et al. A new male sex pheromone and novel cuticular cues for chemical communication in Drosophila. Curr. Biol. 19, 1245–1254 (2009).

    Article  CAS  Google Scholar 

  29. Caterina, M.J. et al. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816–824 (1997).

    Article  CAS  Google Scholar 

  30. Ejima, A. et al. Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate. Curr. Biol. 17, 599–605 (2007).

    Article  CAS  Google Scholar 

  31. Fishilevich, E. & Vosshall, L.B. Genetic and functional subdivision of the Drosophila antennal lobe. Curr. Biol. 15, 1548–1553 (2005).

    Article  CAS  Google Scholar 

  32. Couto, A., Alenius, M. & Dickson, B.J. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biol. 15, 1535–1547 (2005).

    Article  CAS  Google Scholar 

  33. Root, C.M. et al. A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59, 311–321 (2008).

    Article  CAS  Google Scholar 

  34. Issa, F.A. & Edwards, D.H. Ritualized submission and the reduction of aggression in an invertebrate. Curr. Biol. 16, 2217–2221 (2006).

    Article  CAS  Google Scholar 

  35. Wolff, N. & Jing, S. Contextualization of physical and sexual assault in male prisons: incidents and their aftermath. J. Correct. Health Care 15, 58–77 (2009).

    Article  Google Scholar 

  36. Dulac, C. & Torello, A.T. Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat. Rev. Neurosci. 4, 551–562 (2003).

    Article  CAS  Google Scholar 

  37. Mombaerts, P. Genes and ligands for odorant, vomeronasal and taste receptors. Nat. Rev. Neurosci. 5, 263–278 (2004).

    Article  CAS  Google Scholar 

  38. Stowers, L., Holy, T.E., Meister, M., Dulac, C. & Koentges, G. Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 295, 1493–1500 (2002).

    Article  CAS  Google Scholar 

  39. Leypold, B.G. et al. Altered sexual and social behaviors in trp2 mutant mice. Proc. Natl. Acad. Sci. USA 99, 6376–6381 (2002).

    Article  CAS  Google Scholar 

  40. Yoon, H., Enquist, L.W. & Dulac, C. Olfactory inputs to hypothalamic neurons controlling reproduction and fertility. Cell 123, 669–682 (2005).

    Article  CAS  Google Scholar 

  41. Mandiyan, V.S., Coats, J.K. & Shah, N.M. Deficits in sexual and aggressive behaviors in Cnga2 mutant mice. Nat. Neurosci. 8, 1660–1662 (2005).

    Article  CAS  Google Scholar 

  42. Touhara, K. & Vosshall, L.B. Sensing odorants and pheromones with chemosensory receptors. Annu. Rev. Physiol. 71, 307–332 (2009).

    Article  CAS  Google Scholar 

  43. Chamero, P. et al. Identification of protein pheromones that promote aggressive behaviour. Nature 450, 899–902 (2007).

    Article  CAS  Google Scholar 

  44. Zhou, L. et al. Cooperative functions of the reaper and head involution defective genes in the programmed cell death of Drosophila central nervous system midlinecells. Proc. Natl. Acad. Sci. USA 94, 5131–5136 (1997).

    Article  CAS  Google Scholar 

  45. McGuire, S.E., Le, P.T., Osborn, A.J., Matsumoto, K. & Davis, R.L. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302, 1765–1768 (2003).

    Article  CAS  Google Scholar 

  46. Wang, L., Dankert, H., Perona, P. & Anderson, D.J. A common genetic target for environmental and heritable influences on aggressiveness in Drosophila. Proc. Natl. Acad. Sci. USA 105, 5657–5663 (2008).

    Article  CAS  Google Scholar 

  47. Hoyer, S.C. et al. Octopamine in male aggression of Drosophila. Curr. Biol. 18, 159–167 (2008).

    Article  CAS  Google Scholar 

  48. Wenkert, E., Ferreira, V.F., Michelotti, E.L. & Tingoli, M. Synthesis of acyclic, cis olefinic pheromones by way of nickel-catalyzed Grignard reactions. J. Org. Chem. 50, 719–721 (1985).

    Article  CAS  Google Scholar 

  49. Davis, T.L. & Carlson, D.A. Synthesis of 7,11-dienes from enol ether and grignard reagents under nickel catalysis: sex pheromones of Drosophila melanogaster. Synthesis 12, 936–938 (1989).

    Article  Google Scholar 

  50. Gong, W.J. & Golic, K.G. Ends-out, or replacement, gene targeting in Drosophila. Proc. Natl. Acad. Sci. USA 100, 2556–2561 (2003).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank members of the Anderson laboratory for helpful discussions, G. Mancuso for administrative assistance, G. Mosconi for lab management, and K. Scott and L. Vosshall for critical comments on the manuscript. Assistance from N.F. Dalleska and use of gas chromatography–mass spec instrumentation in the Environmental Analysis Center at the California Institute of Technology is gratefully acknowledged. We thank L. Vosshall for generously providing the Or47b mutant alleles generated by J.M. in her laboratory. D.J.A. is an investigator of the Howard Hughes Medical Institute.

Author information

Authors and Affiliations

Authors

Contributions

L.W. carried out the experiments and performed the data analysis. L.W. and D.J.A. conceived the research and wrote the manuscript. X.H. synthesized cuticular hydrocarbon molecules. J.M. generated and characterized Or47b mutant alleles. M.H. characterized the expression of Gr32a-GAL4. J.-C.B., T.M., H.A. and J.D.L. contributed fly strains.

Corresponding authors

Correspondence to Liming Wang or David J Anderson.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–11 (PDF 1991 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, L., Han, X., Mehren, J. et al. Hierarchical chemosensory regulation of male-male social interactions in Drosophila. Nat Neurosci 14, 757–762 (2011). https://doi.org/10.1038/nn.2800

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2800

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing