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.

  • Letter
  • Published:

A double-switch system regulates male courtship behavior in male and female Drosophila melanogaster

Nature Genetics volume 38, pages 1435–1439 (2006)Cite this article

Abstract

Current models describe male-specific fruitless (fruM) as a genetic 'switch' regulating sexual behavior in Drosophila melanogaster, and they postulate that female (F) and male (M) doublesex (dsx) products control body sexual morphology. In contradiction to this simple model, we show that dsx, as well as fruM and non–sex-specific retained (retn), affect both male and female sexual behaviors. In females, both retn and dsxF contribute to female receptivity, and both genes act to repress male-like courtship activity in the presence or absence of fruM. In males, consistent with the opposing functions of dsxM and dsxF, dsxM acts as a positive factor for male courtship. retn also acts counter to fruM in the development of the male-specific muscle of Lawrence. Molecularly, retn seems to regulate sexual behavior via a previously described complex that represses zerknullt. Thus, we show that fru and dsx together act as a 'switch' system regulating behavior in the context of other developmental genes, such as retn.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: retn is antagonistic to fruM in production of courtship and development of the moL.
Figure 2: dsx controls sexual behavior.
Figure 3: Nonoverlapping expression of retn and fruM in the mid-pupal CNS.
Figure 4: retn interacts with dl, gro, Rpd3 and zen to regulate female behavior.
Figure 5: fru and dsx act as parts of a 'switch' system controlling sexual behavior by modulating an intrinsic neural pathway for reproductive behavior in both sexes.

Similar content being viewed by others

References

  1. Hall, J.C. The mating of a fly. Science 264, 1702–1714 (1994).

    Article  CAS  Google Scholar 

  2. Christiansen, A.E., Keisman, E.L., Ahmad, S.M. & Baker, B.S. Sex comes in from the cold: the integration of sex and pattern. Trends Genet. 18, 510–516 (2002).

    Article  CAS  Google Scholar 

  3. Ito, H. et al. Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. Proc. Natl. Acad. Sci. USA 93, 9687–9692 (1996).

    Article  CAS  Google Scholar 

  4. Ryner, L.C. et al. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87, 1079–1089 (1996).

    Article  CAS  Google Scholar 

  5. Usui-Aoki, K. et al. Formation of the male-specific muscle in female Drosophila by ectopic fruitless expression. Nat. Cell Biol. 2, 500–506 (2000).

    Article  CAS  Google Scholar 

  6. Baker, B.S., Taylor, B.J. & Hall, J.C. Are complex behaviors specified by dedicated regulatory genes? Reasoning from Drosophila. Cell 105, 13–24 (2001).

    Article  CAS  Google Scholar 

  7. Demir, E. & Dickson, B.J. fruitless splicing specifies male courtship behavior in Drosophila. Cell 121, 785–794 (2005).

    Article  CAS  Google Scholar 

  8. Manoli, D.S. et al. Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 436, 395–400 (2005).

    Article  CAS  Google Scholar 

  9. Anand, A. et al. Molecular genetic dissection of the sex-specific and vital functions of the Drosophila melanogaster sex determination gene fruitless. Genetics 158, 1569–1595 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Gregory, S.L., Kortschak, R.D., Kalionis, B. & Saint, R. Characterization of the dead ringer gene identifies a novel, highly conserved family of sequence-specific DNA-binding proteins. Mol. Cell. Biol. 16, 792–799 (1996).

    Article  CAS  Google Scholar 

  11. Ditch, L.M. et al. Drosophila retained/dead ringer is necessary for neuronal pathfinding, female receptivity and repression of fruitless independent male courtship behaviors. Development 132, 155–164 (2005).

    Article  CAS  Google Scholar 

  12. Finley, K.D., Taylor, B.J., Milstein, M. & McKeown, M. dissatisfaction, a gene involved in sex-specific behavior and neural development of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 94, 913–918 (1997).

    Article  CAS  Google Scholar 

  13. Villella, A. et al. Extended reproductive roles of the fruitless gene in Drosophila melanogaster revealed by behavioral analysis of new fru mutants. Genetics 147, 1107–1130 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Gailey, D.A., Taylor, B.J. & Hall, J.C. Elements of the fruitless locus regulate development of the muscle of Lawrence, a male-specific structure in the abdomen of Drosophila melanogaster adults. Development 113, 879–890 (1991).

    CAS  PubMed  Google Scholar 

  15. Lawrence, P.A. & Johnston, P. The muscle pattern of a segment of Drosophila may be determined by neurons and not by contributing myoblasts. Cell 45, 505–513 (1986).

    Article  CAS  Google Scholar 

  16. Billeter, J.C. & Goodwin, S.F. Characterization of Drosophila fruitless-gal4 transgenes reveals expression in male-specific fruitless neurons and innervation of male reproductive structures. J. Comp. Neurol. 475, 270–287 (2004).

    Article  CAS  Google Scholar 

  17. Currie, D.A. & Bate, M. Innervation is essential for the development and differentiation of a sex-specific adult muscle in Drosophila melanogaster. Development 121, 2549–2557 (1995).

    CAS  PubMed  Google Scholar 

  18. Waterbury, J.A., Jackson, L.L. & Schedl, P. Analysis of the doublesex female protein in Drosophila melanogaster: role on sexual differentiation and behavior and dependence on intersex. Genetics 152, 1653–1667 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Taylor, B.J., Villella, A., Ryner, L.C., Baker, B.S. & Hall, J.C. Behavioral and neurobiological implications of sex-determining factors in Drosophila. Dev. Genet. 15, 275–296 (1994).

    Article  CAS  Google Scholar 

  20. Villella, A. & Hall, J.C. Courtship anomalies caused by doublesex mutations in Drosophila melanogaster. Genetics 143, 331–344 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Garrett-Engele, C.M. et al. intersex, a gene required for female sexual development in Drosophila, is expressed in both sexes and functions together with doublesex to regulate terminal differentiation. Development 129, 4661–4675 (2002).

    CAS  PubMed  Google Scholar 

  22. Chase, B.A. & Baker, B.S. A genetic analysis of intersex, a gene regulating sexual differentiation in Drosophila melanogaster females. Genetics 139, 1649–1661 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Lee, G. et al. Spatial, temporal, and sexually dimorphic expression patterns of the fruitless gene in the Drosophila central nervous system. J. Neurobiol. 43, 404–426 (2000).

    Article  CAS  Google Scholar 

  24. Stockinger, P., Kvitsiani, D., Rotkopf, S., Tirian, L. & Dickson, B.J. Neural circuitry that governs Drosophila male courtship behavior. Cell 121, 795–807 (2005).

    Article  CAS  Google Scholar 

  25. Valentine, S.A. et al. Dorsal-mediated repression requires the formation of a multiprotein repression complex at the ventral silencer. Mol. Cell. Biol. 18, 6584–6594 (1998).

    Article  CAS  Google Scholar 

  26. Chen, G., Fernandez, J., Mische, S. & Courey, A.J. A functional interaction between the histone deacetylase Rpd3 and the corepressor groucho in Drosophila development. Genes Dev. 13, 2218–2230 (1999).

    Article  CAS  Google Scholar 

  27. Billeter, J.C. et al. Isoform-specific control of male neuronal differentiation and behavior in Drosophila by the fruitless gene. Curr. Biol. 16, 1063–1076 (2006).

    Article  CAS  Google Scholar 

  28. Zhou, J., Zwicker, J., Szymanski, P., Levine, M. & Tjian, R. TAFII mutations disrupt Dorsal activation in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 95, 13483–13488 (1998).

    Article  CAS  Google Scholar 

  29. Akimaru, H., Hou, D.X. & Ishii, S. Drosophila CBP is required for dorsal-dependent twist gene expression. Nat. Genet. 17, 211–214 (1997).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank M. Ludwig for technical assistance; R. Wagaman for cloning pUAST-traF RNAi; B. Dickson (Institute of Molecular Biotechnology of the Austrian Academy of Sciences) for providing fruGal4, FruM and FruΔTra stocks; A. Courey (Department of Chemistry and Biochemistry, University of California, Los Angeles) for providing the Rpd3 null alleles; H. Sone, D. Yamamoto and D. Stewart for help with moL work; K. Wharton and laboratory members for reagents, assistance and discussions and S. Ballard and D. Hazelbaker for comments. This work was supported by a US National Science Foundation grant to M.McK. (IBN-0315660) and a US National Institutes of Health (NIH) grant to B.J.T. (NS33352). T.R.S. is currently an NIH predoctoral trainee (T32GM007601).

Author information

Authors and Affiliations

  1. Molecular Biology, Cell Biology,

    Troy R Shirangi & Michael McKeown

  2. Biochemistry Department, Brown University, 69 Brown Street, Providence, 02912, Rhode Island, USA

    Troy R Shirangi & Michael McKeown

  3. Department of Zoology, Oregon State University, Corvallis, 97331, Oregon, USA

    Barbara J Taylor

Authors
  1. Troy R Shirangi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Barbara J Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael McKeown
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

T.R.S. performed the experiments. T.R.S., B.J.T., and M.McK. developed the project, analyzed the data and wrote the paper.

Corresponding author

Correspondence to Michael McKeown.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Overexpression of retn in its own domain causes courtship deficits in males. (PDF 507 kb)

Supplementary Table 1

Courtship activity of retn−; fruM− males. (PDF 293 kb)

Supplementary Methods (PDF 29 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shirangi, T., Taylor, B. & McKeown, M. A double-switch system regulates male courtship behavior in male and female Drosophila melanogaster. Nat Genet 38, 1435–1439 (2006). https://doi.org/10.1038/ng1908

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng1908

This article is cited by

Search

Advanced 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