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


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.

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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.

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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).

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Authors and Affiliations



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.

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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)

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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).

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