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Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour

Nature volume 436, pages 395–400 (2005)Cite this article

Abstract

Robust innate behaviours are attractive systems for genetically dissecting how environmental cues are perceived and integrated to generate complex behaviours. During courtship, Drosophila males engage in a series of innate, stereotyped behaviours that are coordinated by specific sensory cues. However, little is known about the specific neural substrates mediating this complex behavioural programme1. Genetic, developmental and behavioural studies have shown that the fruitless (fru) gene encodes a set of male-specific transcription factors (FruM) that act to establish the potential for courtship in Drosophila2. FruM proteins are expressed in ∼2% of central nervous system neurons, at least one subset of which coordinates the component behaviours of courtship3,4. Here we have inserted the yeast GAL4 gene into the fru locus by homologous recombination and show that (1) FruM is expressed in subsets of all peripheral sensory systems previously implicated in courtship, (2) inhibition of FruM function in olfactory system components reduces olfactory-dependent changes in courtship behaviour, (3) transient inactivation of all FruM-expressing neurons abolishes courtship behaviour, with no other gross changes in general behaviour, and (4) ‘masculinization’ of FruM-expressing neurons in females is largely sufficient to confer male courtship behaviour. Together, these data demonstrate that FruM proteins specify the neural substrates of male courtship.

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Figure 1: Male-specific fruitless regulates courtship.
Figure 2: fruP1-GAL4 expression in the central nervous system.
Figure 3: fruP1-GAL4 reveals Fru M expression in regions of the peripheral nervous system implicated in courtship behaviours.
Figure 4: Function of Fru M neurons in courtship.

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Acknowledgements

The authors thank T. Clandinin and members of the Baker laboratory for discussions and comments on this manuscript, J. Sekelsky for the gift of the pWhiteOut2 vector, A. O'Reilly and M. Simon for technical advice, Y.-S. Liu for help with dissections, M. Siegal for help with statistics, and G. Bohm for preparation of culture materials and fly food. This work was supported by an NINDS grant to B.J.T., J.C.H. and B.S.B.

Author information

Authors and Affiliations

  1. Neurosciences Program,

    Devanand S. Manoli

  2. Department of Biological Sciences, Stanford University, Stanford, California, 94305, USA

    Devanand S. Manoli & Bruce S. Baker

  3. Department of Zoology, Oregon State University, Oregon, 97331-2914, Corvallis, USA

    Margit Foss & Barbara J. Taylor

  4. Department of Biology, Brandeis University, Massachusetts, 02254, Waltham, USA

    Adriana Villella & Jeffrey C. Hall

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Correspondence to Bruce S. Baker.

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Supplementary information

Supplementary Figure S1

This figure shows courtship index values (CI) for males with and without FruM function. (PDF 707 kb)

Supplementary Figure S2

This figure shows FruM expression in pharate males (a), where low levels of protein can be detected in regions previously not seen, as well as decreased numbers of cells in central brain clusters. (PDF 2912 kb)

Supplementary Figure S3

This figure shows fruP1-gal4, FruM, and fruP1-derived RNA in periperal structures. (PDF 4863 kb)

Supplementary Figure S4

This figure shows fruP1-gal4 expression in CNS components of the visual olfactory, and auditory systems. (PDF 4232 kb)

Supplementary Figure S5

This figure shows a female masculinized in fruP1-gal4 neurons displaying wing extension and vibration when a wild-type male in the chamber produces wing song. (PDF 658 kb)

Supplementary Video S1

This movie shows the behaviour of groups of control and fruP1-GAL4, UAS-shiTS males at restrictive temperatures (31C), illustrating that inhibition of synaptic transmission in fruP1-gal4 neurons does not appear to affects general behaviour in adult males. (MOV 2158 kb)

Supplementary Figures and Video Legends

Legends to accompany the above Supplementary Figures and Supplementary Video. (DOC 23 kb)

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Manoli, D., Foss, M., Villella, A. et al. Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 436, 395–400 (2005). https://doi.org/10.1038/nature03859

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