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

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.

References

  1. 1

    Greenspan, R. J. & Ferveur, J. F. Courtship in Drosophila. Annu. Rev. Genet. 34, 205–232 (2000)

    CAS  Article  Google Scholar 

  2. 2

    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)

    CAS  Article  Google Scholar 

  3. 3

    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)

    CAS  Article  Google Scholar 

  4. 4

    Manoli, D. S. & Baker, B. S. Median bundle neurons coordinate behaviours during Drosophila male courtship. Nature 430, 564–569 (2004)

    ADS  CAS  Article  Google Scholar 

  5. 5

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

    CAS  Article  Google Scholar 

  6. 6

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

    ADS  CAS  Article  Google Scholar 

  7. 7

    Keil, T. A. Fine structure of the pheromone-sensitive sensilla on the antenna of the hawkmoth, Manduca sexta. Tissue Cell 21, 139–151 (1989)

    CAS  Article  Google Scholar 

  8. 8

    Boekhoff-Falk, G. Hearing in Drosophila: development of Johnston's organ and emerging parallels to vertebrate ear development. Dev. Dyn. 232, 550–558 (2005)

    CAS  Article  Google Scholar 

  9. 9

    Ewing, A. W. The neuromuscular basis of courtship song in Drosophila: The role of direct and axillary wing muscles. J. Comp. Physiol. 130, 87–93 (1979)

    Article  Google Scholar 

  10. 10

    Smith, S. A. & Shepherd, D. Central afferent projections of proprioceptive sensory neurons in Drosophila revealed with the enhancer-trap technique. J. Comp. Neurol. 364, 311–323 (1996)

    CAS  Article  Google Scholar 

  11. 11

    Scott, K. C., Taubman, A. D. & Geyer, P. K. Enhancer blocking by the Drosophila gypsy insulator depends upon insulator anatomy and enhancer strength. Genetics 153, 787–798 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  12. 12

    Spieth, H. T. Courtship behavior in Drosophila. Annu. Rev. Entomol. 19, 385–405 (1974)

    CAS  Article  Google Scholar 

  13. 13

    Acebes, A., Cobb, M. & Ferveur, J. F. Species-specific effects of single sensillum ablation on mating position in Drosophila. J. Exp. Biol. 206, 3095–3100 (2003)

    Article  Google Scholar 

  14. 14

    Wolfner, M. F. The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila. Heredity 88, 85–93 (2002)

    CAS  Article  Google Scholar 

  15. 15

    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)

    CAS  Article  Google Scholar 

  16. 16

    Kondoh, Y., Kaneshiro, K. Y., Kimura, K. & Yamamoto, D. Evolution of sexual dimorphism in the olfactory brain of Hawaiian Drosophila. Proc. R. Soc. Lond. B 270, 1005–1013 (2003)

    Article  Google Scholar 

  17. 17

    Vaias, L. J., Napolitano, L. M. & Tompkins, L. Identification of stimuli that mediate experience-dependent modification of homosexual courtship in Drosophila melanogaster. Behav. Genet. 23, 91–97 (1993)

    CAS  Article  Google Scholar 

  18. 18

    Larsson, M. C. et al. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43, 703–714 (2004)

    CAS  Article  Google Scholar 

  19. 19

    Shyamala, B. V. & Chopra, A. Drosophila melanogaster chemosensory and muscle development: identification and properties of a novel allele of scalloped and of a new locus, SG18.1, in a Gal4 enhancer trap screen. J. Genet. 78, 87–97 (1999)

    CAS  Article  Google Scholar 

  20. 20

    McBride, S. M. et al. Mushroom body ablation impairs short-term memory and long-term memory of courtship conditioning in Drosophila melanogaster. Neuron 24, 967–977 (1999)

    CAS  Article  Google Scholar 

  21. 21

    Strauss, R. The central complex and the genetic dissection of locomotor behaviour. Curr. Opin. Neurobiol. 12, 633–638 (2002)

    CAS  Article  Google Scholar 

  22. 22

    Acebes, A., Grosjean, Y., Everaerts, C. & Ferveur, J. F. Cholinergic control of synchronized seminal emissions in Drosophila. Curr. Biol. 14, 704–710 (2004)

    CAS  Article  Google Scholar 

  23. 23

    Lee, G. & Hall, J. C. Abnormalities of male-specific FRU protein and serotonin expression in the CNS of fruitless mutants in Drosophila. J. Neurosci. 21, 513–526 (2001)

    CAS  Article  Google Scholar 

  24. 24

    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 

  25. 25

    Eberl, D. F., Duyk, G. M. & Perrimon, N. A genetic screen for mutations that disrupt an auditory response in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 94, 14837–14842 (1997)

    ADS  CAS  Article  Google Scholar 

  26. 26

    Liu, K. S. & Sternberg, P. W. Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron 14, 79–89 (1995)

    CAS  Article  Google Scholar 

  27. 27

    Shah, N. M. et al. Visualizing sexual dimorphism in the brain. Neuron 43, 313–319 (2004)

    CAS  Article  Google Scholar 

  28. 28

    Song, H. J. et al. The fruitless gene is required for the proper formation of axonal tracts in the embryonic central nervous system of Drosophila. Genetics 162, 1703–1724 (2002)

    CAS  PubMed  PubMed Central  Google Scholar 

  29. 29

    Kitamoto, T. Conditional disruption of synaptic transmission induces male–male courtship behavior in Drosophila. Proc. Natl Acad. Sci. USA 99, 13232–13237 (2002)

    ADS  CAS  Article  Google Scholar 

  30. 30

    Goodwin, S. F. et al. Aberrant splicing and altered spatial expression patterns in fruitless mutants of Drosophila melanogaster. Genetics 154, 725–745 (2000)

    CAS  PubMed  PubMed Central  Google Scholar 

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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.

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Correspondence to Bruce S. Baker.

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Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

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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