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Median bundle neurons coordinate behaviours during Drosophila male courtship

Abstract

Throughout the animal kingdom the innate nature of basic behaviour routines suggests that the underlying neuronal substrates necessary for their execution are genetically determined and developmentally programmed1,2. Complex innate behaviours require proper timing and ordering of individual component behaviours. In Drosophila melanogaster, analyses of combinations of mutations of the fruitless (fru) gene have shown that male-specific isoforms (FruM) of the Fru transcription factor are necessary for proper execution of all steps of the innate courtship ritual3,4,5,6,7,8,9. Here, we eliminate FruM expression in one group of about 60 neurons in the Drosophila central nervous system and observe severely contracted courtship behaviour, including rapid courtship initiation, absence of orienting and tapping, and the simultaneous occurrence of wing vibration, licking and attempted copulation. Our results identify a small group of median bundle neurons, that in wild-type Drosophila appropriately trigger the sequential execution of the component behaviours that constitute the Drosophila courtship ritual.

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Figure 1: The Drosophila courtship ritual and its regulation by the fru branch of the Drosophila sex-determination hierarchy.
Figure 2: P52a-GAL4 expression in FruM neurons of the median bundle.
Figure 3: Inhibition of FruM expression in median bundle neurons leads to aberrant courtship behaviour.
Figure 4: A functional schematic of putative median bundle roles during the Drosophila courtship ritual.

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Acknowledgements

The authors thank R. Fernald, J. Hall, L. Luo, S. McConnell, B. Taylor, N. Anandasabapathy, M. Arbeitman, E. Marin and members of the Baker laboratory for comments and discussions; M. Siegal for help with statistical analysis; J. Nambu and K. Melnattur for the P52a-GAL4 line; S. Barolo for the UAS-GFPnls line; E. Reynaud for the rat anti-FruM antiserum; G. Bohm for the preparation of culture media and fly food. This work was supported by the Medical Scientist Training Program (D.S.M.) and by an NIH grant to B.S.B.

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Correspondence to Bruce S. Baker.

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Supplementary information

Supplementary Figure 1

This figure shows an alternative model for FruM-dependent median bundle function during Drosophila courtship. (DOC 87 kb)

Supplementary Figure 2

This figure shows female internal genitalia following copulation with control and P52a/fruMIR males bearing Dj-GFP-labeled sperm, demonstrating an absence of sperm and/or mating plug following copulation by P52a/fruMIR males. (DOC 392 kb)

Supplementary Figure 3

This figure shows clonal analysis of P52a-labeled median bundle neurons, revealing dendritic arborization within the suboesophageal ganglion. (DOC 425 kb)

Supplementary Video 1

This video shows multiple P52a/fruMIR males attempting simultaneously to court and/or copulate with a single female when placed in a mating chamber. (MP4 348 kb)

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Manoli, D., Baker, B. Median bundle neurons coordinate behaviours during Drosophila male courtship. Nature 430, 564–569 (2004). https://doi.org/10.1038/nature02713

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