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Genes and circuits of courtship behaviour in Drosophila males

Key Points

  • Two terminal genes in the sex determination cascade, fruitless (fru) and doublesex (dsx), produce sex differences in the Drosophila melanogaster nervous system.

  • fru transcripts in male but not female neurons produce Fru proteins (FruM), which function as masculinizing factors.

  • Fru proteins orchestrate target gene transcription by recruiting chromatin regulators, Bonus, Histone deactylase 1 and/or Heterochromatin protein 1a, resulting in all-or-none switching of sex-types of single neurons.

  • Some fru-expressing neurons are found only in males and others are sexually dimorphic in terms of number, neurite projection and/or dendritic pattern.

  • A male-specific cluster, P1, composed of fru and dsx double-positive interneurons in the brain, is excited upon a male's contact with a female and acts to trigger courtship behaviour in the male.

  • fru-expressing neurons in the sensory system serve to detect sex-related cues and those in the motor circuitry participate in patterning of courtship songs.

  • Interconnecting fru-expressing neurons form a core part of the male courtship circuitry.

Abstract

In Drosophila melanogaster, the causal links among a complex behaviour, single neurons and single genes can be demonstrated through experimental manipulations. A key player in establishing the male courtship circuitry is the fruitless (fru) gene, the expression of which yields the FruM proteins in a subset of male but not female neurons. FruM probably regulates chromatin states, leading to single-neuron sex differences and, consequently, a sexually dimorphic circuitry. The mutual connections among fru-expressing neurons — including primary sensory afferents, central interneurons such as the P1 neuron cluster that triggers courtship, and courtship motor pattern generators — probably form the core portion of the male courtship circuitry.

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Figure 1: Male courtship in Drosophila melanogaster.
Figure 2: The mechanism of Fru action in the masculinization of neurons and behaviour.
Figure 3: A circuitry for the integration of pheromone perception.
Figure 4: Central neurons that initiate male courtship.
Figure 5: Courtship-song motor pattern generation in the thoracic ganglia.
Figure 6: Sensory projections of courtship-related stimuli.

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Acknowledgements

The authors' work is funded by Grants-in-Aid for Scientific Research (24113502, 23220007, 1802012 to D.Y., and 24570082 and 23115702 to M.K.) from MEXT, the Strategic Japanese-French Cooperative Program from JST and a Life Science Grant from the Takeda Science Foundation. The authors thank H. Ito for preparing figure 2 and M. Suyama and S. Abe for secretarial assistance.

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Correspondence to Daisuke Yamamoto or Masayuki Koganezawa.

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Glossary

Muscle of Lawrence

(MOL). A pair of dorsal body wall muscles present in the fifth abdominal segment of male adults. The MOL is induced by a fruitless-expressing motor neuron named Mind (MOL-inducing), which undergoes cell death in females, which therefore lack the MOL.

BTB

A 115-amino-acid stretch shared by a group of transcription factors, which bind to each other via this domain. This domain also mediates ubiquitin ligase binding to its substrates.

Polytene chromosomes

Giant chromosomes that are found in salivary gland cells, where replication occurs without cell division. Stereotyped visible bands on polytene chromosomes serve as landmarks in mapping genes.

Suboesophageal ganglion

(SOG). A ganglion that functions as the feeding centre by integrating gustatory inputs and generating motor outputs for feeding. In Drosophila spp., the SOG is physically integrated into the brain sensu lato.

Hypomorphs

Mutants with reduced activity of a given gene, in contrast to null mutants, in which the gene function is completely lost.

MARCM

(Mosaic analysis with a repressible cell marker). A method for labelling and manipulating cell clones that are mutant for a given locus or clones expressing transgenes in the otherwise wild-type environment by using a stochastic chromosomal recombination induced at a given chromosomal site.

Intersectional approach

A method for labelling and manipulating given cell groups that are defined by the overlap in expression of two genes. Targeted expression of a trasngene is confined to this overlapping region.

Thoracic ganglia

Ganglia consisting of the pro-, meso- and meta-thoracic ganglion. The thoracic ganglia and abdominal ganglia fuse to form the ventral nerve cord in Drosophila melanogaster.

Heterospecific courtship

Courtship by an individual of a particular species directed towards an individual of another species.

TN2 neurons

A male-specific cluster composed of approximately seven doublesex-expressing interneurons in the thoracic ganglia.

TN1 neurons

A male-specific cluster composed of approximately 22 doublesex-expressing interneurons in the thoracic ganglia.

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Yamamoto, D., Koganezawa, M. Genes and circuits of courtship behaviour in Drosophila males. Nat Rev Neurosci 14, 681–692 (2013). https://doi.org/10.1038/nrn3567

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