Key Points
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Two terminal genes in the sex determination cascade, fruitless (fru) and doublesex (dsx), produce sex differences in the Drosophila melanogaster nervous system.
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fru transcripts in male but not female neurons produce Fru proteins (FruM), which function as masculinizing factors.
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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.
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Some fru-expressing neurons are found only in males and others are sexually dimorphic in terms of number, neurite projection and/or dendritic pattern.
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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.
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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.
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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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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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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
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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
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Courtship by an individual of a particular species directed towards an individual of another species.
- TN2 neurons
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A male-specific cluster composed of approximately seven doublesex-expressing interneurons in the thoracic ganglia.
- TN1 neurons
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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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DOI: https://doi.org/10.1038/nrn3567
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