Abstract
SummaryBackgroundMale-specific products of the fruitless (fru) gene control the development and function of neuronal circuits that underlie male-specific behaviors in Drosophila, including courtship. Alternative splicing generates at least three distinct Fru isoforms, each containing a different zinc-finger domain. Here, we examine the expression and function of each of these isoforms.ResultsWe show that most fru+ cells express all three isoforms, yet each isoform has a distinct function in the elaboration of sexually dimorphic circuitry and behavior. The strongest impairment in courtship behavior is observed in fruC mutants, which fail to copulate, lack sine song, and do not generate courtship song in the absence of visual stimuli. Cellular dimorphisms in the fru circuit are dependent on FruC rather than other single Fru isoforms. Removal of FruC from the neuronal classes vAB3 or aSP4 leads to cell-autonomous feminization of arborizations and loss of courtship in the dark.ConclusionsThese data map specific aspects of courtship behavior to the level of single fru isoforms and fru+ cell types—an important step toward elucidating the chain of causality from gene to circuit to behavior.
Highlights
Males and females of sexually reproducing animal species typically display profound differences in their mating behaviors, reflecting the operation of sexually dimorphic neural circuits
Alternative splicing generates at least three distinct Fru isoforms, each containing a different zinc-finger domain
We show that most fru+ cells express all three isoforms, yet each isoform has a distinct function in the elaboration of sexually dimorphic circuitry and behavior
Summary
Males and females of sexually reproducing animal species typically display profound differences in their mating behaviors, reflecting the operation of sexually dimorphic neural circuits. With the two endpoints well defined, the mating behaviors of these organisms provide an ideal opportunity to trace the long chain of causality from genes to behavior. This task involves defining the underlying neural circuitry at cellular resolution, relating specific cellular dimorphisms to specific behavioral dimorphisms, and understanding how these structural and functional dimorphisms are shaped by gene activity. Progress toward this goal is currently most advanced for the male-specific courtship behavior of Drosophila melanogaster (reviewed in [2]). The tra gene encodes a splicing factor with two known targets, doublesex (dsx) and fruitless (fru), both of which produce both male-specific (M) and female-specific (F) transcripts. fruF transcripts appear to be nonfunctional, whereas fruM, dsxM, and dsxF all encode predicted transcription factors essential for various aspects of sex-specific differentiation (reviewed in [5])
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