Fruitless specifies sexually dimorphic neural circuitry in the Drosophila brain

Abstract

The Drosophila fruitless (fru) gene product Fru has been postulated to be a neural sex determination factor that directs development of the central nervous system (CNS), thereby producing male-typical courtship behaviour and inducing male-specific muscle. Male-specific Fru protein is expressed in small groups of neurons scattered throughout the CNS of male, but not female, Drosophila. Collectively, these observations suggest that Fru 'masculinizes' certain neurons, thereby establishing neural substrates for male-typical behaviour. However, specific differences between neurons resulting from the presence or absence of Fru are unknown. Previous studies have suggested that Fru might result in sexual differences in the CNS at the functional level, as no overt sexual dimorphism in CNS structure was discernible. Here we identify a subset of fru-expressing interneurons in the brain that show marked sexual dimorphism in their number and projection pattern. We also demonstrate that Fru supports the development of neurons with male-specific dendritic fields, which are programmed to die during female development as a result of the absence of Fru. Thus, Fru expression can produce a male-specific neural circuit, probably used during heterosexual courtship, by preventing cell death in identifiable neurons.

Sex-switching of theDrosophilabrain by two antagonistic chromatin factors

“…This suggests that the sexual differences in " fru-expressing" neurons are produced depending on the presence or absence of the Fru protein. 3,5 However, the mechanism by which the the wild-type form of HDAC1 functions to masculinize mAL neurons and the wild-type form of HP1a to feminize them. These chromatin regulators appear to function in an all-or-none manner for determination of the sexual fate of mAL neurons, because none of the single neurons exhibit intersexual characteristics.…”

“…In females with MARCM clones that are homozygous for Df(3L)H99 in which the hid, grim and rpr genes are deleted, the number of mAL neurons increases to a level similar to that in wild-type males. 5 In addition, males with a strong fru mutation (fru NP21 /fru sat ) that lack the Fru protein in the brain carry 5 mAL neurons, just as wild-type females do. 5 These results suggest that Fru suppresses cell death in the male mAL cluster presumably by downregulating expression of the hid, grim and rpr genes.…”

“…5 In addition, males with a strong fru mutation (fru NP21 /fru sat ) that lack the Fru protein in the brain carry 5 mAL neurons, just as wild-type females do. 5 These results suggest that Fru suppresses cell death in the male mAL cluster presumably by downregulating expression of the hid, grim and rpr genes. Other the Su(var)205 mutation is lost when the mutant males are also heterozygous for a null mutation in bon.…”

“…For instance, mAL neurons (also called aDT-b or aDT2 neurons) 2,4 show sexual dimorphisms in the cell number and projection pattern. 5 The mAL neurons function to integrate gustatory pheromone inputs and transmit the resultant signal from the subesophageal ganglion to the superior lateral protocerebrum. 6 Loss-of-function alleles of the fruitless (fru) gene disrupt many aspects of courtship behavior and induce male-directed courtship in males.…”

Into the mind of a fly

“…One gene named fruitless (fru), identified in 1963 by K. S. Gill and cloned over 30 yr later by Daisuke Yamamoto 22 -and separately by the group effort of Hall, Bruce Baker and Barbara Taylor 23 -is now known to be a master regulator of sexuality in the fly 23,24 . The transcription factor encoded by the fru gene is expressed in a subset of central, peripheral, sensory and motor neurons in the adult fly, which are likely to comprise a circuit controlling sexually dimorphic behaviour [25][26][27] . Mutant fru males show homosexual courtship behaviour in which large groups form chains of males courting each other.…”