Abnormalities of male-specific FRU protein and serotonin expression in the CNS of fruitless mutants in Drosophila.

The fruitless gene in Drosophila produces male-specific protein (FRU(M)) involved in the control of courtship. FRU(M) spatial and temporal patterns were examined in fru mutants that exhibit aberrant male courtship. Chromosome breakpoints at the locus eliminated FRU(M). Homozygous viable mutants exhibited an intriguing array of defects. In fru(1) males, there were absences of FRU(M)-expressing neuronal clusters or stained cells within certain clusters, reductions of signal intensities in others, and ectopic FRU(M) expression in novel cells. fru(2) males exhibited an overall decrement of FRU(M) expression in all neurons normally expressing the gene. fru(4) and fru(sat) mutants only produced FRU(M) in small numbers of neurons at extremely low levels, and no FRU(M) signals were detected in fru(3) males. This array of abnormalities was inferred to correlate with the varying behavioral defects exhibited by these mutants. Such abnormalities include courtship among males, which has been hypothesized to involve anomalies of serotonin (5-HT) function in the brain. However, double-labeling uncovered no coexpression of FRU(M) and 5-HT in brain neurons. Yet, a newly identified set of sexually dimorphic FRU(M)/5-HT-positive neurons was identified in the abdominal ganglion of adult males. These sexually dimorphic neurons (s-Abg) project toward regions of the abdomen involved in male reproduction. The s-Abg neurons and the proximal extents of their axons were unstained or absent in wild-type females and exhibited subnormal or no 5-HT immunoreactivity in certain fru-mutant males, indicating that fruitless controls the formation of these cells or 5-HT production in them.