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

Abstract

The fruitless gene in Drosophila produces male-specific protein (FRUM) involved in the control of courtship. FRUM spatial and temporal patterns were examined in fru mutants that exhibit aberrant male courtship. Chromosome breakpoints at the locus eliminated FRUM. Homozygous viable mutants exhibited an intriguing array of defects. In fru1 males, there were absences of FRUM-expressing neuronal clusters or stained cells within certain clusters, reductions of signal intensities in others, and ectopic FRUM expression in novel cells. fru2 males exhibited an overall decrement of FRUM expression in all neurons normally expressing the gene. fru4 and frusat mutants only produced FRUM in small numbers of neurons at extremely low levels, and no FRUM signals were detected in fru3 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 FRUM and 5-HT in brain neurons. Yet, a newly identified set of sexually dimorphic FRUM/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.