Abstract
SummaryBackgroundSex-specific behavior may originate from differences in brain structure or function. In Drosophila, the action of the male-specific isoform of fruitless in about 2000 neurons appears to be necessary and sufficient for many aspects of male courtship behavior. Initial work found limited evidence for anatomical dimorphism in these fru+ neurons. Subsequently, three discrete anatomical differences in central brain fru+ neurons have been reported, but the global organization of sex differences in wiring is unclear.ResultsA global search for structural differences in the Drosophila brain identified large volumetric differences between males and females, mostly in higher brain centers. In parallel, saturating clonal analysis of fru+ neurons using mosaic analysis with a repressible cell marker identified 62 neuroblast lineages that generate fru+ neurons in the brain. Coregistering images from male and female brains identified 19 new dimorphisms in males; these are highly concentrated in male-enlarged higher brain centers. Seven dimorphic lineages also had female-specific arbors. In addition, at least 5 of 51 fru+ lineages in the nerve cord are dimorphic. We use these data to predict >700 potential sites of dimorphic neural connectivity. These are particularly enriched in third-order olfactory neurons of the lateral horn, where we provide strong evidence for dimorphic anatomical connections by labeling partner neurons in different colors in the same brain.ConclusionOur analysis reveals substantial differences in wiring and gross anatomy between male and female fly brains. Reciprocal connection differences in the lateral horn offer a plausible explanation for opposing responses to sex pheromones in male and female flies.
Highlights
The fruit fly Drosophila melanogaster displays robust, highly stereotyped and dimorphic sexual behaviors [1] that provide an ideal model system to study the genetic and neural basis of innate behavior
Sex-specific behavior may originate from differences in brain structure or function
At least 5 of 51 fru+ lineages in the nerve cord are dimorphic. We use these data to predict >700 potential sites of dimorphic neural connectivity. These are enriched in third-order olfactory neurons of the lateral horn, where we provide strong evidence for dimorphic anatomical connections by labeling partner neurons in different colors in the same brain
Summary
The fruit fly Drosophila melanogaster displays robust, highly stereotyped and dimorphic sexual behaviors [1] that provide an ideal model system to study the genetic and neural basis of innate behavior. Studies using sex mosaics mapped different steps of male courtship to broad regions of the central nervous system [4, 5]. Such results suggest that there are anatomical and functional differences between the sexes in these brain regions. At the level of gross anatomy, few structural dimorphisms have been found, and most are Differences in gross anatomy can identify regions involved in sex-specific behavior, but we must understand how circuit level anatomy and function differ between the sexes. The action of FruM on P1-mRNA-expressing neurons ( fru+ neurons) appears to be sufficient to determine many aspects of male behavior, and at least some of these neurons must be sexually dimorphic in number, morphology, or function
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