Cross-species implementation of an innate courtship behavior by manipulation of the sex-determinant gene.

In accepting a courting male, Drosophila subobscura females require nuptial gift giving in which a male gives regurgitated crop contents to her mouth to mouth. No similar behavior is found in D. melanogaster. By clonal activation of neurons expressing the male-determinant FruM, we identified insulin-like peptide–producing cells (IPCs) and their putative postsynaptic targets, proboscis-innervating motoneurons, as those critical for gift giving. We demonstrate that loss of FruM from D. subobscura IPCs abrogates neurite extension and gift giving, whereas FruM overexpression in their D. melanogaster counterparts induces overgrowth of neurites that harbor functional synapses, culminating in increased regurgitation. We suggest that the acquisition of FruM expression by IPCs was a key event occurring in an ancestral D. subobscura that conferred a latent capability to perform nuptial gift giving. Editor's summary: In the fruit fly Drosophila subobscura, courtship behavior includes nuptial gift giving, in which the male feeds the female a regurgitated food gift. The same behavior is not observed in related species, including the common lab animal D. melanogaster. Tanaka et al. studied the genetics of nuptial gift giving in male animals and showed that expression of the gene FruitlessM (FruM) in insulin-like peptide-producing cells (IPCs) was both necessary and sufficient for triggering this behavior in D. subobscura. Overexpression of FruM in D. melanogaster IPCs induced neurite outgrowth in these cells and increased regurgitation behavior. These results unveil the genetic and neuronal basis of an evolutionary important species-specific behavior. —Mattia Maroso [ABSTRACT FROM AUTHOR]