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

In accepting a courting male, <i>Drosophila subobscura</i> females require nuptial gift giving in which a male gives regurgitated crop contents to her mouth to mouth. No similar behavior is found in <i>D. melanogaster</i>. 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 <i>D. subobscura</i> IPCs abrogates neurite extension and gift giving, whereas FruM overexpression in their <i>D. melanogaster</i> 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 <i>D. subobscura</i> that conferred a latent capability to perform nuptial gift giving.