Kosei Sato

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.

<title>Abstract</title>While epigamic traits likely evolve via sexual selection, the mechanism whereby internal sexual dimorphism arises remains less well understood. Seeking clues as to how the internal sexual dimorphism evolved, we compared the abdominal musculature of 41 <italic>Drosophila montium</italic> group species, to determine whether any of these species carry a male-specific muscle of Lawrence (MOL). Our quantitative analysis revealed that the size of a sexually dimorphic MOL analog found in 19 <italic>montium</italic> group species varied widely from species to species, suggesting the gradual evolution of this sexually dimorphic neuromuscular trait. We attempted the ancestral state reconstitution for the presence or absence of the neuromuscular sexual dimorphism in the A5 segment; the neuromuscular sexual dimorphism existed in an old ancestor of the <italic>montium</italic> group, which was lost in some of the most recent common ancestors of derived lineages, and subsequently some species regained it. This loss-and-gain history was not shared by evolutionary changes in the courtship song pattern, even though both traits were commonly regulated by the master regulator male-determinant protein FruM. It is envisaged that different sets of FruM target genes may serve for shaping the song and MOL characteristics, respectively, and, as a consequence, each phenotypic trait underwent a distinct evolutionary path.

The main theme of the review is how changes in pheromone biochemistry and the sensory circuits underlying pheromone detection contribute to mate choice and reproductive isolation. The review focuses primarily on gustatory and non-volatile signals in Drosophila. Premating isolation is prevalent among closely related species. In Drosophila, preference for conspecifics against other species in mate choice underlies premating isolation, and such preference relies on contact chemosensory communications between a female and male along with other biological factors. For example, although D. simulans and D. melanogaster are sibling species that yield hybrids, their premating isolation is maintained primarily by the contrasting effects of 7,11-heptacosadiene (7,11-HD), a predominant female pheromone in D. melanogaster, on males of the two species: it attracts D. melanogaster males and repels D. simulans males. The contrasting preference for 7,11-HD in males of these two species is mainly ascribed to opposite effects of 7,11-HD on neural activities in the courtship decision-making neurons in the male brain: 7,11-HD provokes both excitatory and inhibitory inputs in these neurons and differences in the balance between the two counteracting inputs result in the contrasting preference for 7,11-HD, i.e., attraction in D. melanogaster and repulsion in D. simulans. Introduction of two double bonds is a key step in 7,11-HD biosynthesis and is mediated by the desaturase desatF, which is active in D. melanogaster females but transcriptionally inactivated in D. simulans females. Thus, 7,11-HD biosynthesis diversified in females and 7,11-HD perception diversified in males, yet it remains elusive how concordance of the changes in the two sexes was attained in evolution.