Genetic and Neural Mechanisms that Inhibit Drosophila from Mating with Other Species

Pu Fan1, 2, 9, Devanand S. Manoli2, 3, 9, Osama M. Ahmed5, Yi Chen7, Neha Agarwal2, Sara Kwong2, Allen G. Cai2, Jeffrey Neitz6, Adam Renslo6, Bruce S. Baker8, Nirao M. Shah2, 4, 5, ,

Genetically hard-wired neural mechanisms must enforce behavioral reproductive isolation because interspecies courtship is rare even in sexually naïve animals of most species. We find that the chemoreceptor Gr32a inhibits male D. melanogaster from courting diverse fruit fly species. Gr32a recognizes nonvolatile aversive cues present on these reproductively dead-end targets, and activity of Gr32a neurons is necessary and sufficient to inhibit interspecies courtship. Male-specific Fruitless (FruM), a master regulator of courtship, also inhibits interspecies courtship. Gr32a and FruM are not coexpressed, but FruM neurons contact Gr32a neurons, suggesting that these genes influence a shared neural circuit that inhibits interspecies courtship. Gr32a and FruM also suppress within-species intermale courtship, but we show that distinct mechanisms preclude sexual displays toward conspecific males and other species. Although this chemosensory pathway does not inhibit interspecies mating in D. melanogaster females, similar mechanisms appear to inhibit this behavior in many other male drosophilids.

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