Olfactory Shifts Parallel Superspecialism for Toxic Fruit in Drosophila melanogaster Sibling, D. sechellia

SummaryOlfaction in the fruit fly Drosophila melanogaster is increasingly understood, from ligand-receptor-neuron combinations 1, 2, 3 and 4 to their axonal projection patterns into the antennal lobe 5 and 6. Drosophila thus offers an excellent opportunity to study the evolutionary and ecological dynamics of olfactory systems. We compared the structure and function of the generalist D. melanogaster with that of specialist D. sechellia, which oviposits exclusively on morinda fruit [7]. Our analyses show that whereas the fruit's headspace was dominated by acids, antennae responded most strongly to hexanoates. D. sechellia exhibited an extraordinarily strong response to methyl hexanoate (MeHex). Behaviorally, D. sechellia was much more attracted to these morinda fruit volatiles than was D. melanogaster. The high sensitivity to MeHex was paralleled by a 2.5×–3× overrepresentation of MeHex neurons on the antenna and a concordant 2.9× increase in volume of the corresponding glomerulus as compared to D. melanogaster. In addition, the MeHex neuron exhibited an extreme sensitivity down to femtograms of its ligand. In contrast, no peripherally mediated shift was found paralleling D. sechellia's increased attraction to acids. These findings are a demonstration of evolution acting at several levels in the olfactory circuitry in mediating a fruit fly's unique preference for fruit toxic to its sibling species 8, 9 and 10.