TY - JOUR T1 - Olfactory receptors tuned to volatile mustard oils in drosophilid flies JF - bioRxiv DO - 10.1101/2019.12.27.889774 SP - 2019.12.27.889774 AU - Teruyuki Matsunaga AU - Carolina E. Reisenman AU - Benjamin Goldman-Huertas AU - Philipp Brand AU - Kevin Miao AU - Hiromu Suzuki AU - Santiago R. Ramírez AU - Noah K. Whiteman Y1 - 2019/01/01 UR - http://biorxiv.org/content/early/2019/12/30/2019.12.27.889774.abstract N2 - Plant toxins are effective defenses because they are aversive to enemies. The same molecules, however, are co-opted as host-finding cues by specialist herbivores. Although such behavioral shifts are central to our understanding of herbivorous insect diversification, it is not well understood how they evolve. We addressed this in Scaptomyza flava, a herbivorous drosophilid fly within a lineage that shifted to feeding on toxic mustard plants (Brassicales) <10 million years ago. S flava lost the ancestral attraction to yeast volatiles and the attendant chemoreceptors that detect these odors. Here we report that S. flava, but not its close microbe-feeding relatives Drosophila melanogaster and S. pallida, is attracted to mustard host-plant odors, including volatile mustard oils (isothiocyanates or ITCs). Our genomic analysis uncovered three S. flava paralogs of an olfactory receptor gene (Or67b) that likely experienced positive selection. We then tested whether these chemoreceptors could underlie the observed attraction to volatile ITCs. Our in vivo recordings revealed that two of the S. flava Or67b proteins (Or67b1 and Or67b3) – but not the homologous Ors from microbe-feeding relatives – responded selectively and sensitively to volatile ITCs. These Ors are the only ITC chemoreceptors other than TRP channel family members (e.g., the TrpA1 ‘wasabi’ receptor) known from animals. Remarkably, S. flava Or67b3 was sufficient to drive olfactory attraction toward butyl ITC when expressed in an attractive olfactory circuit. Our study illuminates that ancestrally aversive chemicals can be co-opted as attractants through gene duplication, leading to the origin of hedonic valence shifts in herbivorous insects.Significance Statement Plant toxins trigger aversive olfactory (volatile-mediated) and gustatory (contact-mediated) responses in animals. Paradoxically, toxic plants are colonized by specialist insects that co-opt toxins as host-plant finding cues. The mechanisms underlying these behavioral shifts, from indifference or repulsion, to attraction, remain unclear. To address this, we used a fly lineage, Scaptomyza flava, that switched from yeast-feeding to feeding on mustard plants less than 10 million years ago. We found that S. flava is attracted to mustard-plant odors and volatile mustard oils (isothiocyanates or ITCs) such as ‘wasabi’, a behavior enabled by the evolution of genes encoding odorant receptors highly sensitive to ITCs. Our study illuminates how insects colonize toxic host plants through duplication and ecological repurposing of genes encoding pre-existing chemoreceptors. ER -