Fecal-Derived Phenol Induces Egg-Laying Aversion in Drosophila

Feces is an abundant, rich source of energy, utilized by a myriad of organisms, not least by members of the order Diptera, i.e., flies. How Drosophila melanogaster reacts to fecal matter remains unclear. Here, we examined oviposition behavior toward a range of fecal samples from mammals native to the putative Southeast African homeland of the fly. We show that D. melanogaster display a strong oviposition aversion toward feces from carnivorous mammals but indifference or even attraction toward herbivore dung. We identify a set of four predictor volatiles, which can be used to differentiate fecal from non-fecal matter, as well as separate carnivore from herbivore feces. Of these volatiles, phenol-indicative of carnivore feces-confers egg-laying aversion and is detected by a single class of sensory neurons expressing Or46a. The Or46a-expressing neurons are necessary and sufficient for oviposition site aversion. We further demonstrate that carnivore feces-unlike herbivore dung-contain a high rate of pathogenic bacteria taxa. These harmful bacteria produce phenol from L-tyrosine, an amino acid specifically enriched in high protein diets, such as consumed by carnivores. Finally, we demonstrate that carnivore feces, as well as phenol, is also avoided by a ball-rolling species of dung beetle, suggesting that phenol is a widespread avoidance signal because of its association with pathogenic bacteria.