Painless-mediated stiffness sensing of egg-laying substrates in Drosophila melanogaster
1 LMU Munich, University of Bonn
2 Columbia University
3 LMU Munich
Evolutionarily, the distinct textural properties of fruits and the varying stages of ripening - present unique ecological niches that have shaped egg-laying decisions across various species of fruit flies. For instance, D. melanogaster choose to oviposit on soft, decaying fruits whereas D. suzukii prefer hard, ripe ones. Unlike our understanding of the role of chemosensation in influencing egg-laying decisions, the contribution of mechanosensation and its underlying neuro-genetic architecture remains unknown. In this study, we attempt to pinpoint oviposition substrate-stiffness sensors at the genetic, neuronal, and tissue levels in D.melanogaster. Examining the role of known mechanoreceptors, we identified the Drosophila gene painless, a TRP ion channel, as a potential sensor of textural stiffness. Using tissue-specific inactivation of painless-expressing neurons, we recognized tarsi in legs as the body parts accommodating stiffness sensors. We visualized painless expression in the tarsi, identifying peripheral neurons innervating mechanosensory, chemosensory bristles, and campaniform sensilla. Unlike chemosensory neurons, leg-specific inactivation of campaniform sensilla, stationed dorsally at the joints between tarsomeres, and ventrally-positioned mechanosensory neurons, resulted in reduced oviposition preference for softer substrates. Moreover, RNAi-induced downregulation of painless in mechanosensory neurons innervating campaniform sensilla and mechanosensory bristles also showed stiffness-sensing defects. Based on our results and the location of these sensory candidates in the tarsi, we hypothesize that a female fruit fly upon coming in contact with a stiffer substratum presses its tarsi, leading to tarsal bending, which further causes dorsal compression of campaniform sensilla and possible bending of mechanosensory bristles, thus functioning as peripheral sensory detectors of substrate-stiffness information.