Ionotropic Receptor-dependent cool cells control the transition of temperature preference in Drosophila larvae

Temperature sensation guides animals to avoid temperature extremes and to seek their optimal temperatures. The larval stage of Drosophila development has a dramatic effect on temperature preference. While early-stage Drosophila larvae pursue a warm temperature, late-stage larvae seek a significantly lower temperature. Previous studies suggest that this transition depends on multiple rhodopsins at the late larval stage. Here, we show that early-stage larvae, in which dorsal organ cool cells (DOCCs) are functionally blocked, exhibit similar cool preference to that of wild type late-stage larvae. The molecular thermoreceptors in DOCCs are formed by three members of the Ionotropic Receptor (IR) family, IR21a, IR93a, and IR25a. Early-stage larvae of each Ir mutant pursue a cool temperature, similar to that of wild type late-stage larvae. At the late larval stage, DOCCs express decreased IR proteins and exhibit reduced cool responses. Importantly, late-stage larvae that overexpress IR21a, IR93a, and IR25a in DOCCs exhibit similar warm preference to that of wild type early-stage larvae. These data suggest that IR21a, IR93a, and IR25a in DOCCs navigate early-stage larvae to avoid cool temperatures and the reduction of these IR proteins in DOCCs results in animals remaining in cool regions during the late larval stage. Together with previous studies, we conclude that multiple temperature-sensing systems are regulated for the transition of temperature preference in fruit fly larvae. Author summary Animals depend on their temperature-sensing systems to avoid noxious temperature extremes and to seek optimal temperatures to survive, mate, and reproduce. Some animals pursue different optimal temperatures during development. We use fruit flies as a model to investigate how temperature-sensing systems are modulated to guide animals to distinct optimal temperatures during development. While early-stage fruit fly larvae pursue a warm temperature, late-stage larvae seek a lower temperature. Previous studies find that this transition depends on multiple rhodopsin molecules. In this study, we find an additional mechanism that also contributes to this transition. At the early larval stage, a set of cool-sensing cells express a high level of cool responsive molecules, respond strongly to low temperatures, and drive animals to avoid cool regions. At the late larval stage, these cool-sensing cells become less sensitive to low temperatures due to the decreased expression of cool responsive molecules and, thus, animals remain in cool regions. Together with previous studies, we conclude that multiple temperature-sensing systems are regulated for the transition of temperature preference in fruit fly larvae.

Automated summary

Animals rely on temperature-sensing systems to avoid extreme temperatures and choose optimal temperatures for survival, mating, and reproduction. Fruit fly larvae change their temperature preferences during development, with early-stage larvae preferring warm temperatures and late-stage larvae seeking cooler temperatures. This transition is regulated by multiple rhodopsin molecules and the expression levels of IR21a, IR93a, and IR25a in DOCCs play a crucial role in guiding larvae to avoid cool temperatures and warm preferences throughout development.