Identification of a neural basis for cold acclimation in Drosophila larvae

Summary Low temperatures can be fatal to insects, but many species have evolved the ability to cold acclimate, thereby increasing their cold tolerance. It has been previously shown that Drosophila melanogaster larvae perform cold-evoked behaviors under the control of noxious cold-sensing neurons (nociceptors), but it is unknown how the nervous system might participate in cold tolerance. Herein, we describe cold-nociceptive behavior among 11 drosophilid species; we find that the predominant cold-evoked larval response is a head-to-tail contraction behavior, which is likely inherited from a common ancestor, but is unlikely to be protective. We therefore tested the hypothesis that cold nociception functions to protect larvae by triggering cold acclimation. We found that Drosophilamelanogaster Class III nociceptors are sensitized by and critical to cold acclimation and that cold acclimation can be optogenetically evoked, sans cold. Collectively, these findings demonstrate that cold nociception constitutes a peripheral neural basis for Drosophila larval cold acclimation.
Graphical abstract
Highlights • Drosophila larvae respond to cold via behaviors which are not obviously protective • Genetically silencing cold nociceptors results in an inability to cold acclimate • Cold acclimation results in nociceptor hypersensitization • Cold tolerance can be improved by activating cold nociceptors sans cold
Biological sciences; Physiology; Neuroscience; Behavioral neuroscience; Cellular neuroscience; Sensory neuroscience