Tropical butterflies lose central nervous system function in the cold from a spreading depolarization event

Abstract

AbstractInsects are ectotherms and their physiological functions are therefore directly influenced by the environmental temperature. By extension, their ability to tolerate thermal extremes is directly linked to their thermal niche and distribution. Understanding the physiological mechanisms that limit insect thermal tolerance is therefore crucial for our ability to predict biogeography and range shifts. Recent studies on fruit flies and locusts suggest that the loss of coordinated movements at the critical thermal minimum is due to a loss of central nervous system function via a spreading depolarization. We hypothesized that a similar mechanism limits nervous function in other insect taxa. Here, we use electrophysiology to investigate whether the same spreading depolarization event occurs in the brain of butterflies exposed to stressful cold. Supporting our hypothesis, we find that exposure to stressful cold induced spreading depolarization in all species tested. This reinforces the idea that loss of central nervous function by a spreading depolarization is a common mechanism underlying the critical thermal minimum in insects. Furthermore, our results highlight how central nervous system performance is finely tuned to match species’ environments. Further research into the physiological mechanisms underlying the spreading depolarization event is likely to elucidate key mechanisms determining insect ecology.