Neural dysfunction correlates with heat coma and CTmax in Drosophila but does not set the boundaries for heat stress survival

Abstract

When heated, insects loose coordinated movement followed by the onset of heat coma (CTmax). These phenotypes are popular measures to quantify inter- and intraspecific differences in insect heat tolerance, and CTmax correlate well with current species distributions. Here we examined the function of the central nervous system (CNS) in five species of Drosophila with different heat tolerances, while they were exposed to either constant high temperature or a gradual increasing temperature (ramp). Tolerant species were able to preserve CNS function at higher temperatures and for longer durations than sensitive species and similar differences were found for the behavioral indices (loss of coordination and onset of heat coma). Furthermore, the timing and temperature (constant and ramp exposure, respectively) for loss of coordination or complete coma coincided with the occurrence of spreading depolarisation (SD) events in the CNS. These SD events disrupt neurological function and silence the CNS suggesting that CNS failure is the primary cause of impaired coordination and heat coma. Heat mortality occurs soon after heat coma in insects and to examine if CNS failure could also be the proximal cause of heat death, we used selective heating of the head (CNS) and abdomen (visceral tissues). When comparing the temperature causing 50% mortality (LT50) of each body part to that of the whole animal, we found that the head was not particularly heat sensitive compared to the abdomen. Accordingly, it is unlikely that nervous failure is the principal/proximate cause of heat mortality in Drosophila. Summary statementHyperthermic failure of the Drosophila central nervous system causes heat coma, a phenotype varying in temperature between drosophilids, but neural failure is likely not the primary cause of heat mortality.