Chill-tolerant <i>Drosophila</i> species maintain electrogenic muscle membrane potential to resist cold-induced depolarization

The ability to tolerate low temperature is among the most important traits defining the functional niche of insects, and it is clear that cold tolerance of most insects is intimately linked to their ability to defend membrane potential (Vm). Failure to maintain membrane polarization results in the loss of neuromuscular function and may ultimately initiate cell death and organismal injury. Prolonged cold exposure challenges membrane polarization through loss of transmembrane ion balance; however, the insect muscle Vm is also dependent on a strong and temperature-dependent electrogenic effect driven by Na+/K+-ATPase activity. In the present study, we investigated the electrogenic contribution of the Na+/K+-ATPase at benign (20°C) and low (0°C) temperature in ten Drosophila species representing a broad spectrum of chill tolerance. We found that the electrogenic effect of the Na+/K+-ATPase contributes a considerable component of the muscle Vm in all ten species at 20°C. This electrogenic contribution is reduced significantly at 0°C in the chill-sensitive species, while tolerant species retain their electrogenic effect at low temperature. Thus, the initial cold-induced muscle depolarization, which is a hallmark of chill-sensitive insects, is largely caused by the loss of Na+/K+-ATPase-dependent electrogenic polarization. We hypothesized that maintenance of Na+/K+-ATPase activity in the cold would be energetically costly, but in contrast to our hypothesis we found no evidence for major energetic costs in the species that maintain membrane polarization at low temperature. On the basis of these observations, we discuss how other adaptations at the protein or membrane level could explain the observed intraspecific differences.