Cold-acclimation improves chill tolerance in the migratory locust through preservation of ion balance and membrane potential

Abstract

Most insects have the ability to alter their cold tolerance in response to temporal temperature fluctuations, and recent studies have shown that insect cold tolerance is closely tied to the ability to maintain transmembrane ion gradients that are important for the maintenance of cell membrane potential (V m ). Several studies have therefore suggested a link between preservation of V m and cellular survival after cold stress, but none has measured V m in this context. We tested this hypothesis by acclimating locusts (Locusta migratoria) to high (31°C) and low temperature (11°C) for 4 days before exposing them to cold stress (0°C) for up to 48 h and subsequently measuring ion balance, cell survival, muscle V m , and whole animal performance. Cold stress caused gradual muscle cell death, which coincided with a loss of ion balance and depolarization of muscle V m . The loss of ion balance and cell polarization were, however, dampened markedly in cold-acclimated locusts such that the development of chill injury was reduced. To further examine the association between cellular injury and V m we exposed in vitro muscle preparations to cold buffers with low, intermediate, or. These experiments revealed that cellular injury during cold exposure occurs when V m becomes severely depolarized. Interestingly, we found that cellular sensitivity to hypothermic hyperkalaemia was lower in cold-acclimated locusts that were better able to defend V m whilst exposed to high extracellular [K + ]. Together these results demonstrate a mechanism of cold acclimation in locusts that improves survival after cold stress: increased cold tolerance is accomplished by preservation of V m through maintenance of ion homeostasis and decreased K + sensitivity.

Cold stress results in sustained locomotor and behavioral deficits in Drosophila melanogaster

“…As the seasons change from autumn to winter, insects use environmental cues such as day length and gradual decrease in temperature to sense the onset of winter and trigger physiological changes (Teets & Denlinger, ). Gradual climatic transitions provide insects the opportunity to acclimate to cold conditions (Jakobs, Gariepy, & Sinclair, ; Sinclair, Coello Alvarado, & Ferguson, ; Teets & Denlinger, ), and indeed cold acclimation directly impacts osmotic regulation to preserve ion homeostasis at low temperature (e.g., Andersen et al, ; Des Marteaux et al, ; MacMillan, Yerushalmi, Jonusaite, Kelly, & Donini, ). In D. melanogaster male reproductive behaviors are negatively influenced by severe cold exposure (Singh & Prasad, ), but exposure to brief cold acclimation (i.e., rapid cold hardening) preserves male reproductive behavior and success (Shreve et al, ).…”

“…Insect thermal tolerance is an important factor mediating population range and dynamics, possibility of invasion, and response to global climate change (Addo‐Bediako et al, ; J. L. Andersen et al, ; Bellard et al, ; Youngsteadt et al, ). As such, great efforts have been devoted to understanding the molecular, physiological, and evolutionary underpinnings of insect thermal tolerance (Andersen et al, ; Andersen et al, ; Findsen et al, ; Macmillan et al, ; Macmillan et al, ). However, there are still gaps in our understanding of the behavioral consequences of cold stress.…”

“…Cold exposure can lead to short-term disruptions in physiology, e.g., dysregulation of ion homeostasis , and long-term fitness consequences, e.g., reduced fecundity (Marshall & Sinclair, 2010;Rinehart et al, 2000). Disruption of membrane polarity and ion balance can cause a decline in neuromuscular cell survival and function (Andersen et al, 2017;Andersen et al, 2018;Findsen et al, 2016;Macmillan et al, 2014Macmillan et al, , 2015 assessing behavioral responses to cold stress using the RING assay.…”

“…L. Andersen et al, 2015;Bellard et al, 2013;Youngsteadt et al, 2017). As such, great efforts have been devoted to understanding the molecular, physiological, and evolutionary underpinnings of insect thermal tolerance (Andersen et al, 2017;Andersen et al, 2018;Findsen et al, 2016;Macmillan et al, 2014;Macmillan et al, 2015). However, there are still gaps in our understanding of the behavioral consequences of cold stress.…”

“…Cold stress affects multiple physiological processes simultaneously (Teets & Denlinger, ), and recent literature indicates that dysregulation of ion balance is a principle route of cold injury (Overgaard & Macmillan, ). Thus, tissues like nerves and muscles, which are highly dependent on ion homeostasis for proper functionality, are particularly sensitive to cold injury (Andersen, Folkersen, MacMillan, & Overgaard, ; Andersen, Jensen, Robertson, & Overgaard, ; Findsen, Overgaard, & Pedersem, ; Macmillan, Baatrup, Overgaard & Macmillan, ; Macmillan et al, ). However, the effects of cold stress on complex behaviors that depend on neuromuscular function have garnered relatively little attention.…”