Sodium distribution predicts the chill tolerance of Drosophila melanogaster raised in different thermal conditions.

Many insects, including the model holometabolous insect Drosophila melanogaster, display remarkable plasticity in chill tolerance in response to the thermal environment experienced during development or as adults. At low temperatures, many insects lose the ability to regulate Na(+) balance, which is suggested to cause a secondary loss of hemolymph water to the tissues and gut lumen that concentrates the K(+) remaining in the hemolymph. The resultant increase in extracellular [K(+)] inhibits neuromuscular excitability and is proposed to cause cellular apoptosis and injury. The present study investigates whether and how variation in chill tolerance induced through developmental and adult cold acclimation is associated with changes in Na(+), water, and K(+) balance. Developmental and adult cold acclimation improved the chilling tolerance of D. melanogaster in an additive manner. In agreement with the proposed model, these effects were intimately related to differences in Na(+) distribution prior to cold exposure, such that chill-tolerant flies had low hemolymph [Na(+)], while intracellular [Na(+)] was similar among treatment groups. The low hemolymph Na(+) of cold-acclimated flies allowed them to maintain hemolymph volume, prevent hyperkalemia, and avoid injury following chronic cold exposure. These findings extend earlier observations of hemolymph volume disruption during cold exposure to the most ubiquitous model insect (D. melanogaster), highlight shared mechanisms of developmental and adult thermal plasticity and provide strong support for ionoregulatory failure as a central mechanism of insect chill susceptibility.