Impacts of thermal fluctuations on heat tolerance and its metabolomic basis across plant and animal species

Abstract

Temperature varies on a daily and seasonal scale and thermal fluctuations are likely to become even more pronounced under future climate changes. Studies suggest that plastic responses are crucial for species’ ability to cope with thermal stress, but traditionally laboratory studies on ectotherms are performed at constant temperatures and often limited to a few model species and thus not representative for the natural environment. We argue that thermoregulatory behavior and microhabitat shape the response exerted by different organisms to fluctuating temperatures. Thus, a sessile organism incapable of significant behavioral temperature avoidance will be more plastic and exert greater physiological response to thermal fluctuations than mobile organisms that can quickly evade temperature stress. Here we investigate how acclimation to fluctuating (13.2-26.9°C) and constant (20.4°C) temperatures impact heat stress tolerance across a plant (Arabidopsis thaliana) and two animal species (Orchesella cincta and Drosophila melanogaster) inhabiting widely different thermal microhabitats and selective pasts. Moreover, we investigate the underlying metabolic responses of acclimation using an NMR metabolomics approach. We find increased heat tolerance for all species exposed to fluctuating acclimation temperatures; most pronounced for A. thaliana which also showed a strong metabolic response to thermal fluctuations. Generally, sugars were more abundant across A. thaliana and D. melanogaster when exposed to fluctuating compared to constant temperatures, whereas amino acids were less abundant. However, we do not find much evidence for similar metabolomics responses to fluctuating temperature acclimation across species. Differences between the investigated species’ ecology, their distinct selective past and different ability to behaviorally thermoregulate may have shaped their physiological response to thermal fluctuations.