Extreme temperatures constrain organismal physiology and impose both acute and chronic effects. Additionally, temperature-induced hormone-mediated stress response pathways and energetic trade-offs are important drivers of life-history variation. This study employs an integrative approach to quantify acute physiological responses to high temperatures in divergent life-history ecotypes of the western terrestrial garter snake (Thamnophis elegans). Using wild-caught animals, we measured oxygen consumption rate and physiological markers of hormonal stress response, energy availability, and anaerobic respiration in blood plasma across five ecologically relevant temperatures (24, 28, 32, 35, and 38° C; 3-hour exposure). Corticosterone, insulin, and glucose concentrations all increased with temperature, but with different thermal response curves, suggesting that high temperatures differently affect energy-regulation pathways. Additionally, oxygen consumption rate increased without plateau and lactate concentration did not increase with temperature, challenging the recent hypothesis that oxygen limitation sets upper thermal tolerance limits. Finally, animals had similar physiological thermal responses to high-temperature exposure regardless of genetic background, suggesting that local adaptation has not resulted in fixed differences between ecotypes. Together, these results identify some of the mechanisms by which higher temperatures alter hormonal-mediated energy balance in reptiles and potential limits to the flexibility of this response.

Accurately predicting the responses of organisms to novel or changing environments requires the development of ecologically‐appropriate experimental methodology and process‐based models. For ectotherms, thermal performance curves (TPCs) have provided a useful framework to describe how organismal performance is dependent on temperature. However, this approach often lacks a mechanistic underpinning, which limits our ability to use TPCs predictively. Furthermore, thermal dependence varies across traits, and performance is also limited by additional abiotic factors, such as oxygen availability. We test a central prediction of our recent Hierarchical Mechanisms of Thermal Limitation (HMTL) Hypothesis which proposes that natural hypoxia exposure will reduce maximal performance and cause the TPC for whole‐organism performance to become more symmetrical. We quantified TPCs for two traits often used as fitness proxies, sprint speed and aerobic scope, in lizards under conditions of normoxia and high‐elevation hypoxia. In line with the predictions of HMTL, anaerobically fuelled sprint speed was unaffected by acute hypoxia while the TPC for aerobic scope became shorter and more symmetrical. This change in TPC shape resulted from both the maximum aerobic scope and the optimal temperature for aerobic scope being reduced in hypoxia as predicted. Following these results, we present a mathematical framework, which we call Temperature–Oxygen Performance Surfaces, to quantify the interactive effects of temperature and oxygen on whole‐organism performance in line with the HMTL hypothesis. This framework is transferrable across traits and levels of organization to allow predictions for how ectotherms will respond to novel combinations of temperature and other abiotic factors, providing a useful tool in a time of rapidly changing environmental conditions. Read the free Plain Language Summary for this article on the Journal blog.