1. The mechanisms that mediate the interaction between the thermal environment and species’ ranges are generally uncertain. Thermal environments may directly restrict species when environments exceed tolerance limits (i.e. the fundamental niche). However, thermal environments might also differentially affect relative performance among species prior to fundamental tolerances being met (i.e. the realized niche).

2. We examined stress physiology (plasma glucose and corticosterone), mitochondrial performance, and the muscle metabolome of congeneric lizards that naturally partition the thermal niche, Elgaria multicarinata (southern alligator lizards; SAL) and E. coerulea (northern alligator lizards; NAL), in response to a thermal challenge to quantify variation in physiological performance and tolerance.

3. Both NAL and SAL displayed physiological stress in response to high temperature, but neither showed signs of irreversible damage. NAL displayed a higher baseline mitochondrial respiration rate than SAL. Moreover, NAL substantially adjusted their physiology in response to thermal challenge whereas SAL did not. For example, the metabolite profile of NAL shifted with changes in key energetic molecules, whereas these were unaffected in SAL.

4. Our results indicate that near-critical high temperatures should incur greater energetic cost in NAL than SAL via an elevated metabolic rate and changes to the metabolome. Thus, SAL displace NAL in warm environments that are within NAL’s fundamental thermal niche, but relatively costly.

5. Our results suggest that sub-critical thermal events can contribute to biogeographic patterns via physiological differences that alter the relative costs of living in warm or cool environments.