Forged by frost, ready for heat: Integration of metabolomics and functional traits investigated along a latitudinal gradient reveals relaxed trade‐offs and enhanced heat tolerance in individuals from cold regions

Acquiring a critical understanding of how organisms respond to environmental changes requires integrating molecular and whole‐organism perspectives while investigating how latitudinal gradients shape thermal responses. We explored trade‐offs between thermal tolerance and performance in the marine intertidal gastropod Littorina littorea collected from 10 locations across a wide latitudinal gradient in North America. Snails were exposed under laboratory conditions to a wide range of temperatures (from 5 to 27°C) for 30 days, after which we characterised their metabolomic profiles in relation to whole‐organism responses obtained from a previous study on the same individuals, including growth, feeding rate, metabolic rate and critical thermal maximum (CT max ). Relationships between growth, feeding rate, CT max and one major metabolomic axis revealed clear trade‐offs between fitness‐related traits and thermal tolerance. The decreased concentrations of metabolites contributing most to such trade‐offs were negatively associated with growth and feeding but positively associated with CT max . Many of these metabolites also differed consistently among locations, with individuals from warmer (lower latitude) regions showing lower concentrations. Their higher concentrations in snails from colder environments may provide them with a greater metabolic capacity, potentially relaxing the trade‐off between thermal tolerance and fitness. Highly abundant metabolites in snails from colder locations were often linked to antioxidant and cellular stress responses. Furthermore, metabolites linearly and non‐linearly related to temperature showed variation in their thermal sensitivity depending on the location, with snails from colder sites showing greater thermal responses. Our results suggest that increased thermal tolerance may come at the expense of reduced investments in fitness‐related traits. The relaxed trade‐offs, the higher production of cellular heat stress defences and the enhanced metabolomic thermal response of snails from colder regions may explain their higher thermal tolerance and acclimation capacity. We show how energy metabolism trade‐offs can shape species thermal tolerance variation across broad environmental gradients. The integrated whole‐organism and molecular perspective we provide offers new insights into the potential adaptive mechanisms governing species responses to current and future climate change. Read the free Plain Language Summary for this article on the Journal blog.