Evidence from the proteome for local adaptation to extreme heat in a widespread tree species

Abstract Heatwaves are increasing in frequency and intensity globally with negative consequences for biological function. Assessing the effect of extreme heat on species requires an understanding of their adaptive capacity for mitigating physiological damage. Where long‐term exposure to extreme heat in natural populations provides sufficient selection pressure, populations should exhibit signals of adaptive thermotolerance to temperature extremes. Using quantitative proteomics, we tested this idea in the widespread and commercially important tree species Eucalyptus grandis (Flooded Gum). Seedlings from six natural populations of E. grandis spanning a 2,000 km gradient were exposed to a four‐day extreme heat treatment (42–24°C day–night cycle) in experimental growth chambers. Populations differed in their long‐term exposure to extreme heat conditions, defined both as the number of days annually ≥15°C above mean annual temperature (MAT), and average number of days annually with temperature maxima ≥35°C between 1960 and 1990. Long‐term exposure to extreme heat conditions in the field predicted the protein‐level response of E. grandis to experimental heatwaves. Relationships between long‐term extreme heat exposure and protein increases were positive and linear for all combinations of extreme heat (days ≥15°C above MAT, mean days with temperature maxima ≥35°C annually) and expression (all differentially expressed proteins, isolated heat shock proteins, proteins involved in molecular stress responses). Although extreme climate events are typically rare (e.g., 1 day 15° ≥MAT per 5 years in some populations in our study), E. grandis populations sampled from across a 2,000 km range exhibit a clear capacity to increase expression of proteins involved in heat stress in response to simulated heatwave exposure. Presumably, they respond similarly under natural heatwave conditions. We show that a long‐lived species with a broad environmental niche exhibits adaptive variation in protein response to temperature extremes at the population level. This implies that restoration, translocation and silvicultural programmes should consider the molecular response of source populations to climatic extremes to maximize success under future climates. Tree populations with low exposure to extreme heat conditions may be limited in their ability to respond to heatwave events, potentially limiting their adaptive capacity to withstand novel climate conditions. A plain language summary is available for this article.