Local Adaptation Drives Leaf Thermoregulation in Tropical Rainforest Trees

Abstract

Tropical forests play a critical role in biodiversity, carbon sequestration, and climate regulation, but are increasingly affected by heatwaves and droughts. Vulnerability to warming may vary within and between species because of phenotypic divergence. Leaf trait variation can affect leaf operating temperatures—a phenomenon termed ‘limited homeothermy’ when it helps avoid heat damage in warmer conditions. However, evidence for this capacity and the relative roles of acclimation or adaptation remain limited. We measured photosynthetic heat tolerance and leaf thermal traits of three co-occurring rainforest tree species across a thermal gradient in the Australian Wet Tropics. Using a leaf energy balance model parameterised with field-measured traits, we predicted variation in leaf-to-air temperature differences (∆T_trait) and resulting thermal safety margins. We combined this with individual-based genome-wide data to detect signals of adaptive divergence and validated findings in a glasshouse trial with provenances grown under contrasting temperature and humidity conditions. Intraspecific trait variation reduced ∆T_trait and increased heat tolerance in warmer sites for Darlingia darlingiana and Elaeocarpus grandis, but not Cardwellia sublimis. As a result, thermal safety margins declined less steeply with increasing growth temperature in species capable of increased heat tolerance and avoidance, indicating these strategies can effectively buffer warming. All species showed genomic signals of selection, with associations to temperature and moisture variables. In E. grandis, glasshouse results confirmed a negative cline in ∆T_trait with temperature of origin. Although contrasting growth temperature and humidity lead to acclimation of individual traits, their coordination maintained ∆T_trait across the conditions imposed. Our findings provide evidence of limited homeothermy and suggest climate gradients have selected for trait combinations that reduce leaf temperatures at warmer sites in some but not all species. Given the rapid pace of climate change, those species with limited capacity to adjust their thermal safety margins through acclimation or adaptation may be at greater risk of local extinction.