Algal Symbionts Indicate Heatwave Vulnerability in Corals From Hotspots but Not From Thermal Refugia

Reef-building corals face continued declines due to climate change-amplified marine heatwaves. In addition to affecting coral heat tolerance, corals' algal endosymbionts (family Symbiodiniaceae) can reflect their prior heatwave exposure, although understanding is often limited to heatwave-induced shifts between symbiont genera. Here, we used ITS2 metabarcoding to characterise Symbiodiniaceae assemblages in 293 individuals of the common Indo-Pacific coral Acropora aff. digitifera in Palau (Western Pacific), between two outer-reef regions with contrasting heatwave histories. During the strongest recorded heatwaves, southwestern 'hotspot' reefs have typically accrued an additional 2°C-weeks of heat stress compared to thermal 'refugia' located 60 km north. In contrast to previous studies that observed declines in symbiont richness following heat stress, we found a greater diversity of symbiont taxa and low-abundance sequence variants in 'hotspot' corals, predominantly within the C40 lineage in genus Cladocopium. Combining these data with experimental heatwave performance from 168 of these corals revealed that approximately 10% of heat tolerance variability at hotspot reefs was associated with hosting different symbiont taxa. Compared to other hotspot corals, those hosting symbionts with the C15h sequence variant suffered bleaching mortality at 0.8°C-weeks lower heat stress. Despite higher variability in heat tolerance among corals from thermal refugia compared to hotspot reefs, we found no association between heat tolerance and the symbionts hosted by refugium corals. As the world's coral reefs are exposed to intensifying marine heatwaves under accelerating climate change, the low-abundance variants that characterise symbionts within genera or lineages may become increasingly important indicators of poor heatwave tolerance.