Environmental, host, and symbiont drivers of heat tolerance in a species complex of reef-building corals

Abstract

Reef-building coral populations are under unprecedented threat from climate warming. Yet, variation in coral heat tolerance exists whereby some colonies can cope with higher sea temperatures than others and thus may hold unique value for conservation and restoration. Here, we quantify variation in heat tolerance of an ecologically important tabular coral species complex across the Great Barrier Reef (GBR) while also measuring genomic variation in the coral host and symbiont partners. Coral bleaching and photochemical traits were measured in 569 colonies within the Acropora hyacinthus species complex from 17 reefs following exposure to standardized acute heat stress assays. We detected substantial variation in heat tolerance, where individual colony thermal thresholds differed by up to 7.3{degrees}C and 5.7{degrees}C among and within reefs, respectively. Sea surface temperature climatology was the strongest predictor of heat tolerance, where colonies from warmer northern and inshore reefs typically exhibited the highest thermal thresholds, while colonies from cooler southern reefs were able to tolerate greater temperature increases relative to their local summer temperatures. Heat tolerance was also positively associated with exposure to thermal stress in the weeks preceding measurements. Assignment of colonies to host genomic clusters revealed four putative species within the A. hyacinthus complex that did not vary in their responses to experimental heat stress. Symbiodiniaceae communities within colonies were comprised primarily of Cladocopium ITS2 variants that differed spatially but had minimal effect on heat tolerance. Between 36 - 80% of heat tolerance variation was explained by environmental, host, and symbiont genomic predictors, leaving 20 - 64% to be explained by additional underlying drivers such as functional genomic variation not measured here. These results may be used to inform conservation and restoration actions, including targeting heat tolerant individuals for selective breeding, and will provide a foundation for evaluating the genomic basis of heat tolerance.