Ocean temperatures continue to rise due to climate change but it is unclear if heat tolerance of marine organisms will keep pace. Understanding how tolerance scales from individuals to species and quantifying adaptive potentials is essential to forecasting responses to warming. We reproductively crossed corals from a globally distributed species (Acropora tenuis) on the Great Barrier Reef (Australia) from three thermally distinct reefs to create 85 novel offspring lineages. Individuals were experimentally exposed to temperatures (27.5, 31, and 35.5 - 36 °C) in adult and two critical early life-history stages (larval development and settlement) to assess acquired heat tolerance via introgression on offspring phenotypes by comparing multiple physiological responses (photosynthetic yields, bleaching, necrosis, settlement, and survival). Adaptive potentials and physiological reaction norms were calculated across multiple life-stages to integrate heat tolerance at different biological scales. Selective breeding improved larval survival to heat by 1.5-2.5x but settlement success showed limited improvement. Adult responses to selection at heat were similar but were greater in larvae from warmer reefs compared to the cooler reef. There was also a divergence between adults and offspring mean population responses, likely underpinned by heat stress imposing strong divergent selection on adult colonies. These results have implications for downstream selection during reproduction, as evidenced by variability in a conserved heat tolerance response across offspring lineages. These results inform our ability to forecast the impacts of climate change on wild populations of corals and will aid in developing novel conservation tools like the assisted evolution of at-risk species.

Ocean temperatures continue to rise owing to climate change, but it is unclear whether heat tolerance of marine organisms will keep pace with warming. Understanding how tolerance scales from individuals to species and quantifying adaptive potentials is essential to forecasting responses to warming. We reproductively crossed corals from a globally distributed species (Acropora tenuis) on the Great Barrier Reef (Australia) from three thermally distinct reefs to create 85 offspring lineages. Individuals were experimentally exposed to temperatures (27.5, 31 and 35.5°C) in adult and two critical early life stages (larval and settlement) to assess acquired heat tolerance via outcrossing of offspring phenotypes by comparing five physiological responses (photosynthetic yields, bleaching, necrosis, settlement and survival). Adaptive potentials and physiological reaction norms were calculated across three stages to integrate heat tolerance at different biological scales. Selective breeding improved larval survival to heat by 1.5–2.5× but did not result in substantial enhancement of settlement, although population crosses were significantly different. Under heat stress, adults were less variable compared with larval responses in warmer reefs than in the cooler reef. Adults and offspring also differed in their mean population responses, likely underpinned by heat stress imposing strong divergent selection on adults. These results have implications for downstream selection during reproduction, evidenced by variability in a conserved heat tolerance response across offspring lineages. These results inform our ability to forecast the impacts of climate change on wild populations of corals and will aid in developing novel conservation tools such as the assisted evolution of at-risk species.