Enhanced survival and lower growth in assisted gene flow corals during a marine heatwave driven by local adaptation

Recent increases in the frequency of mass coral bleaching and mortality events have caused shifts in species composition and rapid global reef decline. Genetic-based techniques, like assisted gene flow (AGF), offer the potential to enhance corals climate readiness by introducing genetic variation associated with heat tolerance into vulnerable populations. This method remains untested in the wild during a marine heatwave. To this end, we selectively bred AGF corals by crossing parent Acropora tersa corals collected across five Great Barrier Reef (GBR) locations spanning a thermal and bleaching gradient. Breeding produced intra- and inter-regional offspring that were then deployed to a central GBR reef. This deployment reef was subsequently hit by a marine heatwave (>31.4{degrees}C for 17 days and >6 Degree Heating Weeks). Heat tolerance-associated traits (survival, growth, and bleaching) were compared between AGF offspring and a native control cross over the 95 days in the wild. Overall, AGF offspring had 4x greater odds of survival compared to controls, and 2x greater odds compared to northern juveniles. Growth rates were 14% higher in control juveniles compared to the mean growth rate across all AGF crosses. Interestingly, heat-stress assays (32{degrees}C) of the parental adult corals showed similar patterns to their offspring, with higher survival and lower bleaching of corals from warmer northern reefs. Taken together, these findings providing critical support that the selective breeding of AGF corals can provide enhanced survival under marine heatwave conditions in the wild. It also suggests further evaluation is needed for trait-specific responses to effectively match donor and recipient reefs in restoration planning.