Although reef-building corals are declining worldwide, responses to bleaching vary within and across species and are partly heritable. Toward predicting bleaching response from genomic data, we generated a chromosome-scale genome assembly for the coral Acropora millepora. We obtained whole-genome sequences for 237 phenotyped samples collected at 12 reefs along the Great Barrier Reef, among which we inferred little population structure. Scanning the genome for evidence of local adaptation, we detected signatures of long-term balancing selection in the heat-shock co-chaperone sacsin. We conducted a genome-wide association study of visual bleaching score for 213 samples, incorporating the polygenic score derived from it into a predictive model for bleaching in the wild. These results set the stage for genomics-based approaches in conservation strategies.

Coral reefs rely upon the highly optimized coral-Symbiodiniaceae symbiosis, making them sensitive to environmental change and susceptible to anthropogenic stress. Coral bleaching is predominantly attributed to photo-oxidative stress, yet nutrient availability and metabolism underpin the stability of symbioses. Recent studies link symbiont proliferation under nutrient enrichment to bleaching; however, the interactions between nutrients and symbiotic stability are nuanced. Here, we demonstrate how bleaching is regulated by the forms and ratios of available nutrients and their impacts on autotrophic carbon metabolism, rather than algal symbiont growth. By extension, historical nutrient conditions mediate hostsymbiont compatibility and bleaching tolerance over proximate and evolutionary timescales. Renewed investigations into the coral nutrient metabolism will be required to truly elucidate the cellular mechanisms leading to coral bleaching. Coral Reefs under Anthropogenic StressCoral reef ecosystems are hotspots of biodiversity and productivity which provide vital and extensive ecosystem services [1-3]. However, these values of coral reefs are under threat due to global mass bleaching events triggered by ocean warming [4]. Coral bleaching (see Glossary) is a stress response to elevated heat and light levels, where corals lose their algal symbionts (Symbiodiniaceae) [5,6]. Corals acquire most of their energy through photosynthates translocated by the algal symbionts [7], and the loss of this energy source for long periods can result in starvation and mortality [5]. Bleaching mortality can lead to reductions in coral cover, species and genetic diversity, which shifts reefs away from a coral-dominated state and impedes ecosystem resilience [8,9]. Although some reefs remain resilient, and there exists potential to adapt to warming oceans through natural means [10] and human interventions [11], strong reductions in anthropogenic carbon emissions are ultimately required to ensure the persistence of coral reefs.Coral reefs are also impacted by local stressors, which reduce water quality and have the potential to interact with warming to increase coral bleaching susceptibility [12]. Changes in land use adjacent to reefs can result in primary nutrient enrichment that may be further altered through biological and physical processes [12]; organisms across a range of trophic levels can secondarily modify the nutrient environment [12,13], and localized fishing results in the removal of significant nutrient subsidies from reefs [14]. Climate change also influences marine biogeochemistry at a global scale, where increased storm activity intensifies enrichment events through riverine flux and water column mixing [12,15,16]. In contrast, ocean warming increases water column stratification which reduces nutrient availability [12,17]. Synergistically, global and local drivers and subsequent biological processes not only impact nutrient levels on coral reefs but also change the forms and ratios of nutrients, making nutrient limitation ...

Although reef-building corals are rapidly declining worldwide, responses to bleaching vary both within and among species. Because these inter-individual differences are partly heritable, they should in principle be predictable from genomic data. Towards that goal, we generated a chromosome-scale genome assembly for the coral Acropora millepora. We then obtained whole genome sequences for 237 phenotyped samples collected at 12 reefs distributed along the Great Barrier Reef, among which we inferred very little population structure. Scanning the genome for evidence of local adaptation, we detected signatures of long-term balancing selection in the heat-shock co-chaperone sacsin. We further used 213 of the samples to conduct a genome-wide association study of visual bleaching score, incorporating the polygenic score derived from it into a predictive model for bleaching in the wild. These results set the stage for the use of genomics-based approaches in conservation strategies.

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