Understanding differential heat tolerance of the threatened mountainous star coral Orbicella faveolata from inshore and offshore reef sites in the Florida Keys using gene network analysis

Climate change driven ocean warming is causing widespread degradation of coral reefs. In the Florida Keys, many reefs have lost much of their coral cover, yet some inshore reefs have maintained higher coral cover and exhibited higher bleaching resistance and resilience than reefs offshore during marine heatwave events. To explore the molecular mechanisms underlying the higher heat tolerance observed on inshore reefs, we subjected three inshore and four offshore genotypes of the coral Orbicella faveolata to 30, 31, 32, or 33°C for 31 days and measured photochemical efficiency (Fv/Fm), the species and relative abundance of dinoflagellate endosymbionts, and gene expression of the host and symbiont. All inshore coral genotypes, regardless of symbiont species, were significantly more thermotolerant than offshore genotypes based on comparatively smaller declines in photochemical efficiently. The most heat-tolerant inshore genotype (In1) was dominated by the symbiont Durusdinium trenchii; all other genotypes, both inshore and offshore, were Breviolum minutum -dominated, suggesting local adaptation or acclimatization contributes to the heat tolerance of inshore genotypes not dominated by D . trenchii . After 31 days of heat stress, all coral genotypes (except In2) had lost most of their B . minutum and became dominated by D . trenchii . Host genotype In1 presented unique expression patterns of genes involved in heat shock response, immunity, and protein degradation. There were fewer changes in the symbiont gene expression of inshore corals under heat stress when compared to the offshore colonies, which experienced significant changes, including increases in ribosomal and photosynthetic proteins. These data show that the differential thermotolerance between inshore and offshore O . faveolata in the Florida Keys is associated with statistically significant differences in both host and symbiont gene expression that provide insights into the mechanisms underlying holobiont heat tolerance.