Corals from the northern Red Sea, in particular the Gulf of Aqaba (GoA), have exceptionally high bleaching thresholds approaching >5℃ above their maximum monthly mean (MMM) temperatures. These elevated thresholds are thought to be due to historical selection, as corals passed through the warmer Southern Red Sea during recolonization from the Arabian Sea. To test this hypothesis, we determined thermal tolerance thresholds of GoA versus central Red Sea (CRS) Stylophora pistillata corals using multi‐temperature acute thermal stress assays to determine thermal thresholds. Relative thermal thresholds of GoA and CRS corals were indeed similar and exceptionally high (~7℃ above MMM). However, absolute thermal thresholds of CRS corals were on average 3℃ above those of GoA corals. To explore the molecular underpinnings, we determined gene expression and microbiome response of the coral holobiont. Transcriptomic responses differed markedly, with a strong response to the thermal stress in GoA corals and their symbiotic algae versus a remarkably muted response in CRS colonies. Concomitant to this, coral and algal genes showed temperature‐induced expression in GoA corals, while exhibiting fixed high expression (front‐loading) in CRS corals. Bacterial community composition of GoA corals changed dramatically under heat stress, whereas CRS corals displayed stable assemblages. We interpret the response of GoA corals as that of a resilient population approaching a tipping point in contrast to a pattern of consistently elevated thermal resistance in CRS corals that cannot further attune. Such response differences suggest distinct thermal tolerance mechanisms that may affect the response of coral populations to ocean warming.

Global warming is causing an unprecedented loss of species and habitats worldwide. This is particularly apparent for tropical coral reefs, with an increasing number of reefs experiencing mass bleaching and mortality on an annual basis. As such, there is a growing need for a standardized experimental approach to rapidly assess the thermal limits of corals and predict the survival of coral species across reefs and regions. Using a portable experimental system, the Coral Bleaching Automated Stress System (CBASS), we conducted standardized 18 h acute thermal stress assays to quantitively determine the upper thermal limits of four coral species across the length of the Red Sea coastline, from the Gulf of Aqaba (GoA) to Djibouti (~ 2100 km). We measured dark-acclimated photosynthetic efficiency (Fv/Fm), algal symbiont density, chlorophyll a, and visual bleaching intensity following heat stress. Fv/Fm was the most precise response variable assessed, advancing the Fv/Fm effective dose 50 (ED50, i.e., the temperature at which 50% of the initial Fv/Fm is measured) as an empirically derived proxy for thermal tolerance. ED50 thermal thresholds from the central/southern Red Sea and Djibouti populations were consistently higher for Acropora hemprichii, Pocillopora verrucosa, and Stylophora pistillata (0.1–1.8 °C above GoA corals, respectively), in line with prevailing warmer maximum monthly means (MMMs), though were lower than GoA corals relative to site MMMs (1.5–3.0 °C). P. verrucosa had the lowest thresholds overall. Despite coming from the hottest site, thresholds were lowest for Porites lobata in the southern Red Sea, suggesting long-term physiological damage or ongoing recovery from a severe, prior bleaching event. Altogether, the CBASS resolved historical, taxonomic, and possibly recent environmental drivers of variation in coral thermal thresholds, highlighting the potential for a standardized, short-term thermal assay as a universal approach for assessing ecological and evolutionary variation in the upper thermal limits of corals.

Corals from the northern Red Sea and Gulf of Aqaba exhibit extreme thermal tolerance. To examine the underlying gene expression dynamics, we exposed Stylophora pistillata from the Gulf of Aqaba to short-term (hours) and long-term (weeks) heat stress with peak seawater temperatures ranging from their maximum monthly mean of 27 °C (baseline) to 29.5 °C, 32 °C, and 34.5 °C. Corals were sampled at the end of the heat stress as well as after a recovery period at baseline temperature. Changes in coral host and symbiotic algal gene expression were determined via RNA-sequencing (RNA-Seq). Shifts in coral microbiome composition were detected by complementary DNA (cDNA)-based 16S ribosomal RNA (rRNA) gene sequencing. In all experiments up to 32 °C, RNA-Seq revealed fast and pervasive changes in gene expression, primarily in the coral host, followed by a return to baseline gene expression for the majority of coral (>94%) and algal (>71%) genes during recovery. At 34.5 °C, large differences in gene expression were observed with minimal recovery, high coral mortality, and a microbiome dominated by opportunistic bacteria (including Vibrio species), indicating that a lethal temperature threshold had been crossed. Our results show that the S. pistillata holobiont can mount a rapid and pervasive gene expression response contingent on the amplitude and duration of the thermal stress. We propose that the transcriptomic resilience and transcriptomic acclimation observed are key to the extraordinary thermal tolerance of this holobiont and, by inference, of other northern Red Sea coral holobionts, up to seawater temperatures of at least 32 °C, that is, 5 °C above their current maximum monthly mean.