Contrasting heat stress response patterns of coral holobionts across the Red Sea suggest distinct mechanisms of thermal tolerance

Abstract

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.

Census of heat tolerance among Florida's threatened staghorn corals finds resilient individuals throughout existing nursery populations

“…While these temperatures are not representative of the typical temperatures encountered by corals during a natural bleaching event, they do serve as reliable proxies of relative thermal tolerance [28], allowing us to compare differences among individuals. The 2.57°C difference between the least and most thermotolerant individuals found here is comparable to the 2.7°C difference in average ED50 observed between two populations of Stylophora pistillata from the northern and central Red Sea (34.1-36.8°C), also measured using CBASS [24]. The latter populations are separated by approximately 900 km and a MMM temperature gradient of 3.7°C (5 km data product), making it remarkable that the Florida population, spanning just approximately 300 km and only 1°C in MMM, contains an equivalent range in thermal tolerance among individuals.…”

“…Overcoming these challenges requires a better understanding of the natural variation in coral heat tolerance, the distribution of heat-tolerant genotypes and phenotypes and the degree to which heat tolerance is determined by a coral's genes, symbiotic interactions and environment. There is extensive variation in coral heat tolerance across latitudinal and environmental gradients [19][20][21][22][23][24][25], with populations from warmer locations having higher tolerance. However, such differences can also occur over reefal scales of just 10s to 100s of metres [26][27][28], indicating strong selection across habitats and microenvironments over small spatial scales, and/or an important role for acclimatization [29,30].…”

“…Specifically, sets of portable experimental tanks termed coral bleaching automated stress systems (CBASS; [28]), can facilitate the application of standardized, rapid thermal tolerance assays on corals in remote field settings. Importantly, these rapid, acute assays can recapitulate outcomes of longer-term, ecologically relevant bleaching scenarios [24,41], indicating they can be used to generate meaningful, quantitative and comparable metrics of thermal tolerance. Such efforts are now beginning to be applied to broadly census thermal tolerance in wild coral populations [42], from which the identification of tolerant individuals could inform targeted nursery development [13], and other active conservation interventions.…”

Variation in Coral Thermotolerance Across a Pollution Gradient Erodes as Coral Symbionts Shift to More Heat-Tolerant Genera

“…This approach has been shown to determine differences in coral thermotolerance similarly to a classic longterm heat stress assay (Voolstra et al, 2020;Evensen et al, 2021). We chose to use this 1-day ramp-hold assay in 2019 rather than repeat the 2014-style assay due to the logistical advantage of a 1-day assay and to be more comparable to recent studies using CBASS (Voolstra et al, 2020(Voolstra et al, , 2021Cunning et al, 2021;Evensen et al, 2021;Savary et al, 2021). This assay consists of four replicate tanks to test three experimental temperature treatments and one control, for a total of eight tanks.…”

Highly variable response of hard coral taxa to successive coral bleaching events (2019-2020) and rising ocean temperatures in Northeast Peninsular Malaysia

“…Therefore, we suggest a complex networking effect of wind, light and depth on bleaching response across and within individual reefs, further underlined by high-frequency diel temperature variability (DTR). This complex network of environmental differences may further inlfuence species-specific physiological limits that determine adaptive mechanism and upper thermal limits, such as genotypic predisposition (Dixon et al 2015), hostspecific physiological traits (Fitt et al, 2009), and associations with specific symbionts and holobionts (Baker et al, 2004;Voolstra et al, 2021). Thus, species identity played a factor for numerous, but not all taxa.…”