Gene expression plasticity and frontloading promote thermotolerance in Pocilloporid corals

Ecosystems worldwide are suffering from climate change. For example, the coral reef ecosystems are globally threatened by increasing sea surface temperatures. However gene expression plasticity provides the potential for organisms to respond rapidly and effectively to environmental change, and would be favored in variable environments. In this study we investigated the thermal stress response of pocilloporid corals from two contrasting thermal regimes (more stable seawater temperatures in New Caledonia, more variable in Oman) by exposing them to heat stress. We compared the physiological state, bacterial and Symbiodinium communities (using 16S and ITS2 metabarcoding), and gene expression levels (using RNA-Seq) between control conditions and heat stress (the temperature just below the first signs of compromised health). Colonies from both thermal regimes remained apparently normal and had open and colored polyps during heat stress, with no change in bacterial and Symbiodinium community composition. In contrast, they differed in their transcriptomic responses. The thermotolerant colonies (Oman) presented a more plastic transcriptome (more differentially expressed genes and higher fold-changes between control and heat stress conditions), but some other genes had a higher basal expression level (frontloading) compared to the thermosensitive colonies (New Caledonia). In terms of biological function we observed a trade-off between stress response (including induction of tumor necrosis factor receptors, heat shock proteins, and detoxification of reactive oxygen species) and morpho-anatomical functions. Gene regulation (transcription factors, mobile elements) appeared to be highly enriched, indicating possible epigenetic regulation. These results provide new insights into the balance between plasticity and frontloading, and the origin and evolution of these strategies.