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Anomalous heat waves are causing a major decline of hard corals around the world and threatening the persistence of coral reefs. There are, however, reefs that have been exposed to recurrent thermal stress over the years and whose corals appear to have been tolerant against heat. One of the mechanisms that could explain this phenomenon is local adaptation, but the underlying molecular mechanisms are poorly known. In this work, we applied a seascape genomics approach to study heat stress adaptation in three coral species of New Caledonia (southwestern Pacific) and to uncover the molecular actors potentially involved. We used remote sensing data to characterize the environmental trends across the reef system, and sampled corals living at the most contrasted sites. These samples underwent next generation sequencing to reveal single nucleotide polymorphisms (SNPs), frequencies of which were associated with heat stress gradients. As these SNPs might underpin an adaptive role, we characterized the functional roles of the genes located in their genomic region. In each of the studied species, we found heat stress-associated SNPs located in proximity of genes involved in pathways well known to contribute to the cellular responses against heat, such as protein folding, oxidative stress homeostasis, inflammatory and apoptotic pathways, and DNA damage-repair. In some cases, the same candidate molecular targets of heat stress adaptation recurred among species. Together, these results underline the relevance and the power of the seascape genomics approach for the discovery of adaptive traits that could allow corals to persist across wider thermal ranges.
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