Seascape genomics reveals candidate molecular targets of heat stress adaptation in three coral species

Abstract

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 had been exposed to recurrent thermal stress over the years and whose corals appeared 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 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) of which frequencies 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 neighborhood.In each of the studied species, we found heat stress associated SNPs notably located in proximity of genes coding for well-established actors of the cellular responses against heat. Among these, we can mention proteins involved in DNA damage-repair, protein folding, oxidative stress homeostasis, inflammatory and apoptotic pathways. In some cases, the same putative molecular targets of heat stress adaptation recurred among species.Together, these results underscore 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.

Coral cover surveys corroborate predictions on reef adaptive potential to thermal stress

“…In (b), a logistic model of heat stress adaptation is shown. This model is based on the frequencies of potentially adaptive genotypes of three coral species of New Caledonia 23 . The plot displays the probability of adaptation to heat stress as a logistic function of BAF overall (blue line, with the grey band showing the 95% interval of confidence).…”

“…Previous seascape genomics analyses on three corals of the region ( Acropora millepora, Pocillopora damicornis and Pocillopora acuta ) revealed the presence of multiple genetic variants (32 in total) potentially implicated in heat stress resistance 23 . We employed this data to construct a logistic model of heat stress adaptation defining the probability of presence of potentially adaptive variants (PA HEAT ) as a function of BAF overall (Fig.…”

“…Previous studies have reported reefs that display increased thermal tolerance after recurrent exposure to heat stress 7–11 , and recent research suggested that the thermal contrasts of New Caledonia might have driven adaptive processes in corals of the region 23 . Our results supported this view: while recent thermal stress (BAF previous year ) was associated with a reduction in coral cover, this reduction was mitigated at reefs that have experienced past thermal stress and were therefore predicted with high PA HEAT (Fig.…”

“…We first used remote sensing data to (1) evaluate the thermal variability of the study area and (2) estimate patterns of sea current connectivity between reefs. Next, we employed genomic data from a seascape genomics study on three coral species of the region 23 in order to (1) compute the probability of adaptation to heat stress across the whole region, and (2) verify whether predicted reef connectivity matched genetic correlation between corals. Last, we compared our predictions with field surveys of living coral cover recorded by the New Caledonian observational network of coral reef (RORC) 24 .…”

“…The blue dots correspond to sites of coral cover survey of the New Caledonian observational network of coral reef 24 . The red dots correspond to the sampling locations of coral specimen for the seascape genomics study that provide genetic data in the present study 23 . Sea regions highlighted in purple correspond to the marine reserves and protected areas as catalogued by the French agency for MPAs (http://www.aires-marines.fr/).…”