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The response of Acropora digitifera to ocean acidification is determined using geochemical proxy measurements of the skeletal composition of A. digitifera cultured under a range of pH levels. We show that the chemical composition ( delta super(11)B, Sr/Ca, Mg/Ca, and Ba/Ca) of the coral skeletons can provide quantitative constraints on the effects of seawater pH on the pH in the calcification fluid (pH sub(CF)) and the mechanisms controlling the incorporation of trace elements into coral aragonite. With the decline of seawater pH, the skeletal delta super(11)B value decreased, while the Sr/Ca ratio showed an increasing trend. The relationship between Mg/Ca and Ba/Ca versus seawater pH was not significant. Inter-colony variation of delta super(11)B was insignificant, although inter-colony variation was observed for Ba/Ca. The decreasing trend of pH sub(CF) calculated from delta super(11)B was from ~8.5, 8.4, and 8.3 for seawater pH of ~8.1, 7.8, and 7.4, respectively. Model calculations based on Sr/Ca and pH sub(CF) suggest that upregulation of pH sub(CF) occurs via exchange of H super(+) with Ca super(2+) with kinetic effects (Rayleigh fractionation), reducing Sr/Ca relative to inorganic deposition of aragonite from seawater. We show that it is possible to constrain the overall carbonate chemistry of the calcifying fluid with estimates of the carbonate saturation of the calcifying fluid ( Omega sub(CF)) being derived from skeletal Sr/Ca and pH sub(CF) (from delta super(11)B). These estimates suggest that the aragonite saturation state of the calcifying fluid Omega sub(CF) is elevated by a factor of 5-10 relative to ambient seawater under all treatment conditions.

Stony corals form the foundation of coral reef ecosystems. Their phylogeny is characterized by a deep evolutionary divergence that separates corals into a robust and complex clade dating back to at least 245 mya. However, the genomic consequences and clade-specific evolution remain unexplored. In this study we have produced the genome of a robust coral, Stylophora pistillata , and compared it to the available genome of a complex coral, Acropora digitifera . We conducted a fine-scale gene-based analysis focusing on ortholog groups. Among the core set of conserved proteins, we found an emphasis on processes related to the cnidarian-dinoflagellate symbiosis. Genes associated with the algal symbiosis were also independently expanded in both species, but both corals diverged on the identity of ortholog groups expanded, and we found uneven expansions in genes associated with innate immunity and stress response. Our analyses demonstrate that coral genomes can be surprisingly disparate. Future analyses incorporating more genomic data should be able to determine whether the patterns elucidated here are not only characteristic of the differences between S. pistillata and A. digitifera but also representative of corals from the robust and complex clade at large.

Large-scale rearing of coral larvae during mass spawning events and subsequent direct introduction of competent larvae onto denuded reefs (‘larval seeding’) has been proposed as a low-tech and affordable way of enhancing coral settlement and hence recovery of degraded reefs. While some studies have shown positive short-term effects on settlement, to date, none have examined the long-term effects of larval seeding for a broadcast-spawning coral. Here, we test whether larval seeding significantly increases coral recruitment rates both in the short (5 wk) and longer (~6 mo to 1 yr) term. Larvae of Acropora digitifera were reared ex situ, and ~1 million larvae were introduced to 7 artificial reefs (ARs) while 7 others were left unseeded. Settlement tiles deployed on both seeded and control ARs were retrieved for examination 5 and 30 wk after seeding. In addition, the presence of visible coral recruits on the AR surfaces was monitored before and for ~13 mo post-seeding. Density of acroporid spat was significantly higher on seeded tiles than on controls 5 wk after seeding, but this effect had vanished by 30 wk. Comparison of the densities of new visible Acropora recruits between seeded and control ARs showed no significant difference ~13 mo after seeding. Larval seeding therefore had no long-term effect due to high post-settlement mortality (which appeared to be density-related). Results suggest that reef-rehabilitation methods that aim to harness coral sexual reproduction might better focus on rearing juveniles through early post-settlement mortality bottlenecks.

Climate change threatens the survival of coral reefs on a global scale, primarily through mass bleaching and mortality as a result of marine heatwaves. While these short-term effects are clear, predicting the fate of coral reefs over the coming century is a major challenge. One way to understand the longer-term effect of rapid climate change is to examine the response of coral populations to past climate shifts. Coastal and shallow-water marine ecosystems such as coral reefs have been reshaped many times by sea-level changes during the Pleistocene, yet few studies have directly linked this with its consequences on population demographics, dispersal, and adaptation. Here we use powerful analytical techniques, afforded by haplotype-phased whole-genomes, to establish such links for the reef-building coral, Acropora digitifera. We show that three genetically distinct populations are present in northwestern Australia, and that their rapid divergence since the last glacial maximum (LGM) can be explained by a combination of founder-effects and restricted gene flow. Signatures of selective sweeps, too strong to be explained by demographic history, are present in all three populations and overlap with genes that show different patterns of functional enrichment between inshore and offshore habitats. In contrast to rapid divergence in the host, we find that photosymbiont communities are largely undifferentiated between corals from all three locations, spanning almost 1000 km, indicating that selection on host genes, and not acquisition of novel symbionts, has been the primary driver of adaptation for this species in northwestern Australia.

The neighbourhoods of cytochrome P450 (CYP) genes in deuterostome genomes, as well as those of the cnidarians Nematostella vectensis and Acropora digitifera and the placozoan Trichoplax adhaerens were examined to find clues concerning the evolution of CYP genes in animals. CYP genes created by the 2R whole genome duplications in chordates have been identified. Both microsynteny and macrosynteny were used to identify genes that coexisted near CYP genes in the animal ancestor. We show that all 11 CYP clans began in a common gene environment. The evidence implies the existence of a single locus, which we term the ‘cytochrome P450 genesis locus’, where one progenitor CYP gene duplicated to create a tandem set of genes that were precursors of the 11 animal CYP clans: CYP Clans 2, 3, 4, 7, 19, 20, 26, 46, 51, 74 and mitochondrial. These early CYP genes existed side by side before the origin of cnidarians, possibly with a few additional genes interspersed. The Hox gene cluster, WNT genes, an NK gene cluster and at least one ARF gene were close neighbours to this original CYP locus. According to this evolutionary scenario, the CYP74 clan originated from animals and not from land plants nor from a common ancestor of plants and animals. The CYP7 and CYP19 families that are chordate-specific belong to CYP clans that seem to have originated in the CYP genesis locus as well, even though this requires many gene losses to explain their current distribution. The approach to uncovering the CYP genesis locus overcomes confounding effects because of gene conversion, sequence divergence, gene birth and death, and opens the way to understanding the biodiversity of CYP genes, families and subfamilies, which in animals has been obscured by more than 600 Myr of evolution.

Despite the importance of stony corals in many research fields related to global issues, such as marine ecology, climate change, paleoclimatogy, and metazoan evolution, very little is known about the evolutionary origin of coral skeleton formation. In order to investigate the evolution of coral biomineralization, we have identified skeletal organic matrix proteins (SOMPs) in the skeletal proteome of the scleractinian coral, Acropora digitifera, for which large genomic and transcriptomic datasets are available. Scrupulous gene annotation was conducted based on comparisons of functional domain structures among metazoans. We found that SOMPs include not only coral-specific proteins, but also protein families that are widely conserved among cnidarians and other metazoans. We also identified several conserved transmembrane proteins in the skeletal proteome. Gene expression analysis revealed that expression of these conserved genes continues throughout development. Therefore, these genes are involved not only skeleton formation, but also in basic cellular functions, such as cell-cell interaction and signaling. On the other hand, genes encoding coral-specific proteins, including extracellular matrix domain-containing proteins, galaxins, and acidic proteins, were prominently expressed in post-settlement stages, indicating their role in skeleton formation. Taken together, the process of coral skeleton formation is hypothesized as: 1) formation of initial extracellular matrix between epithelial cells and substrate, employing pre-existing transmembrane proteins; 2) additional extracellular matrix formation using novel proteins that have emerged by domain shuffling and rapid molecular evolution and; 3) calcification controlled by coral-specific SOMPs.

Indo-Pacific corals predominantly reproduce using synchronous mass spawning events to maximise fertilisation. However, as disturbances continue to thin population densities, the quantities of gametes released declines and colonies become more isolated, reducing the likelihood of cross-fertilisation. Local hydrodynamic conditions can promote or inhibit gamete contact; thus, the interaction between the abiotic environment and sperm density will determine the amount of time gametes interact. In this study, we investigated the sensitivity of reproduction to manipulations of two key limiting factors of fertilisation: sperm concentration and contact time between gametes. We explored fertilisation kinetics of phylogenetically and functionally similar and diverse coral taxa on the Great Barrier Reef and Western Australia (Acropora digitifera, A. tenuis; Coelastrea aspera, Platygyra daedalea). Results indicate that fertilisation is optimised at sperm concentrations > 103 sperm mL−1 and contact times > 30 s, but the extent of these relationships is species-specific. All species showed clear differences in fertilisation success across contact times, although these differences were less distinct for A. tenuis and P. daedalea at very high sperm concentrations. Acropora digitifera and P. daedalea exhibited nonlinear trends with steep slopes of increased fertilisation success once sperm concentration surpassed values of 104 sperm mL−1 and 102 sperm mL−1, respectively, followed by slight declines. Acropora tenuis and A. digitifera had the highest maximum fertilisation success, likely owing to beneficial evolved functional traits like large egg sizes. The present analysis underpins studies of fertilisation kinetics in natural reef populations to help inform management and restoration practices that assist population resilience and recovery.

Photoreception is essential to coral growth, reproduction, and stress responses. Thus far, opsin-based photoreception and potential photoadaptation in Scleractinian corals remains unclear. This study used natural and light-emitting diode (LED) lighting to investigate how Acropora digitifera , which is adapted to shallow-water environments, responds to day–night conditions. We successfully cloned three opsin genes ( Adopsin1, Adopsin2 , and Adopsin3 ) . Adopsin1 and Adopsin2 clustered with the Cnidopsins, whereas Adopsin3 clustered with the anthozoan-specific opsin I group. In situ hybridization showed positive signals of these genes in coral endodermal and ectodermal layers. When A. digitifera branches were reared under a day–night cycle with natural light, a day-high and night-low pattern was observed in the transcript levels of Adopsin1 and Adopsin3. Genes related to calcification [plasma membrane calcium transporting ATPase 2 ( PMCA )] and oxygen homeostasis regulation [hypoxia-inducible factor 1 alpha ( HIF1α )] showed similar patterns. Rearing of branches under a day–night cycle (photoperiod = 12:12, 26.5–29.3 μmol s −1  m −2 ) with red ( λ max  = 628 nm), but not blue (464 nm) or green (519 nm) LED lighting led to increases in transcript levels of Adopsin1 and Adopsin3 during photophase. The transcript levels of carbonic anhydrase, PMCA , HIFα , and sodium-glucose cotransporter were significantly higher during photophase than during scotophase. Furthermore, Adopsin3 upregulation occurred within 4 h of exposure to a red LED light at night. These results suggest that A. digitifera can responding to long wavelengths of light, which play a crucial role in the photophysiology of the coral host. The capacity to perceive red light provides advantages in physiological adaptation and ecological niche occupation by A. digitifera in shallow waters.

Coral reefs are suffering a major decline due to the environmental constraints imposed by climate change. Over the last 20 years, three major coral bleaching events occurred in concomitance with anomalous heatwaves, provoking a severe loss of coral cover worldwide. The conservation strategies for preserving reefs, as they are implemented now, cannot cope with global climatic shifts. Consequently, researchers are advocating for preservation networks to be set‐up to reinforce coral adaptive potential. However, the main obstacle to this implementation is that studies on coral adaption are usually hard to generalize at the scale of a reef system. Here, we study the relationships between genotype frequencies and environmental characteristics of the sea (seascape genomics), in combination with connectivity analysis, to investigate the adaptive potential of a flagship coral species of the Ryukyu Archipelago (Japan). By associating genotype frequencies with descriptors of historical environmental conditions, we discovered six genomic regions hosting polymorphisms that might promote resistance against heat stress. Remarkably, annotations of genes in these regions were consistent with molecular roles associated with heat responses. Furthermore, we combined information on genetic and spatial distances between reefs to predict connectivity at a regional scale. The combination of these results portrayed the adaptive potential of this population: we were able to identify reefs carrying potential heat stress adapted genotypes and to understand how they disperse to neighbouring reefs. This information was summarized by objective, quantifiable and mappable indices covering the whole region, which can be extremely useful for future prioritization of reefs in conservation planning. This framework is transferable to any coral species on any reef system and therefore represents a valuable tool for empowering preservation efforts dedicated to the protection of coral reefs in warming oceans.