Mesophotic depths hide high coral cover communities in French Polynesia.

The rapid decline of shallow coral reefs has increased the interest in the long-understudied mesophotic coral ecosystems (MCEs). However, MCEs are usually characterised by rather low to moderate scleractinian coral cover, with only a few descriptions of high coral cover at depth. Here, we explored eight islands across French Polynesia over a wide depth range (6 to 120 m) to identify coral cover hotspots at mesophotic depths and the co-occurrent biotic groups and abiotic factors that influence such high scleractinian cover. Using Bayesian modelling, we found that 20 out of 64 of studied deep sites exhibited a coral cover higher than expected in the mesophotic range (e.g. as high as 81.8 % at 40 m, 74.5 % at 60 m, 53 % at 90 m and 42 % at 120 m vs the average expected values based on the model of 31.2 % at 40 m, 22.8 % at 60 m, 14.6 % at 90 m and 9.8 % at 120 m). Omitting the collinear factors light-irradiance and depth, these 'hotspots' of coral cover corresponded to mesophotic sites and depths characterised by hard substrate, a steep to moderate slope, and the dominance of laminar corals. Our work unveils the presence of unexpectedly and unique high coral cover communities at mesophotic depths in French Polynesia, highlighting the importance of expanding the research on deeper depths for the potential relevance in the conservation management of tropical coral reefs.

Mesophotic coral ecosystems.

Pim Bongaerts introduces mesophotic, lower-light coral ecosystems.

Deep connections: Divergence histories with gene flow in mesophotic Agaricia corals.

Largely understudied, mesophotic coral ecosystems lie below shallow reefs (at >30 m depth) and comprise ecologically distinct communities. Brooding reproductive modes appear to predominate among mesophotic-specialist corals and may limit genetic connectivity among populations. Using reduced representation genomic sequencing, we assessed spatial population genetic structure at 50 m depth in an ecologically important mesophotic-specialist species Agaricia grahamae, among locations in the Southern Caribbean. We also tested for hybridisation with the closely related (but depth-generalist) species Agaricia lamarcki, within their sympatric depth zone (50 m). In contrast to our expectations, no spatial genetic structure was detected between the reefs of Curaçao and Bonaire (~40 km apart) within A. grahamae. However, cryptic taxa were discovered within both taxonomic species, with those in A. lamarcki (incompletely) partitioned by depth and those in A. grahamae occurring sympatrically (at the same depth). Hybrid analyses and demographic modelling identified contemporary and historical gene flow among cryptic taxa, both within and between A. grahamae and A. lamarcki. These results (1) indicate that spatial connectivity and subsequent replenishment may be possible between islands of moderate geographic distances for A. grahamae, an ecologically important mesophotic species, (2) that cryptic taxa occur in the mesophotic zone and environmental selection along shallow to mesophotic depth gradients may drive divergence in depth-generalists such as A. lamarcki, and (3) highlight that gene flow links taxa within this relativity diverse Caribbean genus.

Mesophotic coral communities escape thermal coral bleaching in French Polynesia.

Climate change and consequent coral bleaching are causing the disappearance of reef-building corals worldwide. While bleaching episodes significantly impact shallow waters, little is known about their impact on mesophotic coral communities. We studied the prevalence of coral bleaching two to three months after a heat stress event, along an extreme depth range from 6 to 90 m in French Polynesia. Bayesian modelling showed a decreasing probability of bleaching of all coral genera over depth, with little to no bleaching observed at lower mesophotic depths (greater than or equal to 60 m). We found that depth-generalist corals benefit more from increasing depth than depth-specialists (corals with a narrow depth range). Our data suggest that the reduced prevalence of bleaching with depth, especially from shallow to upper mesophotic depths (40 m), had a stronger relation with the light-irradiance attenuation than temperature. While acknowledging the geographical and temporal variability of the role of mesophotic reefs as spatial refuges during thermal stress, we ought to understand why coral bleaching reduces with depth. Future studies should consider repeated monitoring and detailed ecophysiological and environmental data. Our study demonstrated how increasing depth may offer a level of protection and that lower mesophotic communities could escape the impacts of a thermal bleaching event.

Morphological stasis masks ecologically divergent coral species on tropical reefs.

Coral reefs are the epitome of species diversity, yet the number of described scleractinian coral species, the framework-builders of coral reefs, remains moderate by comparison. DNA sequencing studies are rapidly challenging this notion by exposing a wealth of undescribed diversity, but the evolutionary and ecological significance of this diversity remains largely unclear. Here, we present an annotated genome for one of the most ubiquitous corals in the Indo-Pacific (Pachyseris speciosa) and uncover, through a comprehensive genomic and phenotypic assessment, that it comprises morphologically indistinguishable but ecologically divergent lineages. Demographic modeling based on whole-genome resequencing indicated that morphological crypsis (across micro- and macromorphological traits) was due to ancient morphological stasis rather than recent divergence. Although the lineages occur sympatrically across shallow and mesophotic habitats, extensive genotyping using a rapid molecular assay revealed differentiation of their ecological distributions. Leveraging "common garden" conditions facilitated by the overlapping distributions, we assessed physiological and quantitative skeletal traits and demonstrated concurrent phenotypic differentiation. Lastly, spawning observations of genotyped colonies highlighted the potential role of temporal reproductive isolation in the limited admixture, with consistent genomic signatures in genes related to morphogenesis and reproduction. Overall, our findings demonstrate the presence of ecologically and phenotypically divergent coral species without substantial morphological differentiation and provide new leads into the potential mechanisms facilitating such divergence. More broadly, they indicate that our current taxonomic framework for reef-building corals may be scratching the surface of the ecologically relevant diversity on coral reefs, consequently limiting our ability to protect or restore this diversity effectively.

Symbiotic associations of the deepest recorded photosynthetic scleractinian coral (172 m depth).

The symbiosis between scleractinian corals and photosynthetic algae from the family Symbiodiniaceae underpins the health and productivity of tropical coral reef ecosystems. While this photosymbiotic association has been extensively studied in shallow waters (<30 m depth), we do not know how deeper corals, inhabiting large and vastly underexplored mesophotic coral ecosystems, modulate their symbiotic associations to grow in environments that receive less than 1% of surface irradiance. Here we report on the deepest photosymbiotic scleractinian corals collected to date (172 m depth), and use amplicon sequencing to identify the associated symbiotic communities. The corals, identified as Leptoseris hawaiiensis, were confirmed to host Symbiodiniaceae, predominantly of the genus Cladocopium, a single species of endolithic algae from the genus Ostreobium, and diverse communities of prokaryotes. Our results expand the reported depth range of photosynthetic scleractinian corals (0-172 m depth), and provide new insights on their symbiotic associations at the lower depth extremes of tropical coral reefs.

Genomic signatures in the coral holobiont reveal host adaptations driven by Holocene climate change and reef specific symbionts.

Genetic signatures caused by demographic and adaptive processes during past climatic shifts can inform predictions of species' responses to anthropogenic climate change. To identify these signatures in Acropora tenuis, a reef-building coral threatened by global warming, we first assembled the genome from long reads and then used shallow whole-genome resequencing of 150 colonies from the central inshore Great Barrier Reef to inform population genomic analyses. We identify population structure in the host that reflects a Pleistocene split, whereas photosymbiont differences between reefs most likely reflect contemporary (Holocene) conditions. Signatures of selection in the host were associated with genes linked to diverse processes including osmotic regulation, skeletal development, and the establishment and maintenance of symbiosis. Our results suggest that adaptation to post-glacial climate change in A. tenuis has involved selection on many genes, while differences in symbiont specificity between reefs appear to be unrelated to host population structure.

A contemporary baseline record of the world's coral reefs.

Addressing the global decline of coral reefs requires effective actions from managers, policymakers and society as a whole. Coral reef scientists are therefore challenged with the task of providing prompt and relevant inputs for science-based decision-making. Here, we provide a baseline dataset, covering 1300 km of tropical coral reef habitats globally, and comprised of over one million geo-referenced, high-resolution photo-quadrats analysed using artificial intelligence to automatically estimate the proportional cover of benthic components. The dataset contains information on five major reef regions, and spans 2012-2018, including surveys before and after the 2016 global bleaching event. The taxonomic resolution attained by image analysis, as well as the spatially explicit nature of the images, allow for multi-scale spatial analyses, temporal assessments (decline and recovery), and serve for supporting image recognition developments. This standardised dataset across broad geographies offers a significant contribution towards a sound baseline for advancing our understanding of coral reef ecology and thereby taking collective and informed actions to mitigate catastrophic losses in coral reefs worldwide.

Mesophotic.org: a repository for scientific information on mesophotic ecosystems.

Mesophotic coral ecosystems (MCEs) and temperate mesophotic ecosystems (TMEs) occur at depths of roughly 30-150 m depth and are characterized by the presence of photosynthetic organisms despite reduced light availability. Exploration of these ecosystems dates back several decades, but our knowledge remained extremely limited until about a decade ago, when a renewed interest resulted in the establishment of a rapidly growing research community. Here, we present the 'mesophotic.org' database, a comprehensive and curated repository of scientific literature on mesophotic ecosystems. Through both manually curated and automatically extracted metadata, the repository facilitates rapid retrieval of available information about particular topics (e.g. taxa or geographic regions), exploration of spatial/temporal trends in research and identification of knowledge gaps. The repository can be queried to comprehensively obtain available data to address large-scale questions and guide future research directions. Overall, the 'mesophotic.org' repository provides an independent and open-source platform for the ever-growing research community working on MCEs and TMEs to collate and expedite our understanding of the occurrence, composition and functioning of these ecosystems. Database URL: http://mesophotic.org/.

Erratum: Publisher Correction: Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis.

[This corrects the article DOI: 10.1038/s42003-018-0098-3.].

Morphological and genetic divergence between Mediterranean and Caribbean populations of Madracis pharensis (Heller 1868) (Scleractinia, Pocilloporidae): too much for one species?

The colonial stony coral genus Madracis is cosmopolitan, lives in shallow and deep water habitats, and includes zooxanthellate, azooxanthellate and facultative symbiotic species. One of its species, Madracis pharensis, has been recorded from the Mediterranean and East Atlantic, where it forms small knobby and facultative zooxanthellate colonies (also named M. pharensis f. pharensis), and from the tropical Caribbean, where it also occurs in a massive and zooxanthellate form (named M. pharensis f. luciphila by some). These two forms have been previously found to host different Symbiodinium species. In this study, species boundaries and phylogenetic relationships between these two Madracis pharensis forms (from the Mediterranean Sea and the Caribbean), M. senaria, and the Indo-west Pacific M. kirbyi were analyzed through an integrated systematics approach, including corallite dimensions, micromorphology and two molecular markers (ITS and ATP8). Significant genetic and morphological differences were found between all the examined Madracis species, and between M. pharensis from the Mediterranean Sea and M. pharensis f. luciphila from the Caribbean in particular. Based on these results, the latter does not represent a zooxanthellate ecomorph of the former but a different species. Its identity remains to be ascertained and its relationship with the Caribbean M. decactis, with which it bears morphologic resemblance, must be investigated in further studies. Overall, the presence of cryptic Madracis species in the Easter and Central Atlantic Ocean remains to be evaluated.

Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis.

Symbiosis between dinoflagellates of the genus Symbiodinium and reef-building corals forms the trophic foundation of the world's coral reef ecosystems. Here we present the first draft genome of Symbiodinium goreaui (Clade C, type C1: 1.03 Gbp), one of the most ubiquitous endosymbionts associated with corals, and an improved draft genome of Symbiodinium kawagutii (Clade F, strain CS-156: 1.05 Gbp) to further elucidate genomic signatures of this symbiosis. Comparative analysis of four available Symbiodinium genomes against other dinoflagellate genomes led to the identification of 2460 nuclear gene families (containing 5% of Symbiodinium genes) that show evidence of positive selection, including genes involved in photosynthesis, transmembrane ion transport, synthesis and modification of amino acids and glycoproteins, and stress response. Further, we identify extensive sets of genes for meiosis and response to light stress. These draft genomes provide a foundational resource for advancing our understanding of Symbiodinium biology and the coral-algal symbiosis.

Rethinking the Coral Microbiome: Simplicity Exists within a Diverse Microbial Biosphere.

Studies of the coral microbiome predominantly characterize the microbial community of the host species as a collective, rather than that of the individual. This ecological perspective on the coral microbiome has led to the conclusion that the coral holobiont is the most diverse microbial biosphere studied thus far. However, investigating the microbiome of the individual, rather than that of the species, highlights common and conserved community attributes which can provide insights into the significance of microbial associations to the host. Here, we show there are consistent characteristics between individuals in the proposed three components of the coral microbiome (i.e., "environmentally responsive community," "resident or individual microbiome," and "core microbiome"). We found that the resident microbiome of a photoendosymbiotic coral harbored <3% (∼605 phylotypes) of the 16S rRNA phylotypes associated with all investigated individuals of that species ("species-specific microbiome") (∼21,654 phylotypes; individuals from Pachyseris speciosa [n = 123], Mycedium elephantotus [n = 95], and Acropora aculeus [n = 91] from 10 reef locations). The remaining bacterial phylotypes (>96%) (environmentally responsive community) of the species-specific microbiome were in fact not found in association with the majority of individuals of the species. Only 0.1% (∼21 phylotypes) of the species-specific microbiome of each species was shared among all individuals of the species (core microbiome), equating to ∼3.4% of the resident microbiome. We found taxonomic redundancy and consistent patterns of composition, structure, and taxonomic breadth across individual microbiomes from the three coral species. Our results demonstrate that the coral microbiome is structured at the individual level.IMPORTANCE We propose that the coral holobiont should be conceptualized as a diverse transient microbial community that is responsive to the surrounding environment and encompasses a simple, redundant, resident microbiome and a small conserved core microbiome. Most importantly, we show that the coral microbiome is comparable to the microbiomes of other organisms studied thus far. Accurately characterizing the coral-microbe interactions provides an important baseline from which the functional roles and the functional niches within which microbes reside can be deciphered.

Deep reefs of the Great Barrier Reef offer limited thermal refuge during mass coral bleaching.

Our rapidly warming climate is threatening coral reefs as thermal anomalies trigger mass coral bleaching events. Deep (or "mesophotic") coral reefs are hypothesised to act as major ecological refuges from mass bleaching, but empirical assessments are limited. We evaluated the potential of mesophotic reefs within the Great Barrier Reef (GBR) and adjacent Coral Sea to act as thermal refuges by characterising long-term temperature conditions and assessing impacts during the 2016 mass bleaching event. We found that summer upwelling initially provided thermal relief at upper mesophotic depths (40 m), but then subsided resulting in anomalously warm temperatures even at depth. Bleaching impacts on the deep reefs were severe (40% bleached and 6% dead colonies at 40 m) but significantly lower than at shallower depths (60-69% bleached and 8-12% dead at 5-25 m). While we confirm that deep reefs can offer refuge from thermal stress, we highlight important caveats in terms of the transient nature of the protection and their limited ability to provide broad ecological refuge.

Mesophotic coral ecosystems are threatened and ecologically distinct from shallow water reefs.

The rapid degradation of coral reefs is one of the most serious biodiversity problems facing our generation. Mesophotic coral reefs (at depths of 30 to 150 meters) have been widely hypothesized to provide refuge from natural and anthropogenic impacts, a promise for the survival of shallow reefs. The potential role of mesophotic reefs as universal refuges is often highlighted in reef conservation research. This hypothesis rests on two assumptions: (i) that there is considerable overlap in species composition and connectivity between shallow and deep populations and (ii) that deep reefs are less susceptible to anthropogenic and natural impacts than their shallower counterparts. Here we present evidence contradicting these assumptions and argue that mesophotic reefs are distinct, impacted, and in as much need of protection as shallow coral reefs.

Adaptation to reef habitats through selection on the coral animal and its associated microbiome.

Spatially adjacent habitats on coral reefs can represent highly distinct environments, often harbouring different coral communities. Yet, certain coral species thrive across divergent environments. It is unknown whether the forces of selection are sufficiently strong to overcome the counteracting effects of the typically high gene flow over short distances, and for local adaptation to occur. We screened the coral genome (using restriction site-associated sequencing) and characterized both the dinoflagellate photosymbiont- and tissue-associated prokaryote microbiomes (using metabarcoding) of a reef flat and slope population of the reef-building coral, Pocillopora damicornis, at two locations on Heron Island in the southern Great Barrier Reef. Reef flat and slope populations were separated by <100 m horizontally and ~5 m vertically, and the two study locations were separated by ~1 km. For the coral host, genetic divergence between habitats was much greater than between locations, suggesting limited gene flow between the flat and slope populations. Consistent with environmental selection, outlier loci primarily belonged to the conserved, minimal cellular stress response, likely reflecting adaptation to the different temperature and irradiance regimes on the reef flat and slope. The prokaryote community differed across both habitat and, to a lesser extent, location, whereas the dinoflagellate photosymbionts differed by habitat but not location. The observed intraspecific diversity associated with divergent habitats supports that environmental adaptation involves multiple members of the coral holobiont. Adaptive alleles or microbial associations present in coral populations from the environmentally variable reef flat may provide a source of adaptive variation for assisted evolution approaches, through assisted gene flow, artificial cross-breeding or probiotic inoculations, with the aim to increase climate resilience in the slope populations.

High species richness and lineage diversity of reef corals in the mesophotic zone.

Coral reefs are increasingly threatened by thermal bleaching and tropical storm events associated with rising sea surface temperatures. Deeper habitats offer some protection from these impacts and may safeguard reef-coral biodiversity, but their faunas are largely undescribed for the Indo-Pacific. Here, we show high species richness of scleractinian corals in mesophotic habitats (30-125 m) for the northern Great Barrier Reef region that greatly exceeds previous records for mesophotic habitats globally. Overall, 45% of shallow-reef species (less than or equal to 30 m), 78% of genera, and all families extended below 30 m depth, with 13% of species, 41% of genera, and 78% of families extending below 45 m. Maximum depth of occurrence showed a weak relationship to phylogeny, but a strong correlation with maximum latitudinal extent. Species recorded in the mesophotic had a significantly greater than expected probability of also occurring in shaded microhabitats and at higher latitudes, consistent with light as a common limiting factor. The findings suggest an important role for deeper habitats, particularly depths 30-45 m, in preserving evolutionary lineages of Indo-Pacific corals. Deeper reef areas are clearly more diverse than previously acknowledged and therefore deserve full consideration in our efforts to protect the world's coral reef biodiversity.

Microbiome variation in corals with distinct depth distribution ranges across a shallow-mesophotic gradient (15-85 m).

Mesophotic coral ecosystems (MCEs) are generally poorly studied, and our knowledge of lower MCEs (below 60 m depth) is largely limited to visual surveys. Here, we provide a first detailed assessment of the prokaryotic community associated with scleractinian corals over a depth gradient to the lower mesophotic realm (15-85 m). Specimens of three Caribbean coral species exhibiting differences in their depth distribution ranges (Agaricia grahamae, Madracis pharensis and Stephanocoenia intersepta) were collected with a manned submersible on the island of Curaçao, and their prokaryotic communities assessed using 16S rRNA gene sequencing analysis. Corals with narrower depth distribution ranges (depth-specialists) were associated with a stable prokaryotic community, whereas corals with a broader niche range (depth-generalists) revealed a higher variability in their prokaryotic community. The observed depth effects match previously described patterns in Symbiodinium depth zonation. This highlights the contribution of structured microbial communities over depth to the coral's ability to colonize a broader depth range.

Deep reefs are not universal refuges: Reseeding potential varies among coral species.

Deep coral reefs (that is, mesophotic coral ecosystems) can act as refuges against major disturbances affecting shallow reefs. It has been proposed that, through the provision of coral propagules, such deep refuges may aid in shallow reef recovery; however, this "reseeding" hypothesis remains largely untested. We conducted a genome-wide assessment of two scleractinian coral species with contrasting reproductive modes, to assess the potential for connectivity between mesophotic (40 m) and shallow (12 m) depths on an isolated reef system in the Western Atlantic (Bermuda). To overcome the pervasive issue of endosymbiont contamination associated with de novo sequencing of corals, we used a novel subtraction reference approach. We have demonstrated that strong depth-associated selection has led to genome-wide divergence in the brooding species Agaricia fragilis (with divergence by depth exceeding divergence by location). Despite introgression from shallow into deep populations, a lack of first-generation migrants indicates that effective connectivity over ecological time scales is extremely limited for this species and thus precludes reseeding of shallow reefs from deep refuges. In contrast, no genetic structuring between depths (or locations) was observed for the broadcasting species Stephanocoenia intersepta, indicating substantial potential for vertical connectivity. Our findings demonstrate that vertical connectivity within the same reef system can differ greatly between species and that the reseeding potential of deep reefs in Bermuda may apply to only a small number of scleractinian species. Overall, we argue that the "deep reef refuge hypothesis" holds for individual coral species during episodic disturbances but should not be assumed as a broader ecosystem-wide phenomenon.