Unlocking the single-cell mysteries of a reef-building coral.

Coral reefs are one of the most important ecosystems in the world but least understood from a cellular level. In this issue of Cell, Levy et al. unravel the single-cell gene expression of the coral holobiont and open the doors to better understand the novel diversity of cell types.

A stony coral cell atlas illuminates the molecular and cellular basis of coral symbiosis, calcification, and immunity.

Stony corals are colonial cnidarians that sustain the most biodiverse marine ecosystems on Earth: coral reefs. Despite their ecological importance, little is known about the cell types and molecular pathways that underpin the biology of reef-building corals. Using single-cell RNA sequencing, we define over 40 cell types across the life cycle of Stylophora pistillata. We discover specialized immune cells, and we uncover the developmental gene expression dynamics of calcium-carbonate skeleton formation. By simultaneously measuring the transcriptomes of coral cells and the algae within them, we characterize the metabolic programs involved in symbiosis in both partners. We also trace the evolution of these coral cell specializations by phylogenetic integration of multiple cnidarian cell type atlases. Overall, this study reveals the molecular and cellular basis of stony coral biology.

Coral Reef Population Genomics in an Age of Global Change.

Coral reefs are both exceptionally biodiverse and threatened by climate change and other human activities. Here, we review population genomic processes in coral reef taxa and their importance for understanding responses to global change. Many taxa on coral reefs are characterized by weak genetic drift, extensive gene flow, and strong selection from complex biotic and abiotic environments, which together present a fascinating test of microevolutionary theory. Selection, gene flow, and hybridization have played and will continue to play an important role in the adaptation or extinction of coral reef taxa in the face of rapid environmental change, but research remains exceptionally limited compared to the urgent needs. Critical areas for future investigation include understanding evolutionary potential and the mechanisms of local adaptation, developing historical baselines, and building greater research capacity in the countries where most reef diversity is concentrated.

Plastic pollution on the world's coral reefs.

Coral reefs are losing the capacity to sustain their biological functions1. In addition to other well-known stressors, such as climatic change and overfishing1, plastic pollution is an emerging threat to coral reefs, spreading throughout reef food webs2, and increasing disease transmission and structural damage to reef organisms3. Although recognized as a global concern4, the distribution and quantity of plastics trapped in the world's coral reefs remains uncertain3. Here we survey 84 shallow and deep coral ecosystems at 25 locations across the Pacific, Atlantic and Indian ocean basins for anthropogenic macrodebris (pollution by human-generated objects larger than 5 centimetres, including plastics), performing 1,231 transects. Our results show anthropogenic debris in 77 out of the 84 reefs surveyed, including in some of Earth's most remote and near-pristine reefs, such as in uninhabited central Pacific atolls. Macroplastics represent 88% of the anthropogenic debris, and, like other debris types, peak in deeper reefs (mesophotic zones at 30-150 metres depth), with fishing activities as the main source of plastics in most areas. These findings contrast with the global pattern observed in other nearshore marine ecosystems, where macroplastic densities decrease with depth and are dominated by consumer items5. As the world moves towards a global treaty to tackle plastic pollution6, understanding its distribution and drivers provides key information to help to design the strategies needed to address this ubiquitous threat.

Widespread retreat of coastal habitat is likely at warming levels above 1.5 °C.

Several coastal ecosystems-most notably mangroves and tidal marshes-exhibit biogenic feedbacks that are facilitating adjustment to relative sea-level rise (RSLR), including the sequestration of carbon and the trapping of mineral sediment1. The stability of reef-top habitats under RSLR is similarly linked to reef-derived sediment accumulation and the vertical accretion of protective coral reefs2. The persistence of these ecosystems under high rates of RSLR is contested3. Here we show that the probability of vertical adjustment to RSLR inferred from palaeo-stratigraphic observations aligns with contemporary in situ survey measurements. A deficit between tidal marsh and mangrove adjustment and RSLR is likely at 4 mm yr-1 and highly likely at 7 mm yr-1 of RSLR. As rates of RSLR exceed 7 mm yr-1, the probability that reef islands destabilize through increased shoreline erosion and wave over-topping increases. Increased global warming from 1.5 °C to 2.0 °C would double the area of mapped tidal marsh exposed to 4 mm yr-1 of RSLR by between 2080 and 2100. With 3 °C of warming, nearly all the world's mangrove forests and coral reef islands and almost 40% of mapped tidal marshes are estimated to be exposed to RSLR of at least 7 mm yr-1. Meeting the Paris agreement targets would minimize disruption to coastal ecosystems.

The evolution of fast-growing coral reef fishes.

Individual growth is a fundamental life history trait1-4, yet its macroevolutionary trajectories have rarely been investigated for entire animal assemblages. Here we analyse the evolution of growth in a highly diverse vertebrate assemblage-coral reef fishes. We combine state-of-the-art extreme gradient boosted regression trees with phylogenetic comparative methods to detect the timing, number, location and magnitude of shifts in the adaptive regime of somatic growth. We also explored the evolution of the allometric relationship between body size and growth. Our results show that the evolution of fast growth trajectories in reef fishes has been considerably more common than the evolution of slow growth trajectories. Many reef fish lineages shifted towards faster growth and smaller body size evolutionary optima in the Eocene (56-33.9 million years ago), pointing to a major expansion of life history strategies in this Epoch. Of all lineages examined, the small-bodied, high-turnover cryptobenthic fishes shifted most towards extremely high growth optima, even after accounting for body size allometry. These results suggest that the high global temperatures of the Eocene5 and subsequent habitat reconfigurations6 might have been critical for the rise and retention of the highly productive, high-turnover fish faunas that characterize modern coral reef ecosystems.

Coral reefs benefit from reduced land-sea impacts under ocean warming.

Coral reef ecosystems are being fundamentally restructured by local human impacts and climate-driven marine heatwaves that trigger mass coral bleaching and mortality1. Reducing local impacts can increase reef resistance to and recovery from bleaching2. However, resource managers lack clear advice on targeted actions that best support coral reefs under climate change3 and sector-based governance means most land- and sea-based management efforts remain siloed4. Here we combine surveys of reef change with a unique 20-year time series of land-sea human impacts that encompassed an unprecedented marine heatwave in Hawai'i. Reefs with increased herbivorous fish populations and reduced land-based impacts, such as wastewater pollution and urban runoff, had positive coral cover trajectories predisturbance. These reefs also experienced a modest reduction in coral mortality following severe heat stress compared to reefs with reduced fish populations and enhanced land-based impacts. Scenario modelling indicated that simultaneously reducing land-sea human impacts results in a three- to sixfold greater probability of a reef having high reef-builder cover four years postdisturbance than if either occurred in isolation. International efforts to protect 30% of Earth's land and ocean ecosystems by 2030 are underway5. Our results reveal that integrated land-sea management could help achieve coastal ocean conservation goals and provide coral reefs with the best opportunity to persist in our changing climate.

Continent-wide declines in shallow reef life over a decade of ocean warming.

Human society is dependent on nature1,2, but whether our ecological foundations are at risk remains unknown in the absence of systematic monitoring of species' populations3. Knowledge of species fluctuations is particularly inadequate in the marine realm4. Here we assess the population trends of 1,057 common shallow reef species from multiple phyla at 1,636 sites around Australia over the past decade. Most populations decreased over this period, including many tropical fishes, temperate invertebrates (particularly echinoderms) and southwestern Australian macroalgae, whereas coral populations remained relatively stable. Population declines typically followed heatwave years, when local water temperatures were more than 0.5 °C above temperatures in 2008. Following heatwaves5,6, species abundances generally tended to decline near warm range edges, and increase near cool range edges. More than 30% of shallow invertebrate species in cool latitudes exhibited high extinction risk, with rapidly declining populations trapped by deep ocean barriers, preventing poleward retreat as temperatures rise. Greater conservation effort is needed to safeguard temperate marine ecosystems, which are disproportionately threatened and include species with deep evolutionary roots. Fundamental among such efforts, and broader societal needs to efficiently adapt to interacting anthropogenic and natural pressures, is greatly expanded monitoring of species' population trends7,8.

Finding genes and pathways that underlie coral adaptation.

Mass coral bleaching is one of the clearest threats of climate change to the persistence of marine biodiversity. Despite the negative impacts of bleaching on coral health and survival, some corals may be able to rapidly adapt to warming ocean temperatures. Thus, a significant focus in coral research is identifying the genes and pathways underlying coral heat adaptation. Here, we review state-of-the-art methods that may enable the discovery of heat-adaptive loci in corals and identify four main knowledge gaps. To fill these gaps, we describe an experimental approach combining seascape genomics with CRISPR/Cas9 gene editing to discover and validate heat-adaptive loci. Finally, we discuss how information on adaptive genotypes could be used in coral reef conservation and management strategies.

Linking cell biology and ecology to understand coral symbiosis evolution.

Understanding the evolution of coral endosymbiosis requires a predictive framework that integrates life-history theory and ecology with cell biology. The time has come to bridge disciplines and use a model systems approach to achieve this aim.

Including environmental and climatic considerations for sustainable coral reef restoration.

Coral reefs provide ecosystem benefits to millions of people but are threatened by rapid environmental change and ever-increasing human pressures. Restoration is becoming a priority strategy for coral reef conservation, yet implementation remains challenging and it is becoming increasingly apparent that indirect conservation and restoration approaches will not ensure the long-term sustainability of coral reefs. The important role of environmental conditions in restoration practice are currently undervalued, carrying substantial implications for restoration success. Giving paramount importance to environmental conditions, particularly during the pre-restoration planning phase, has the potential to bring about considerable improvements in coral reef restoration and innovation. This Essay argues that restoration risk may be reduced by adopting an environmentally aware perspective that gives historical, contemporary, and future context to restoration decisions. Such an approach will open up new restoration opportunities with improved sustainability that have the capacity to dynamically respond to environmental trajectories.

Seasonal tissue-specific gene expression in wild crown-of-thorns starfish reveals reproductive and stress-related transcriptional systems.

Animals are influenced by the season, yet we know little about the changes that occur in most species throughout the year. This is particularly true in tropical marine animals that experience relatively small annual temperature and daylight changes. Like many coral reef inhabitants, the crown-of-thorns starfish (COTS), well known as a notorious consumer of corals and destroyer of coral reefs, reproduces exclusively in the summer. By comparing gene expression in 7 somatic tissues procured from wild COTS sampled on the Great Barrier Reef, we identified more than 2,000 protein-coding genes that change significantly between summer and winter. COTS genes that appear to mediate conspecific communication, including both signalling factors released into the surrounding sea water and cell surface receptors, are up-regulated in external secretory and sensory tissues in the summer, often in a sex-specific manner. Sexually dimorphic gene expression appears to be underpinned by sex- and season-specific transcription factors (TFs) and gene regulatory programs. There are over 100 TFs that are seasonally expressed, 87% of which are significantly up-regulated in the summer. Six nuclear receptors are up-regulated in all tissues in the summer, suggesting that systemic seasonal changes are hormonally controlled, as in vertebrates. Unexpectedly, there is a suite of stress-related chaperone proteins and TFs, including HIFa, ATF3, C/EBP, CREB, and NF-κB, that are uniquely and widely co-expressed in gravid females. The up-regulation of these stress proteins in the summer suggests the demands of oogenesis in this highly fecund starfish affects protein stability and turnover in somatic cells. Together, these circannual changes in gene expression provide novel insights into seasonal changes in this coral reef pest and have the potential to identify vulnerabilities for targeted biocontrol.

The effect of reef morphology on coral recruitment at multiple spatial scales.

Coral reefs are in decline worldwide, making it increasingly important to promote coral recruitment in new or degraded habitat. Coral reef morphology-the structural form of reef substrate-affects many aspects of reef function, yet the effect of reef morphology on coral recruitment is not well understood. We used structure-from-motion photogrammetry and airborne remote sensing to measure reef morphology (rugosity, curvature, slope, and fractal dimension) across a broad continuum of spatial scales and evaluated the effect of morphology on coral recruitment in three broadcast-spawning genera. We also measured the effect of other environmental and biotic factors such as fish density, adult coral cover, hydrodynamic larval import, and depth on coral recruitment. All variables combined explained 72% of coral recruitment in the study region. Coarse reef rugosity and curvature mapped at ≥2 m spatial resolution-such as large colonies, knolls, and boulders-were positively correlated with coral recruitment, explaining 22% of variation in recruitment. Morphology mapped at finer scales (≤32 cm resolution) was not significant. Hydrodynamic larval import was also positively related to coral recruitment in Porites and Montipora spp., and grazer fish density was linked to significantly lower recruitment in all genera. In addition, grazer density, reef morphology, and hydrodynamic import had differential effects on coral genera, reflecting genus-specific life history traits, and model performance was lower in gonochoric species. Overall, coral reef morphology is a key indicator of recruitment potential that can be detected by remote sensing, allowing potential larval sinks to be identified and factored into restoration actions.

Climate change impacts on mesophotic regions of the Great Barrier Reef.

Climate change projections for coral reefs are founded exclusively on sea surface temperatures (SST). While SST projections are relevant for the shallowest reefs, neglecting ocean stratification overlooks the striking differences in temperature experienced by deeper reefs for all or part of the year. Density stratification creates a buoyancy barrier partitioning the upper and lower parts of the water column. Here, we mechanistically downscale climate models and quantify patterns of thermal stratification above mesophotic corals (depth 30 to 50 m) of the Great Barrier Reef (GBR). Stratification insulates many offshore regions of the GBR from heatwaves at the surface. However, this protection is lost once global average temperatures exceed ~3 °C above preindustrial, after which mesophotic temperatures surpass a recognized threshold of 30 °C for coral mortality. Bottom temperatures on the GBR (30 to 50 m) from 2050 to 2060 are estimated to increase by ~0.5 to 1 °C under lower climate emissions (SSP1-1.9) and ~1.2 to 1.7 °C under higher climate emissions (SSP5-8.5). In short, mesophotic coral reefs are also threatened by climate change and research might prioritize the sensitivity of such corals to stress.

Combining environmental DNA and visual surveys can inform conservation planning for coral reefs.

Environmental DNA (eDNA) metabarcoding has the potential to revolutionize conservation planning by providing spatially and taxonomically comprehensive data on biodiversity and ecosystem conditions, but its utility to inform the design of protected areas remains untested. Here, we quantify whether and how identifying conservation priority areas within coral reef ecosystems differs when biodiversity information is collected via eDNA analyses or traditional visual census records. We focus on 147 coral reefs in Indonesia's hyper-diverse Wallacea region and show large discrepancies in the allocation and spatial design of conservation priority areas when coral reef species were surveyed with underwater visual techniques (fishes, corals, and algae) or eDNA metabarcoding (eukaryotes and metazoans). Specifically, incidental protection occurred for 55% of eDNA species when targets were set for species detected by visual surveys and 71% vice versa. This finding is supported by generally low overlap in detection between visual census and eDNA methods at species level, with more overlap at higher taxonomic ranks. Incomplete taxonomic reference databases for the highly diverse Wallacea reefs, and the complementary detection of species by the two methods, underscore the current need to combine different biodiversity data sources to maximize species representation in conservation planning.

High germline mutation rates, but not extreme population outbreaks, influence genetic diversity in a keystone coral predator.

Lewontin's paradox, the observation that levels of genetic diversity (π) do not scale linearly with census population size (Nc) variation, is an evolutionary conundrum. The most extreme mismatches between π and Nc are found for highly abundant marine invertebrates. Yet, the influences of new mutations on π relative to extrinsic processes such as Nc fluctuations are unknown. Here, we provide the first germline mutation rate (µ) estimate for a marine invertebrate in corallivorous crown-of-thorns sea stars (Acanthaster cf. solaris). We use high-coverage whole-genome sequencing of 14 parent-offspring trios alongside empirical estimates of Nc in Australia's Great Barrier Reef to jointly examine the determinants of π in populations undergoing extreme Nc fluctuations. The A. cf. solaris mean µ was 9.13 x 10-09 mutations per-site per-generation (95% CI: 6.51 x 10-09 to 1.18 x 10-08), exceeding estimates for other invertebrates and showing greater concordance with vertebrate mutation rates. Lower-than-expected Ne (~70,000-180,000) and low Ne/Nc values (0.0047-0.048) indicated weak influences of population outbreaks on long-term π. Our findings are consistent with elevated µ evolving in response to reduced Ne and generation time length, with important implications for explaining high mutational loads and the determinants of genetic diversity in marine invertebrate taxa.

Rapid physiological and transcriptomic changes associated with oxygen delivery in larval anemonefish suggest a role in adaptation to life on hypoxic coral reefs.

Connectivity of coral reef fish populations relies on successful dispersal of a pelagic larval phase. Pelagic larvae must exhibit high swimming abilities to overcome ocean and reef currents, but once settling onto the reef, larvae transition to endure habitats that become hypoxic at night. Therefore, coral reef fish larvae must rapidly and dramatically shift their physiology over a short period of time. Taking an integrative, physiological approach, using swimming respirometry, and examining hypoxia tolerance and transcriptomics, we show that larvae of cinnamon anemonefish (Amphiprion melanopus) rapidly transition between "physiological extremes" at the end of their larval phase. Daily measurements of swimming larval anemonefish over their entire early development show that they initially have very high mass-specific oxygen uptake rates. However, oxygen uptake rates decrease midway through the larval phase. This occurs in conjunction with a switch in haemoglobin gene expression and increased expression of myoglobin, cytoglobin, and neuroglobin, which may all contribute to the observed increase in hypoxia tolerance. Our findings indicate that critical ontogenetic changes in the gene expression of oxygen-binding proteins may underpin the physiological mechanisms needed for successful larval recruitment to reefs.

Ocean acidification does not impair the behaviour of coral reef fishes.

The partial pressure of CO2 in the oceans has increased rapidly over the past century, driving ocean acidification and raising concern for the stability of marine ecosystems1-3. Coral reef fishes are predicted to be especially susceptible to end-of-century ocean acidification on the basis of several high-profile papers4,5 that have reported profound behavioural and sensory impairments-for example, complete attraction to the chemical cues of predators under conditions of ocean acidification. Here, we comprehensively and transparently show that-in contrast to previous studies-end-of-century ocean acidification levels have negligible effects on important behaviours of coral reef fishes, such as the avoidance of chemical cues from predators, fish activity levels and behavioural lateralization (left-right turning preference). Using data simulations, we additionally show that the large effect sizes and small within-group variances that have been reported in several previous studies are highly improbable. Together, our findings indicate that the reported effects of ocean acidification on the behaviour of coral reef fishes are not reproducible, suggesting that behavioural perturbations will not be a major consequence for coral reef fishes in high CO2 oceans.

Global status and conservation potential of reef sharks.

Decades of overexploitation have devastated shark populations, leaving considerable doubt as to their ecological status1,2. Yet much of what is known about sharks has been inferred from catch records in industrial fisheries, whereas far less information is available about sharks that live in coastal habitats3. Here we address this knowledge gap using data from more than 15,000 standardized baited remote underwater video stations that were deployed on 371 reefs in 58 nations to estimate the conservation status of reef sharks globally. Our results reveal the profound impact that fishing has had on reef shark populations: we observed no sharks on almost 20% of the surveyed reefs. Reef sharks were almost completely absent from reefs in several nations, and shark depletion was strongly related to socio-economic conditions such as the size and proximity of the nearest market, poor governance and the density of the human population. However, opportunities for the conservation of reef sharks remain: shark sanctuaries, closed areas, catch limits and an absence of gillnets and longlines were associated with a substantially higher relative abundance of reef sharks. These results reveal several policy pathways for the restoration and management of reef shark populations, from direct top-down management of fishing to indirect improvement of governance conditions. Reef shark populations will only have a high chance of recovery by engaging key socio-economic aspects of tropical fisheries.

Oceanic forcing of penultimate deglacial and last interglacial sea-level rise.

Sea-level histories during the two most recent deglacial-interglacial intervals show substantial differences1-3 despite both periods undergoing similar changes in global mean temperature4,5 and forcing from greenhouse gases6. Although the last interglaciation (LIG) experienced stronger boreal summer insolation forcing than the present interglaciation7, understanding why LIG global mean sea level may have been six to nine metres higher than today has proven particularly challenging2. Extensive areas of polar ice sheets were grounded below sea level during both glacial and interglacial periods, with grounding lines and fringing ice shelves extending onto continental shelves8. This suggests that oceanic forcing by subsurface warming may also have contributed to ice-sheet loss9-12 analogous to ongoing changes in the Antarctic13,14 and Greenland15 ice sheets. Such forcing would have been especially effective during glacial periods, when the Atlantic Meridional Overturning Circulation (AMOC) experienced large variations on millennial timescales16, with a reduction of the AMOC causing subsurface warming throughout much of the Atlantic basin9,12,17. Here we show that greater subsurface warming induced by the longer period of reduced AMOC during the penultimate deglaciation can explain the more-rapid sea-level rise compared with the last deglaciation. This greater forcing also contributed to excess loss from the Greenland and Antarctic ice sheets during the LIG, causing global mean sea level to rise at least four metres above modern levels. When accounting for the combined influences of penultimate and LIG deglaciation on glacial isostatic adjustment, this excess loss of polar ice during the LIG can explain much of the relative sea level recorded by fossil coral reefs and speleothems at intermediate- and far-field sites.