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Once one of the predominant reef-building corals in the region, Acropora cervicornis is now a focal species of coral restoration efforts in Florida and the western Caribbean. Scientists and restoration practitioners have been independently collecting phenotypic data on genets of A. cervicornis grown in restoration nurseries. While these data are important for understanding the intraspecific response to varying environmental conditions, and thus the potential genetic contribution to phenotypic variation, in isolation these observations are of limited use for large-scale, multi- institution restoration efforts that are becoming increasingly necessary. Here, we present the Acropora cervicornis Data Coordination Hub, a web-accessible relational database to align disparate datasets to compare genet-specific performance. In this data descriptor, we release data for 248 genets evaluated across 38 separate traits. We present a framework to align datasets with the ultimate goal of facilitating informed, data-driven restoration throughout the Caribbean.

The congruence between phylogenies of tightly associated groups of organisms (cophylogeny) reflects evolutionary links between ecologically important interactions. However, despite being a classic example of an obligate symbiosis, tests of cophylogeny between scleractinian corals and their photosynthetic algal symbionts have been hampered in the past because both corals and algae contain genetically unresolved and morphologically cryptic species. Here, we studied co-occurring, cryptic Pocillopora species from Mo’orea, French Polynesia, that differ in their relative abundance across depth. We constructed new phylogenies of the host Pocillopora (using genomic loci, complete mitochondrial genomes, and thousands of single nucleotide polymorphisms) and their Symbiodiniaceae symbionts (using ITS2 and psbAncr markers) and tested for cophylogeny. The analysis supported the presence of five Pocillopora species on the fore-reef at Mo’orea that mostly hosted either Cladocopium latusorum or C. pacificum. Only Pocillopora species hosting C. latusorum, and that have similar relative abundances across depths, also hosted taxa from Symbiodinium and Durusdinium. In general, the Cladocopium phylogeny mirrored the Pocillopora phylogeny. Within Cladocopium species, lineages also differed in their associations with Pocillopora haplotypes, except those showing evidence of nuclear introgression, and with depth in the two most common Pocillopora species. We also found evidence for a new Pocillopora species (haplotype 10), that has so far only been sampled from French Polynesia, that warrants formal identification. The linked phylogenies of these Pocillopora and Cladocopium species and lineages suggest that symbiont speciation is driven by niche diversification in the host, but there is still evidence for symbiont flexibility in rare cases.

Context Coral reef resilience is the product of multiple interacting processes that occur across various interacting scales. This complexity presents challenges for identifying solutions to the ongoing worldwide decline of coral reef ecosystems that are threatened by both local and global human stressors. Objectives We highlight how coral reef resilience is studied at spatial, temporal, and functional scales, and explore emerging technologies that are bringing new insights to our understanding of reef resilience. We then provide a framework for integrating insights across scales by using new and existing technological and analytical tools. We also discuss the implications of scale on both the ecological processes that lead to declines of reefs, and how we study those mechanisms. Methods To illustrate, we present a case study from Kāneʻohe Bay, Hawaiʻi, USA, linking remotely sensed hyperspectral imagery to within-colony symbiont communities that show differential responses to stress. Results In doing so, we transform the scale at which we can study coral resilience from a few individuals to entire ecosystems. Conclusions Together, these perspectives guide best practices for designing management solutions that scale from individuals to ecosystems by integrating multiple levels of biological organization from cellular processes to global patterns of coral degradation and resilience.

Reef-building corals form nutritional symbioses with endosymbiotic dinoflagellates (Symbiodiniaceae), a relationship that facilitates the ecological success of coral reefs. These symbionts are mostly acquired anew each generation from the environment during early life stages ("horizontal transmission"). Symbiodiniaceae species exhibit trait variation that directly impacts the health and performance of the coral host under ocean warming. Here, we test the capacity for larvae of a horizontally transmitting coral, Acropora tenuis, to establish symbioses with Symbiodiniaceae species in four genera that have varying thermal thresholds (the common symbiont genera, Cladocopium and Durusdinium, and the less common Fugacium and Gerakladium). Over a 2-week period in January 2018, a series of both no-choice and four-way choice experiments were conducted at three temperatures (27, 30, and 31°C). Symbiont acquisition success and cell proliferation were measured in individual larvae. Larvae successfully acquired and maintained symbionts of all four genera in no-choice experiments, and80% of larvae were infected with at least three genera when offered a four-way choice. Unexpectedly, Gerakladium symbionts increased in dominance over time, and at high temperatures outcompeted Durusdinium, which is regarded as thermally tolerant. Although Fugacium displayed the highest thermal tolerance in culture and reached similar cell densities to the other three symbionts at 31°C, it remained a background symbiont in choice experiments, suggesting host preference for other symbiont species. Larval survivorship at 1 week was highest in larvae associated with Gerakladium and Fugacium symbionts at 27 and 30°C, however at 31°C, mortality was similar for all treatments. We hypothesize that symbionts that are currently rare in corals (e.g., Gerakladium) may become more common and widespread in early life stages under climate warming. Uptake of such symbionts may function as a survival strategy in the wild, and has implications for reef restoration practices that use sexually produced coral stock.

Background Historically, Hawai’i has had few massive coral bleaching events, until two consecutive heatwaves elevated seawater temperatures in 2014 and 2015. Consequent mortality and thermal stress were observed in the reef systems of Kane’ohe Bay (O’ahu). Two of the dominant species exhibited a phenotypic dichotomy of either bleaching resistance or susceptibility (Montipora capitata and Porites compressa), while a third species (Pocillopora acuta) was broadly susceptible to bleaching. In order to survey temporal shifts in the coral microbiomes during bleaching and recovery in all three of these coral species, 50 colonies were tagged and periodically monitored. Metabarcoding of three genetic markers (16S rRNA gene ITS1 and ITS2) followed by compositional approaches for community structure analysis, differential abundance and correlations for longitudinal data were used to temporally track and compare Bacteria/Archaea, Fungi and Symbiodiniaceae dynamics of the tagged colonies. Results Bleaching susceptible P. compressa corals recovered faster than P. acuta and Montipora capitata. Prokaryotic and algal microbiomes were majorly shaped by host species, and had no apparent pattern of temporal acclimatization in the overall community structure. Symbiodiniaceae signatures were identified at the colony scale, and were at times related to bleaching susceptibility, revealing higher intraspecific resolution than previously reported. Bacterial compositions were practically constant between bleaching phenotypes, and more diverse in P. acuta and M. capitata. P. compressa’s prokaryotic community was dominated by a single symbiotic bacterium. Fungal associates remained unexplored due to untargeted DNA co-amplification. Compositional approaches (via microbial balances) allowed the identification of fine-scale differences in the abundance of a consortium of microbes, driving changes by bleaching susceptibility and time across all hosts. Conclusions The three major coral reef founders in Kane’ohe Bay revealed different physiological and microbiome responses after 2014–2015 heatwaves. It is difficult to forecast though, a more successful strategy towards future scenarios of global warming. Differentially abundant microbial taxa across time and/or bleaching susceptibility were broadly shared between all hosts, suggesting that locally, the same microbes may modulate stress responses in sympatric coral species. Our study highlights the potential of investigating microbial balances to identify fine-scale microbiome changes, serving as local diagnostic tools of coral reef fitness.

Climate change-amplified heatwaves are known to drive extensive mortality in marine foundation species. However, a paucity of longitudinal genomic datasets has impeded understanding of how these rapid selection events alter species’ genetic structure. Impacts of these events may be exacerbated in species with obligate symbioses, where the genetics of multiple co-evolving species may be affected. Here, we tracked the symbiotic associations and fate of reef-building corals for six years through a prolonged heatwave. Coral genetics strongly predicted survival of the common coralPoritesthrough the event, with strong differential survival (15 to 64%) apparent across morphologically identical -but genetically distinct- lineages. The event also disrupted strong associations between coral lineages and their symbiotic partners, homogenizing symbiotic assemblages across lineages and reducing the specificity of coral-algal symbioses. These results highlight that marine heatwaves threaten cryptic genetic diversity of foundation species and have the potential to decouple tight relationships between co-evolving host-symbiont pairs.

Some reef-building corals form symbioses with multiple algal partners that differ in ecologically important traits like heat tolerance. Coral bleaching and recovery can drive symbiont community turnover toward more heat-tolerant partners, and this ‘adaptive bleaching’ response can increase future bleaching thresholds by 1–2°C, aiding survival in warming oceans. However, this mechanism of rapid acclimatization only occurs in corals that are compatible with multiple symbionts, and only when the disturbance regime and competitive dynamics among symbionts are sufficient to bring about community turnover. The full scope of coral taxa and ecological scenarios in which symbiont shuffling occurs remains poorly understood, though its prevalence is likely to increase as warming oceans boost the competitive advantage of heat-tolerant symbionts, increase the frequency of bleaching events, and strengthen metacommunity feedbacks. Still, the constraints, limitations, and potential tradeoffs of symbiont shuffling suggest it will not save coral reef ecosystems; however, it may significantly improve the survival trajectories of some, or perhaps many, coral species. Interventions to manipulate coral symbionts and symbiont communities may expand the scope of their adaptive potential, which may boost coral survival until climate change is addressed.

Algal symbiont shuffling in favour of more thermotolerant species has been shown to enhance coral resistance to heat-stress. Yet, the mechanistic underpinnings and long-term implications of these changes are poorly understood. This work studied the modifications in coral DNA methylation, an epigenetic mechanism involved in coral acclimatization, in response to symbiont manipulation and subsequent heat stress exposure. Symbiont composition was manipulated in the great star coral Montastraea cavernosa through controlled thermal bleaching and recovery, producing paired ramets of three genets dominated by either their native symbionts (genus Cladocopium) or the thermotolerant species (Durusdinium trenchi). Single-base genome-wide analyses showed significant modifications in DNA methylation concentrated in intergenic regions, introns and transposable elements. Remarkably, DNA methylation changes in response to heat stress were dependent on the dominant symbiont, with twice as many differentially methylated regions found in heat-stressed corals hosting different symbionts (Cladocopium vs. D. trenchii) compared to all other comparisons. Interestingly, while differential gene body methylation was not correlated with gene expression, an enrichment in differentially methylated regions was evident in repetitive genome regions. Overall, these results suggest that changes in algal symbionts favouring heat tolerant associations are accompanied by changes in DNA methylation in the coral host. The implications of these results for coral adaptation, along with future avenues of research based on current knowledge gaps, are discussed in the present work.

Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.

Prospects for coral persistence through increasingly frequent and extended heatwaves seem bleak. Coral recovery from bleaching is only known to occur after temperatures return to normal, and mitigation of local stressors does not appear to augment coral survival. Capitalizing on a natural experiment in the equatorial Pacific, we track individual coral colonies at sites spanning a gradient of local anthropogenic disturbance through a tropical heatwave of unprecedented duration. Unexpectedly, some corals survived the event by recovering from bleaching while still at elevated temperatures. These corals initially had heat-sensitive algal symbiont communities, endured bleaching, and then recovered through proliferation of heat-tolerant symbionts. This pathway to survival only occurred in the absence of strong local stressors. In contrast, corals in highly disturbed areas were already dominated by heat-tolerant symbionts, and despite initially resisting bleaching, these corals had no survival advantage in one species and 3.3 times lower survival in the other. These unanticipated connections between disturbance, coral symbioses and heat stress resilience reveal multiple pathways to coral survival through future prolonged heatwaves., Climate change and local anthropogenic stressors threaten the persistence of coral reefs. Here the authors track coral bleaching over the course of a heatwave and find that some colonies recovered from bleaching while high temperatures persisted, but only at sites lacking in other strong anthropogenic stressors.

Some reef corals form stable, dominant or codominant associations with multiple endosymbiotic dinoflagellate species (family Symbiodiniaceae). Given the immense genetic and physiological diversity within this family, Symbiodiniaceae community composition has the potential to impact the nutritional physiology and fitness of the cnidarian host and all associated symbionts. Here we assessed the impact of the symbiont community composition on the metabolome of the coral Montipora capitata in Kāne‘ohe Bay, Hawai‘i, where different colonies can be dominated by stress-tolerant Durusdinium glynnii or stress-sensitive Cladocopium spp. Based on our existing knowledge of these symbiont taxa, we hypothesised that the metabolite profile of D. glynnii-dominated corals would be consistent with poorer nutritional support of the host relative to those corals dominated by Cladocopium spp. However, comparative metabolite profiling revealed that the metabolite pools of the host and symbiont were unaffected by differences in the abundance of the two symbionts within the community. The abundance of the individual metabolites was the same in the host and in the endosymbiont regardless of whether the host was populated with D. glynnii or Cladocopium spp. These results suggest that coral-dinoflagellate symbioses have the potential to undergo physiological adjustments over time to accommodate differences in their resident symbionts. Such mechanisms may involve host heterotrophic compensation (increasing the level of nutrition generated by feeding relative to delivery from the algae), dynamic regulation of metabolic pathways when exchange of metabolites between the organisms differs, and/or modification of both the type and quantity of metabolites that are exchanged. We discuss these adjustments and the implications for the physiology and survival of reef corals under changing environmental regimes.

Increased ocean temperatures from anthropogenic climate change induce coral bleaching, the breakdown of symbioses between corals and photosynthetic dinoflagellates. However, some corals thrive in marginal, warm environments that exceed typical bleaching thresholds. Their survival may be mediated by specific genes within the coral host, association with heat-tolerant algal symbionts, and/or distinct bacterial communities. At Mermaid Reef in Great Abaco, The Bahamas, Orbicella faveolata colonies did not bleach during a warming event that reached 33.0 °C, while at Sandy Cay Reef (~ 18 km south), which reached only 32.0 °C, O. faveolata bleached extensively. To investigate abiotic and biotic factors contributing to Mermaid Reef’s higher thermal tolerance, we compared temperature, depth, and coral composition at each site and used microsatellite genotyping, quantitative PCR, and 16S rRNA metabarcoding to examine host genotype diversity, Symbiodiniaceae composition, and bacterial communities in O. faveolata. All O. faveolata colonies at the tolerant Mermaid Reef were clonemates and hosted exclusively Durusdinium symbionts, while colonies at Sandy Cay Reef comprised diverse genotypes and hosted varying proportions of four Symbiodiniaceae genera, which were primarily structured by depth. Mermaid Reef colonies also tended to have higher bacterial family richness than Sandy Cay Reef. These findings suggest that shallow, warm environments like Mermaid Reef may select for few, putatively heat-tolerant genotypes of corals and symbionts, and that while warming may greatly reduce genetic diversity, certain individuals may thrive. Such individuals existing today can provide valuable biological insights and resources for intervention conservation aimed at boosting reef resilience under climate change.

Coral reefs are increasingly experiencing stressful conditions, such as high temperatures, that cause corals to undergo bleaching, a process where they lose their photosynthetic algal symbionts. Bleaching threatens both corals’ survival and the health of the reef ecosystems they create. One possible mechanism for corals to resist bleaching is through association with stress-tolerant symbionts, which are resistant to bleaching but may be worse partners in mild conditions. Some corals have been found to associate with multiple symbiont species simultaneously, which potentially gives them access to the benefits of both stress-sensitive and -tolerant symbionts. However, within-host competition between symbionts may lead to competitive exclusion of one partner, and the consequences of associating with multiple partners simultaneously are not well understood. We modify a mechanistic model of coral-algal symbiosis to investigate the effect of environmental conditions on within-host competitive dynamics between stress-sensitive and -tolerant symbionts and the effect of access to a tolerant symbiont on the dynamics of recovery from bleaching. We found that the addition of a tolerant symbiont can increase host survival and recovery from bleaching in high-light conditions. Competitive exclusion of the tolerant symbiont occurred slowly at intermediate light levels. Interestingly, there were some cases of post-bleaching competitive exclusion after the tolerant symbiont had helped the host recover.

Dynamic Energy Budget models relate whole organism processes such as growth, reproduction and mortality to suborganismal metabolic processes. Much of their potential derives from extensions of the formalism to describe the exchange of metabolic products between organisms or organs within a single organism, for example the mutualism between corals and their symbionts. Without model simplification, such models are at risk of becoming parameter-rich and hence impractical. One natural simplification is to assume that some metabolic processes act on ‘fast’ timescales relative to others. A common strategy for formulating such models is to assume that ‘fast’ processes equilibrate immediately, while ‘slow’ processes are described by ordinary differential equations. This strategy can bring a subtlety with it. What if there are multiple, interdependent fast processes that have multiple equilibria, so that additional information is needed to unambiguously specify the model dynamics? This situation can easily arise in contexts where an organism or community can persist in a ‘healthy’ or an ‘unhealthy’ state with abrupt transitions between states possible. To approach this issue, we offer the following: (a) a method to unambiguously complete implicitly defined models by adding hypothetical ‘fast’ state variables; (b) an approach for minimizing the number of additional state variables in such models, which can simplify the numerical analysis and give insights into the model dynamics; and (c) some implications of the new approach that are of practical importance for model dynamics, e.g. on the bistability of flux dynamics and the effect of different initialization choices on model outcomes. To demonstrate those principles, we use a simplified model for root-shoot dynamics of plants and a related model for the interactions between corals and endosymbiotic algae that describes coral bleaching and recovery.

The rapid loss of reef-building corals owing to ocean warming is driving the development of interventions such as coral propagation and restoration, selective breeding and assisted gene flow. Many of these interventions target naturally heat-tolerant individuals to boost climate resilience, but the challenges of quickly and reliably quantifying heat tolerance and identifying thermotolerant individuals have hampered implementation. Here, we used coral bleaching automated stress systems to perform rapid, standardized heat tolerance assays on 229 colonies of Acropora cervicornis across six coral nurseries spanning Florida's Coral Reef, USA. Analysis of heat stress dose–response curves for each colony revealed a broad range in thermal tolerance among individuals (approx. 2.5°C range in F v /F m ED50), with highly reproducible rankings across independent tests ( r = 0.76). Most phenotypic variation occurred within nurseries rather than between them, pointing to a potentially dominant role of fixed genetic effects in setting thermal tolerance and widespread distribution of tolerant individuals throughout the population. The identification of tolerant individuals provides immediately actionable information to optimize nursery and restoration programmes for Florida's threatened staghorn corals. This work further provides a blueprint for future efforts to identify and source thermally tolerant corals for conservation interventions worldwide.

The purpose of this protocol is to quantify Cladocopium and Durusdinium Symbiodiniaceae cell ratio densities (symbiont to host cell ratios) from individual coral DNA samples using the StepOnePlus™ Real-Time PCR System. It allows for a quick assessment of the symbiont community composition and ratio using targeted primers.

Coral bleaching is the single largest global threat to coral reefs worldwide. Integrating the diverse body of work on coral bleaching is critical to understanding and combating this global problem. Yet investigating the drivers, patterns, and processes of coral bleaching poses a major challenge. A recent review of published experiments revealed a wide range of experimental variables used across studies. Such a wide range of approaches enhances discovery, but without full transparency in the experimental and analytical methods used, can also make comparisons among studies challenging. To increase comparability but not stifle innovation, we propose a common framework for coral bleaching experiments that includes consideration of coral provenance, experimental conditions, and husbandry. For example, reporting the number of genets used, collection site conditions, the experimental temperature offset(s) from the maximum monthly mean (MMM) of the collection site, experimental light conditions, flow, and the feeding regime will greatly facilitate comparability across studies. Similarly, quantifying common response variables of endosymbiont (Symbiodiniaceae) and holobiont phenotypes (i.e., color, chlorophyll, endosymbiont cell density, mortality, and skeletal growth) could further facilitate cross-study comparisons. While no single bleaching experiment can provide the data necessary to determine global coral responses of all corals to current and future ocean warming, linking studies through a common framework as outlined here, would help increase comparability among experiments, facilitate synthetic insights into the causes and underlying mechanisms of coral bleaching, and reveal unique bleaching responses among genets, species, and regions. Such a collaborative framework that fosters transparency in methods used would strengthen comparisons among studies that can help inform coral reef management and facilitate conservation strategies to mitigate coral bleaching worldwide. published

Many corals form close associations with a diverse assortment of coral-dwelling fishes and other fauna. As coral reefs around the world are increasingly threatened by mass bleaching events, it is important to understand how these biotic interactions influence corals' susceptibility to bleaching. We used dynamic energy budget modeling to explore how nitrogen excreted by coral-dwelling fish affects the physiological performance of host corals. In our model, fish presence influenced the functioning of the coral-Symbiodiniaceae symbiosis by altering nitrogen availability, and the magnitude and sign of these effects depended on environmental conditions. Although our model predicted that fish-derived nitrogen can promote coral growth, the relationship between fish presence and coral tolerance of photo-oxidative stress was non-linear. Fish excretions supported denser symbiont populations that provided protection from incident light through self-shading. However, these symbionts also used more of their photosynthetic products for their own growth, rather than sharing with the coral host, putting the coral holobiont at a higher risk of becoming carbon-limited and bleaching. The balance between the benefits of increased symbiont shading and costs of reduced carbon sharing depended on environmental conditions. Thus, while there were some scenarios under which fish presence increased corals' tolerance of light stress, fish could also exacerbate bleaching and slow or prevent subsequent recovery. We discuss how the contrast between the potentially harmful effects of fish predicted by our model and results of empirical studies may relate to key model assumptions that warrant further investigation. Overall, this study provides a foundation for future work on how coral-associated fauna influence the bioenergetics of their host corals, which in turn has implications for how these corals respond to bleaching-inducing stressors.

The absorbtion of human-emitted CO2 by the oceans (elevated PCO2) is projected to alter the physiological performance of coral reef organisms by perturbing seawater chemistry (i.e. ocean acidification). Simultaneously, greenhouse gas emissions are driving ocean warming and changes in irradiance (through turbidity and cloud cover), which have the potential to influence the effects of ocean acidification on coral reefs. Here, we explored whether physiological impacts of elevated PCO2 on a coral–algal symbiosis (Pocillopora acuta–Symbiodiniaceae) are mediated by light and/or temperature levels. In a 39 day experiment, elevated PCO2 (962 versus 431 µatm PCO2) had an interactive effect with midday light availability (400 versus 800 µmol photons m−2 s−1) and temperature (25 versus 29°C) on areal gross and net photosynthesis, for which a decline at 29°C was ameliorated under simultaneous high-PCO2 and high-light conditions. Light-enhanced dark respiration increased under elevated PCO2 and/or elevated temperature. Symbiont to host cell ratio and chlorophyll a per symbiont increased at elevated temperature, whilst symbiont areal density decreased. The ability of moderately strong light in the presence of elevated PCO2 to alleviate the temperature-induced decrease in photosynthesis suggests that higher substrate availability facilitates a greater ability for photochemical quenching, partially offsetting the impacts of high temperature on the photosynthetic apparatus. Future environmental changes that result in moderate increases in light levels could therefore assist the P. acuta holobiont to cope with the ‘one–two punch’ of rising temperatures in the presence of an acidifying ocean.

The purpose of this protocol is to quantify Cladocopium and Durusdinium Symbiodiniaceae cell ratio densities (symbiont to host cell ratios) from individual coral DNA samples using the StepOnePlus™ Real-Time PCR System. It allows for a quick assessment of the symbiont community composition and ratio using targeted primers.

Some corals may become more resistant to bleaching by shuffling their Symbiodiniaceae communities toward thermally tolerant species, and manipulations to boost the abundance of these symbionts in corals may increase resilience in warming oceans. However, the thermotolerant symbiont Durusdinium trenchii may reduce growth and fecundity in Caribbean corals, and these tradeoffs need to be better understood as this symbiont spreads through the region. We sought to understand how D. trenchii modulates coral gene expression by manipulating symbiont communities in Montastraea cavernosa to produce replicate ramets containing D. trenchii together with paired ramets of these same genets (n = 3) containing Cladocopium C3 symbionts. We then examined differences in global gene expression between corals hosting Durusdinium and Cladocopium under control temperatures, and in response to short-term heat stress. We identified numerous transcriptional differences associated with symbiont identity, which explained 2%-14% of the transcriptional variance. Corals with D. trenchii upregulated genes related to translation, ribosomal structure and biogenesis, and downregulated genes related to extracellular structures, and carbohydrate and lipid transport and metabolism, relative to corals with Cladocopium. Unexpectedly, these changes were similar to those observed in Cladocopium-dominated corals in response to heat stress, suggesting that thermotolerant D. trenchii may cause corals to increase expression of heat stress-responsive genes, explaining both the increased heat tolerance and the associated energetic tradeoffs in corals containing D. trenchii. These findings provide insight into the ecological changes occurring on contemporary coral reefs in response to climate change, and the diverse ways in which different symbionts modulate emergent phenotypes of their hosts.

Comparative analysis of the expanding genomic resources for scleractinian corals may provide insights into the evolution of these organisms, with implications for their continued persistence under global climate change. Here, we sequenced and annotated the genome of Pocillopora damicornis, one of the most abundant and widespread corals in the world. We compared this genome, based on protein-coding gene orthology, with other publicly available coral genomes (Cnidaria, Anthozoa, Scleractinia), as well as genomes from other anthozoan groups (Actiniaria, Corallimorpharia), and two basal metazoan outgroup phlya (Porifera, Ctenophora). We found that 46.6% of P. damicornis genes had orthologs in all other scleractinians, defining a coral ‘core’ genome enriched in basic housekeeping functions. Of these core genes, 3.7% were unique to scleractinians and were enriched in immune functionality, suggesting an important role of the immune system in coral evolution. Genes occurring only in P. damicornis were enriched in cellular signaling and stress response pathways, and we found similar immune-related gene family expansions in each coral species, indicating that immune system diversification may be a prominent feature of scleractinian coral evolution at multiple taxonomic levels. Diversification of the immune gene repertoire may underlie scleractinian adaptations to symbiosis, pathogen interactions, and environmental stress.

Scleractinian corals form symbioses with diverse photosynthetic dinoflagellates (genus Symbiodinium) that confer varying levels of performance and stress tolerance to their hosts. Variation in thermal stress susceptibility (i.e., bleaching) among conspecific corals is linked to variability in symbiont community composition, yet factors driving heterogeneous symbiont associations within a population are poorly understood. To investigate potential drivers, we characterized Symbiodinium communities in Montipora capitata (N = 707 colonies) across the biophysical regions, reef types, and depth range of Kāne‘ohe Bay (Hawai‘i, USA), where this dominant reef-builder associates with Symbiodinium spp. in clade C (C31) and/or D (S. glynnii), and occurs as brown and orange color morphs. The distribution of these traits was primarily influenced by depth: orange, D-dominated colonies were more prevalent in shallow, high light environments (

Dynamic symbioses with functionally diverse dinoflagellate algae in the genus Symbiodinium may allow some reef corals to alter their phenotypes through ‘symbiont shuffling’, or changes in symbiont community composition. In particular, corals may become more bleaching resistant by increasing the relative abundance of thermally tolerant Symbiodinium in clade D after bleaching. Despite the immediate relevance of this phenomenon to corals living in warming oceans—and to interventions aimed at boosting coral resilience—the mechanisms governing how, why, and when symbiont shuffling occurs are still poorly understood. Here, we performed controlled thermal bleaching and recovery experiments on three species of Caribbean corals hosting mixtures of D1a (S. trenchii) and other symbionts in clades B or C. We show that the degree of symbiont shuffling is related to (1) the duration of stress exposure and (2) the difference in photochemical efficiency (F v /F m) of co-occurring symbionts under stress (i.e., the ‘photochemical advantage’ of one symbiont over the other). The advantage of D1a under stress was greatest in Montastraea cavernosa, intermediate in Siderastrea siderea, and lowest in Orbicella faveolata and correlated positively with the magnitude of shuffling toward D1a. In holobionts where D1a had less of an advantage over co-occurring symbionts (i.e., only slightly higher F v /F m under stress), a longer stress duration was required to elicit commensurate increases in D1a abundance. In fact, across these three coral species, 92.9% of variation in the degree of symbiont shuffling could be explained by the time-integrated photochemical advantage of D1a under heat stress. Although F v /F m is governed by numerous factors that this study is unable to resolve mechanistically, its strong empirical relationship with symbiont shuffling helps elucidate general features that govern this process in reef corals, which will help refine predictions of coral responses to environmental change and inform interventions to manipulate symbiont communities to enhance coral resilience.

Anthropogenic climate change compromises reef growth as a result of increasing temperatures and ocean acidification. Scleractinian corals vary in their sensitivity to these variables, suggesting species composition will influence how reef communities respond to future climate change. Because data are lacking for many species, most studies that model future reef growth rely on uniform scleractinian calcification sensitivities to temperature and ocean acidification. In order to address this knowledge gap, calcification of twelve common and understudied Caribbean coral species was measured for two months under crossed temperatures (27°C, 30.3°C) and CO2 partial pressures (pCO2) (400, 900, 1300 μatm). Mixed effects models of calcification for each species were then used to project community-level scleractinian calcification using Florida Keys reef composition data and IPCC AR5 ensemble climate model data. Three of the four most abundant species, Orbicella faveolata, Montastraea cavernosa, and Porites astreoides, had negative calcification responses to both elevated temperature and pCO2. In the business-as-usual CO2 emissions scenario, reefs with high abundances of these species had projected end-of-century declines in scleractinian calcification of >50% relative to present-day rates. Siderastrea siderea, the other most-common species, was insensitive to both temperature and pCO2 within the levels tested here. Reefs dominated by this species had the most stable end-of-century growth. Under more optimistic scenarios of reduced CO2 emissions, calcification rates throughout the Florida Keys declined

Dredging poses a potential threat to coral reefs, yet quantifying impacts is often difficult due to the large spatial footprint of potential effects and co-occurrence of other disturbances. Here we analyzed in situ monitoring data and remotely-sensed sediment plumes to assess impacts of the 2013–2015 Port of Miami dredging on corals and reef habitat. To control for contemporaneous bleaching and disease, we analyzed the spatial distribution of impacts in relation to the dredged channel. Areas closer to dredging experienced higher sediment trap accumulation, benthic sediment cover, coral burial, and coral mortality, and our spatial analyses indicate that >560,000 corals were killed within 0.5 km, with impacts likely extending over 5–10 km. The occurrence of sediment plumes explained ~60% of spatial variability in measured impacts, suggesting that remotely-sensed plumes, when properly calibrated against in situ monitoring data, can reliably estimate the magnitude and extent of dredging impacts.

Regulating partner abunclance may allow symmotic organisms to mediate interaction outcomes, facilitating adaptive responses to environmental change. To explore the capacity for-adaptive regulation in an ecologically important endosymbiosis, we studied the population dynamics of symbiotic algae in reef-building corals under different abiotic contexts. We found high natural variability in symbiont abundance in corals across reefs, but this variability converged to different symbiont-specific abundances when colonies were maintained under constant conditions. When conditions changed seasonally, symbiont abundance readjusted to new equilibria. We explain these patterns using an a priori model of symbiotic costs and benefits to the coral host, which shows that the observed changes in symbiont abundance are consistent with the maximization of interaction benefit under different environmental conditions. These results indicate that, while regulating symbiont abundance helps hosts sustain maximum benefit in a dynamic environment, spatiotemporal variation in abiotic factors creates a broad range of symbiont abundances (and interaction outcomes) among corals that may account for observed natural variability in performance (e.g., growth rate) and stress tolerance (e.g., bleaching susceptibility). This cost or benefit framework provides a new perspective on the dynamic regulation of reef coral symbioses and illustrates that the dependence of interaction outcomes on biotic and abiotic contexts may be important in understanding how diverse mutualisms respond to environmental change.

Coral reef ecosystems owe their ecological success–and vulnerability to climate change–to the symbiotic metabolism of corals andSymbiodiniumspp. The urgency to understand and predict the stability and breakdown of these symbioses (i.e., coral ‘bleaching’) demands the development and application of theoretical tools. Here, we develop a dynamic bioenergetic model of coral-Symbiodiniumsymbioses that demonstrates realistic steady-state patterns in coral growth and symbiont abundance across gradients of light, nutrients, and feeding. Furthermore, by including a mechanistic treatment of photo-oxidative stress, the model displays dynamics of bleaching and recovery that can be explained as transitions between alternate stable states. These dynamics reveal that ‘healthy’ and ‘bleached’ states correspond broadly to nitrogen- and carbon-limitation in the system, with transitions between them occurring as integrated responses to multiple environmental factors. Indeed, a suite of complex emergent behaviors reproduced by the model (e.g., bleaching is exacerbated by nutrients and attenuated by feeding) suggests it captures many important attributes of the system; meanwhile, its modular framework and open source R code are designed to facilitate further problem-specific development. We see significant potential for this modeling framework to generate testable hypotheses and predict integrated, mechanistic responses of corals to environmental change, with important implications for understanding the performance and maintenance of symbiotic systems.

Coral reef ecosystems owe their ecological success - and vulnerability to climate change - to the symbiotic metabolism of corals and Symbiodinium spp. The urgency to understand and predict the stability and breakdown of these symbioses (i.e., coral 'bleaching') demands the development and application of theoretical tools. Here, we develop a dynamic bioenergetic model of coral-Symbiodinium symbioses that demonstrates realistic steady-state patterns in coral growth and symbiont abundance across gradients of light, nutrients, and feeding. Furthermore, by including a mechanistic treatment of photo-oxidative stress, the model displays dynamics of bleaching and recovery that can be explained as transitions between alternate stable states. These dynamics reveal that "healthy" and "bleached" states correspond broadly to nitrogen- and carbon-limitation in the system, with transitions between them occurring as integrated responses to multiple environmental factors. Indeed, a suite of complex emergent behaviors reproduced by the model (e.g., bleaching is exacerbated by nutrients and attenuated by feeding) suggests it captures many important attributes of the system; meanwhile, its modular framework and open source R code are designed to facilitate further problem-specific development. We see significant potential for this modeling framework to generate testable hypotheses and predict integrated, mechanistic responses of corals to environmental change, with important implications for understanding the performance and maintenance of symbiotic systems.

Reef corals are sensitive to thermal stress, which induces coral bleaching (the loss of algal symbionts), often leading to coral mortality. However, corals hosting certain symbionts (notably Symbiodinium in clade D) resist bleaching when exposed to high temperatures. To determine if these symbionts are also cold tolerant, we exposed corals hosting either Symbiodinium C3 or D1a to incremental warming (+1°C week−1 to 35°C) and cooling (−1°C week−1 to 15°C), and measured photodamage and symbiont loss. During warming to 33°C, C3-corals were photodamaged and lost >99% of symbionts, while D1a-corals experienced photodamage but did not bleach. During cooling, D1a-corals suffered more photodamage than C3-corals but still did not bleach, while C3-corals lost 94% of symbionts. These results indicate that photodamage does not always lead to bleaching, suggesting alternate mechanisms exist by which symbionts resist bleaching, and helping explain the persistence of D1a symbionts on recently-bleached reefs, with implications for the future of these ecosystems.

Ocean acidification (OA) is predicted to reduce reef coral calcification rates and threaten the long-term growth of coral reefs under climate change. Reduced coral growth at elevated p CO 2 may be buffered by sufficiently high irradiances; however, the interactive effects of OA and irradiance on other fundamental aspects of coral physiology, such as the composition and energetics of coral biomass, remain largely unexplored. This study tested the effects of two light treatments (7.5 versus 15.7 mol photons m −2 d −1 ) at ambient or elevated p CO 2 (435 versus 957 µatm) on calcification, photopigment and symbiont densities, biomass reserves (lipids, carbohydrates, proteins), and biomass energy content (kJ) of the reef coral Pocillopora acuta from Kāne‘ohe Bay, Hawai‘i. While p CO 2 and light had no effect on either area- or biomass-normalized calcification, tissue lipids gdw −1 and kJ gdw −1 were reduced 15% and 14% at high p CO 2 , and carbohydrate content increased 15% under high light. The combination of high light and high p CO 2 reduced protein biomass (per unit area) by approximately 20%. Thus, under ecologically relevant irradiances, P. acuta in Kāne‘ohe Bay does not exhibit OA-driven reductions in calcification reported for other corals; however, reductions in tissue lipids, energy content and protein biomass suggest OA induced an energetic deficit and compensatory catabolism of tissue biomass. The null effects of OA on calcification at two irradiances support a growing body of work concluding some reef corals may be able to employ compensatory physiological mechanisms that maintain present-day levels of calcification under OA. However, negative effects of OA on P. acuta biomass composition and energy content may impact the long-term performance and scope for growth of this species in a high p CO 2 world.

The growth and survival of reef corals are influenced by their symbiotic algal partners (Symbiodinium spp.), which may be flexible in space and time. Tradeoffs among partnerships exist such that corals with thermotol- erant symbionts (e.g., clade D) resist bleaching but grow more slowly, making the long-term ecosystem-level impacts of different host-symbiont associations uncertain. However, much of this uncertainty is due to limited data regarding these tradeoffs and particularly how they are mediated by the environment. To address this knowledge gap, we measured growth and survival of Pocillopora damicornis with thermally sensitive (clade C) or tolerant (clade D) symbionts at three temperatures over 18-55 weeks. Warming reduced coral growth overall, but altered the tradeoffs associated with symbiont type. While clade D corals grew 35-40 % slower than clade C corals at cooler temperatures (26 C), warming of 1.5-3 C reduced and eliminated this growth disadvantage. These results suggest that although warmer oceans will negatively impact corals, clade D may enhance survival at no cost to growth relative to clade C. Understanding these genotype- environment interactions can help improve modeling efforts and conservation strategies for reefs under global climate change.

Mutualistic organisms can be particularly susceptible to climate change stress, as their survivorship is often limited by the most vulnerable partner. However, symbiotic plasticity can also help organisms in changing environments by expanding their realized niche space. Coral–algal (Symbiodinium spp.) symbiosis exemplifies this dichotomy: the partnership is highly susceptible to ‘bleaching’ (stress-induced symbiosis breakdown), but stress-tolerant symbionts can also sometimes mitigate bleaching. Here, we investigate the role of diverse and mutable symbiotic partnerships in increasing corals' ability to thrive in high temperature conditions. We conducted repeat bleaching and recovery experiments on the coral Montastraea cavernosa, and used quantitative PCR and chlorophyll fluorometry to assess the structure and function of Symbiodinium communities within coral hosts. During an initial heat exposure (32 °C for 10 days), corals hosting only stress-sensitive symbionts (Symbiodinium C3) bleached, but recovered (at either 24 °C or 29 °C) with predominantly (>90%) stress-tolerant symbionts (Symbiodinium D1a), which were not detected before bleaching (either due to absence or extreme low abundance). When a second heat stress (also 32 °C for 10 days) was applied 3 months later, corals that previously bleached and were now dominated by D1a Symbiodinium experienced less photodamage and symbiont loss compared to control corals that had not been previously bleached, and were therefore still dominated by Symbiodinium C3. Additional corals that were initially bleached without heat by a herbicide (DCMU, at 24 °C) also recovered predominantly with D1a symbionts, and similarly lost fewer symbionts during subsequent thermal stress. Increased thermotolerance was also not observed in C3-dominated corals that were acclimated for 3 months to warmer temperatures (29 °C) before heat stress. These findings indicate that increased thermotolerance post-bleaching resulted from symbiont community composition changes, not prior heat exposure. Moreover, initially undetectable D1a symbionts became dominant only after bleaching, and were critical to corals' resilience after stress and resistance to future stress.

Corals in the genus Pocillopora are the primary framework builders of eastern tropical Pacific (ETP) reefs. These corals typically associate with algal symbionts (genus Symbiodinium) in clade C and/or D, with clade D associations having greater thermal tolerance and resistance to bleaching. Recently, cryptic "species" delineations within both Pocillopora and Symbiodinium have been suggested, with host–symbiont specificity used as a supporting taxonomic character in both genera. In particular, it has been suggested that three lineages of Pocillopora (types 1–3) exist in the ETP, of which type 1 is the exclusive host of heat-tolerant Symbiodinium D1. This host specificity has been used to support the species name "Symbiodinium glynni" for this symbiont. To validate these host–symbiont relationships and their taxonomic utility, we identified Pocillopora types and their associated Symbiodinium at three sites in the ETP. We found greater flexibility in host–symbiont combinations than previously reported, with both Pocillopora types 1 and 3 able to host and be dominated by Symbiodinium in clade C or D. The prevalence of certain combinations did vary among sites, showing that a gradient of specificity exists which may be mediated by evolutionary relationships and environmental disturbance history. However, these results limit the utility of apparent host–symbiont specificity (which may have been a result of undersampling) in defining species boundaries in either corals or Symbiodinium. They also suggest that a greater diversity of corals may benefit from the thermal tolerance of clade D symbionts, affirming the need to conserve Pocillopora across its entire geographic and environmental range.

Reef corals are sensitive to thermal stress, which induces coral bleaching (the loss of algal symbionts), often leading to coral mortality. However, corals hosting certain symbionts (notably some members of

Coral reefs of the eastern tropical Pacific (ETP) are unique in being the only reef region in the world that has experienced multiple episodes of mass coral bleaching while also being exposed to chronically depressed aragonite saturation states as a result of regional upwelling. These characteristics make them ideal case studies for the continued effects of climate change on coral reefs, and in particular for the responses of reef corals and their dinoflagellate algal symbionts (Symbiodinium spp.) to combined climate stressors. As a result, the diversity, distribution and stability of Symbiodinium in ETP corals have been studied since the mid-1990s, shortly after contemporary molecular methods to identify Symbiodinium were first developed. ETP reefs have been instrumental in the discovery that certain members of Symbiodinium in clade D impart bleaching resistance to their coral hosts. In the ETP, clade D is represented by a single symbiont type (D1, also referred to as S. glynni), which has been shown to be tolerant of both episodic El Nino-driven high temperature stress (e.g., 1997 in the Gulf of Chiriqui, Panama), and low temperature stress during an unusually cold winter (e.g., 2008 in Baja California, Mexico). Virtually all studies in the region have focused on corals in the genus Pocillopora, which is both the dominant reef-building genus and the most symbiotically diverse, being the only coral genus in the ETP that routinely hosts heat tolerant D1 symbionts at high abundance. There is debate over the mechanisms by which D1 becomes dominant on pocilloporid reefs, with evidence for both differential mortality of corals, and dynamic change in symbiont communities in response to thermal history and/or disturbance. The relative importance of these two mechanisms is likely to be critical in determining reef survival trajectories over the coming century, as is the degree to which non-pocilloporid corals in the region can associate with, or become dominated by, D1. Dynamic change in symbiont communities may allow corals to survive recurrent bleaching events if stepwise increases in the abundance of D1 following each bleaching event allow these thermotolerant symbionts to accumulate. However, controlled experiments and continued monitoring are required to resolve the debate over symbiont stability versus lability, and there may be significant differences in coral response across the region. Finally, understanding whether different Symbiodinium can alter coral response to high CO2 or depressed aragonite saturation state (Ωarag) remains a priority research area for the region, especially given the potential for strong interactions between Ωarag, coral growth, and symbiont community structure.

For many coral species, the obligate association with phylogenetically diverse algal endosymbiont species is dynamic in time and space. Here, we used controlled laboratory inoculations of newly settled, aposymbiotic corals (Orbicella faveolata) with two cultured species of algal symbiont (Symbiodinium microadriaticum and S. minutum) to examine the role of symbiont identity on growth, survivorship, and thermal tolerance of the coral holobiont. We evaluated these data in the context of Symbiodinium photophysiology for 9 months post-settlement and also during a 5-d period of elevated temperatures Our data show that recruits that were inoculated with S. minutum grew significantly slower than those inoculated with S. microadriaticum (occasionally co-occurring with S. minutum), but that there was no difference in survivorship of O. faveolata polyps infected with Symbiodinium. However, photophysiological metrics (∆Fv/F'm, the efficiency with which available light is used to drive photosynthesis and α, the maximum light utilization coefficient) were higher in those slower growing recruits containing S. minutum. These findings suggest that light use (i.e., photophysiology) and carbon acquisition by the coral host (i.e., host growth) are decoupled, but did not distinguish the source of this difference. Neither Symbiodinium treatment demonstrated a significant negative effect of a 5-d exposure to temperatures as high as 32°C under low light conditions similar to those measured at settlement habitats.

Understanding the factors that influence coral susceptibility to thermally induced bleaching may aid reef management efforts. Now corals with high symbiont cell densities are shown to be more susceptible to bleaching, indicating that environmental conditions which increase symbiont densities—such as nutrient pollution—could exacerbate climate-induced coral bleaching.