Dr Emily Howells

The genetic diversity and connectivity of reef-building coral populations are key to their survival in warming oceans. Yet our understanding of corals' demographic resilience and adaptive potential is complicated by cryptic species diversity, wide geographic distributions, and complex coral-algal symbioses. To address these challenges, we investigated the genetic connectivity and diversity of the broadcast-spawning coral Acropora cf. spathulata and its associated Symbiodiniaceae across 29 reefs spanning the Great Barrier Reef, the Coral Sea, and New Caledonia, using whole-genome sequencing of 1,088 colonies. We identified four genetically distinct coral populations that diverged between 0.27 and 0.65 mya, likely due to geographic isolation across thousands of kilometers. These populations maintained asymmetrical gene flow along major ocean currents despite demographic isolation and sustained large local effective population sizes (∼2,900), supported by a high dispersal range of ∼100 km per generation. In contrast, their Symbiodiniaceae partners varied over finer spatial scales, with five distinct Cladocopium taxa distributed along latitudinal and cross-shore gradients, likely driven by local environmental conditions. These results suggest that high dispersal capacity and large local population size promote demographic resilience within reef systems, while environment-specific symbioses and long-distance gene flow across reef systems support adaptation and evolutionary rescue.

1. Climate change threatens coral reef ecosystems, motivating the development of restoration strategies such as selective breeding to enhance coral heat tolerance. Rapid heat stress assays offer promise for high‐throughput phenotyping in selective breeding programmes, but their effectiveness in detecting coral‐based heritable variation in heat tolerance remains unvalidated. Further, the existence of trade‐offs with heat tolerance are poorly studied.
2. We estimated thermal thresholds for photochemical efficiency and chlorophyll retention in gravid colonies of Acropora tersa and Acropora spathulata on the Great Barrier Reef and assessed a possible trade‐off with fecundity, because reduced fecundity of heat‐tolerant parental colonies could impact restoration stock production. Rankings of photochemical efficiency thermal thresholds were then used to select A . spathulata broodstock and predict offspring heat tolerance. 3. Fecundity (number of eggs per polyp) positively correlated with chlorophyll retention under rapid heat stress in Acropora spathulata but did not correlate with either trait in Acropora tersa . We found that offspring of colonies ranking in the top 25th percentile did not show significantly greater survival under 27.5°C or 35.5°C than offspring of colonies ranking in the bottom 25th percentile or offspring produced by gametes from all spawning colonies, regardless of their heat tolerance. Rankings of parental photochemical efficiency thermal thresholds therefore failed to predict larval heat tolerance, likely due to weak correlations between adult photophysiology and larval thermal tolerance traits and/or confounding maternal effects.
4. Practical implication . Rapid heat stress assays measuring broodstock photochemical efficiency are inadequate for informing the production of heat‐tolerant A. spathulata larvae, necessitating development of alternative high‐throughput broodstock screening methods that better capture heritable thermal tolerance.

Increasing trends of coral mortality are a challenge to coral reef management worldwide, and a need exists to identify the causes and pathways involved. Pathology is useful to help decipher potential causes of mortality in animals, because it illuminates agents associated with lesions and gives insights on the nature of how a host responds to said agents. To better understand the nature of threats facing corals in the Arabian Peninsula, we performed gross and microscopic pathology on corals from Saudi Arabia, Qatar, and the United Arab Emirates. Among 321 coral fragments examined from 21 genera, tissue loss was the most common lesion seen in 31% of samples, reflecting its widespread presence on reefs from the Arabian Peninsula. Histologically, 68% of lesions exhibited necrosis, predominantly in the basal body wall and surface body wall. Endolithic filamentous microalgae and sponges, originating from the skeleton, were associated with 57% and 39% of lesions, respectively, and were often linked to necrosis and hyaline membrane formation. Cell-associated microbial aggregates and coccidia were detected mainly in Acropora, Pocillopora, and Porites but were not associated with adverse host response. Notably, 69–100% of fragments showing lesions were female likely reflecting the temporal reproductive life history of corals in the region. Our findings highlight endolithic organisms as major contributors to coral tissue degradation in the Arabian Peninsula. Future studies might focus on drivers of endolithic microalgal and sponge dynamics in the region and their role in coral reef health.

Standing genetic variation in fitness-related traits is critical to determine how fast populations can adapt to climate warming but is unknown for many species. Here we show that heritable genetic variation in heat tolerance in reef-building coral populations is widespread and strongly associated with selective pressure imposed by marine heatwaves. Our findings suggest that coral populations may be adapting to warming consistent with recent increases in their upper thermal limits.

Coral reefs are increasingly threatened by climate change-induced stressors, including marine heatwaves, which can lead to coral mortality, reduced reproductive output, and compromised natural recovery. Successful coral reef recovery requires the settlement of coral larvae and recruitment in degraded areas, replenishing coral communities and promoting resilience. Some restoration strategies involve utilizing natural spawning slicks, composed of coral gametes and embryos, to produce larvae to reseed reefs. However, verifying the taxonomic composition of these slicks is challenging. Here, we tested the performance of two coral ITS primer sets, CoralITS2 and CoralITS2_acro, on mock communities to evaluate their ability to capture genera composition and relative abundances. Both primer sets demonstrated high accuracy (>97%) in detecting and quantifying coral taxa. Subsequently, these primers were applied to wild-collected spawning slicks from the Great Barrier Reef, revealing variation in scleractinian (reef-building) coral community composition among slicks. For the CoralITS2_acro assay, Acropora was consistently the most abundant resolved genus detected across wild slick sample sites, with the exception of samples from the Whitsundays region, where Platygyra was dominant. The CoralITS2 assay successfully differentiated reef-building (Scleractinian) corals from other co-occurring spawning taxa, such as soft corals, anemones, and sponges, and revealed that these other co-spawners dominated slicks at two sites. Our findings underscore the potential of eDNA-based monitoring as a scalable tool to confirm the presence and relative abundance of diverse coral assemblages in natural slicks, informing restoration efforts. By enabling the characterization and comparison of slick composition across large spatial and temporal scales, eDNA metabarcoding can support restoration practices that align with the ecological requirements of reef ecosystems, safeguarding biodiversity and promoting resilience against future disturbances.

Effective biodiversity conservation requires knowledge of species' distributions across large areas, yet prevalence data for marine sessile species is scarce, with traditional variables often unavailable at appropriate temporal and spatial resolutions. As marine organism distributions generally depend on terrain heterogeneity, topographic variables derived from digital elevation models (DEMs) can be useful proxies in ecological modelling, given appropriate spatial resolutions. Here, we use three reef‐building Acropora coral species across the Great Barrier Reef, Australia, in a case study to (1) assess high‐resolution bathymetry DEM sources for accuracy, (2) harness their derived topographic variables for regional coral species distribution models (SDMs), and (3) develop a transferable framework to produce, select and integrate multi‐resolution variables into marine spatial models. For this, we obtained and processed three distinct bathymetric digital depth models that we treat as DEMs, which are available across the GBR extent: (i) Allen Coral Atlas (ACA) at 10 m, (ii) DeepReef at 30 m and (iii) DeepReef at 100 m. We generalised the three DEMs to multiple nested spatial resolutions (15 m–120 m) and derived the same eight topographic variables to assess SDM sensitivity to bathymetry source and spatial resolution. The ACA and DeepReef DEMs shared similar vertical accuracies, each producing topographic variables relevant to marine SDMs. Slope and vector ruggedness measure (VRM), capturing hydrodynamic movement and shelter or exposure, were the most relevant variables in SDMs of all three species. Interestingly, variables at the finest resolution (15 m) were not always the most relevant for producing accurate coral SDMs, with optimal resolutions between 15 and 60 m depending on the variable type and species. Using multi‐resolution topographic variables in SDMs provided nuanced insights into the multiscale drivers of regional coral distributions. Drawing from this case study, we provide a practical and transferable framework to facilitate the adoption of multiscale SDMs for better‐informed conservation and management planning.

Reef-building coral populations face unprecedented threats from climate warming. Standing variation in heat tolerance is crucial for evolutionary processes necessary for corals to persist. Yet, the spatial distribution of heat-tolerant corals and the underlying factors that determine heat tolerance are poorly understood from individual to ecosystem scales. Here, we show extensive variation in the heat tolerance of a foundational coral species complex across the Great Barrier Reef. Thermal thresholds of 569 individuals differed by up to 7.3 degrees C across scales from meters to >1250 km. Variation in thresholds among reefs was consistent with local adaptation and acclimatization to historical and recent thermal history. However, variation within reefs was sometimes greater than among reefs and largely unexplained by environmental predictors, putative host species, or symbiont communities. This indicates that within-reef heat tolerance differences may be informed primarily by other factors, such as adaptive genomic variation. We anticipate our findings will inform conservation and restoration actions, including targeting individuals for selective breeding of enhanced heat tolerance.

Adaptation of reef-building corals to global warming depends upon standing heritable variation in tolerance traits upon which selection can act. Yet limited knowledge exists on heat-tolerance variation among conspecific individuals separated by metres to hundreds of kilometres. Here, we performed standardized acute heat-stress assays to quantify the thermal tolerance traits of 709 colonies of Acropora spathulata from 13 reefs spanning 1060 km (9.5° latitude) of the Great Barrier Reef. Thermal thresholds for photochemical efficiency and chlorophyll retention varied considerably among individual colonies both among reefs (approximately 6°C) and within reefs (approximately 3°C). Although tolerance rankings of colonies varied between traits, the most heat-tolerant corals (i.e. top 25% of each trait) were found at virtually all reefs, indicating widespread phenotypic variation. Reef-scale environmental predictors explained 12–62% of trait variation. Corals exposed to high thermal averages and recent thermal stress exhibited the greatest photochemical performance, probably reflecting local adaptation and stress pre-acclimatization, and the lowest chlorophyll retention suggesting stress pre-sensitization. Importantly, heat tolerance relative to local summer temperatures was the greatest on higher latitude reefs suggestive of higher adaptive potential. These results can be used to identify naturally tolerant coral populations and individuals for conservation and restoration applications.

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.

Scleractinian corals are colonial animals with a range of life history strategies, making up diverse species assemblages that define coral reefs. We tagged and tracked approximately 30 colonies from each of 11 species during seven trips spanning six years (2009-2015) in order to measure their vital rates and competitive interactions on the reef crest at Trimodal Reef, Lizard Island, Australia. Pairs of species were chosen from five growth forms where one species of the pair was locally rare (R) and the other common (C). The sampled growth forms were massive [Goniastrea pectinata (R) and G. retiformis (C)], digitate [Acropora humilis (R) and A. cf. digitifera (C)], corymbose [A. millepora (R) and A. nasuta (C)], tabular [A. cytherea (R) and A. hyacinthus (C)] and arborescent [A. robusta (R) and A. intermedia (C)]. An extra corymbose species with intermediate abundance, A. spathulata was included when it became apparent that A. millepora was too rare on the reef crest, making the 11 species in total. The tagged colonies were visited each year in the weeks prior to spawning. During visits, two or more observers each took 2-3 photographs of each tagged colony from directly above and on the horizontal plane with a scale plate to track planar area. Dead or missing colonies were recorded and new colonies tagged in order to maintain approximately 30 colonies per species throughout the six years of the study. In addition to tracking tagged corals, 30 fragments were collected from neighboring untagged colonies of each species for counting numbers of eggs per polyp (fecundity); and fragments of untagged colonies were brought into the laboratory where spawned eggs were collected for biomass and energy measurements. We also conducted surveys at the study site to generate size structure data for each species in several of the years. Each tagged colony photograph was digitized by at least two people. Therefore, we could examine sources of error in planar area for both photographers and outliners. Competitive interactions were recorded for a subset of species by measuring the margins of tagged colony outlines interacting with neighboring corals. The study was abruptly ended by Tropical Cyclone Nathan (Category 4) that killed all but nine of the over 300 tagged colonies in early 2015. Nonetheless, these data will be of use to other researchers interested in coral demography and coexistence, functional ecology, and parametrizing population, community and ecosystem models. The data set is not copyright restricted, and users should cite this paper when using the data.