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Coral spawning on the oceanic reef systems of north-western Australia was recently discovered during autumn and spring, but the degree to which species and particularly colonies participated in one or both of these spawnings was unknown. At the largest of the oceanic reef systems, the participation by colonies in the two discrete spawning events was investigated over three years in 13 species of Acropora corals (n = 1,855 colonies). Seven species spawned during both seasons; five only in autumn and one only in spring. The majority of tagged colonies (n = 218) spawned once a year in the same season, but five colonies from three species spawned during spring and autumn during a single year. Reproductive seasonality was not influenced by spatial variation in habitat conditions, or by Symbiodinium partners in the biannual spawner Acropora tenuis. Colonies of A. tenuis spawning during different seasons separated into two distinct yet cryptic groups, in a bayesian clustering analysis based on multiple microsatellite markers. These groups were associated with a major genetic divergence (G\"ST = 0.469), despite evidence of mixed ancestry in a small proportion of individuals. Our results confirm that temporal reproductive isolation is a common feature of Acropora populations at Scott Reef and indicate that spawning season is a genetically determined trait in at least A. tenuis. This reproductive isolation may be punctuated occasionally by interbreeding between genetic groups following favourable environmental conditions, when autumn spawners undergo a second annual gametogenic cycle and spawn during spring.

Knowledge of the degree to which corals undergo physiological acclimatization or genetic adaptation in response to changes in their thermal environment is crucial to the success of coral reef conservation strategies. The potential of corals to acclimatize to temperatures exceeding historical thermal regimes was investigated by reciprocal transplantation of Acropora millepora colonies between the warm central and cool southern regions of the Great Barrier Reef (GBR) for a duration of 14 months. Colony fragments retained at native sites remained healthy, whereas transplanted fragments, although healthy over initial months when temperatures remained within native thermal regimes, subsequently bleached and suffered mortality during seasonal temperature extremes. Corals hosting Symbiodinium D transplanted to the southern GBR bleached in winter and the majority suffered whole (40%; n = 20 colonies) or partial (50%) mortality at temperatures 1.1°C below their 15-year native minimum. In contrast, corals hosting Symbiodinium C2 transplanted to the central GBR bleached in summer and suffered whole (50%; n = 10 colonies) or partial (42%) mortality at temperatures 2.5°C above their 15-year native maximum. During summer bleaching, the dominant Symbiodinium type changed from C2 to D within corals transplanted to the central GBR. Corals transplanted to the cooler, southern GBR grew 74-80% slower than corals at their native site, and only 50% of surviving colonies reproduced, at least partially because of cold water bleaching of transplants. Despite the absence of any visual signs of stress, corals transplanted to the warmer, central GBR grew 52-59% more slowly than corals at their native site before the summer bleaching (i.e., from autumn to spring). Allocation of energy to initial acclimatization or reproduction may explain this pattern, as the majority (65%) of transplants reproduced one month earlier than portions of the same colonies retained at the southern native site. All parameters investigated (bleaching, mortality, Symbiodinium type fidelity, reproductive timing) demonstrated strong interactions between genotype and environment, indicating that the acclimatization potential of A. millepora populations may be limited by adaptation of the holobiont to native thermal regimes.

The ability of corals to adapt to global warming may involve trade-offs among the traits that influence their success as the foundational species of coral reefs.The ability of corals to adapt to global warming may involve trade-offs among the traits that influence their success as the foundational species of coral reefs.

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 °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 to thermal histories governs differences in coral heat tolerance between reefs, whereas within reefs, variations in heat tolerance cannot be explained by environmental predictors and may instead be a result of genomic variations, suggesting analyses of coral samples from the Great Barrier Reef.

Reef-building corals show a marked decrease in total species richness from the tropics to high latitude regions. Several hypotheses have been proposed to account for this pattern in the context of abiotic and biotic factors, including temperature thresholds, light limitation, aragonite saturation, nutrient or sediment loads, larval dispersal constraints, competition with macro-algae or other invertebrates, and availability of suitable settlement cues or micro-algal symbionts. Surprisingly, there is a paucity of data supporting several of these hypotheses. Given the immense pressures faced by corals in the Anthropocene, it is critical to understand the factors limiting their distribution in order to predict potential range expansions and the role that high latitude reefs can play as refuges from climate change. This review examines these factors and outlines critical research areas to address knowledge gaps in our understanding of light/temperature interactions, coral-Symbiodiniaceae associations, settlement cues, and competition in high latitude reefs.

Reef-building corals live very close to their upper thermal limits and their persistence is imperiled by a rapidly warming climate. Human interventions may be used to increase the thermal limits of sensitive corals by cross-breeding with heat-adapted populations. However, the scope of breeding interventions is constrained by regional variation in the annual reproductive cycle of corals. Here we use cryopreservation technology to overcome this barrier and cross-breed conspecific coral populations across ocean basins for the first time. During regional spawning events, sperm samples were cryopreserved from populations of the widespread Indo-Pacific coral, Platygyra daedalea , from the southern Persian Gulf (maximum daily sea surface temperature of 36 °C), the Oman Sea (33 °C), and the central Great Barrier Reef (30 °C). These sperm samples were thawed during a later spawning event to test their ability to fertilize freshly spawned eggs of P. daedalea colonies from the central Great Barrier Reef. Average fertilization success for the Persian Gulf (9%) and Oman Sea (6%) sperm were 1.4–2.5 times lower than those for the native cryopreserved sperm from Great Barrier Reef (13–15%), potentially due to lower sperm quality of the Middle Eastern sperm and/or reproductive incompatibility between these distant populations. Overall, fertilization success with cryopreserved sperm was low compared with fresh sperm (>80%), likely due to the low motility of thawed sperm (≤5%, reduced from 50% to >90% in fresh sperm). To evaluate whether cross-bred offspring had enhanced thermal tolerance, the survival of larvae sired by Persian Gulf cryopreserved sperm, Great Barrier Reef cryopreserved sperm, and Great Barrier Reef fresh sperm was monitored for six days at ambient (27 °C) and elevated (33 °C) temperature. Against expectations of thermal tolerance enhancement, survival of larvae sired by Persian Gulf cryopreserved sperm was 2.6 times lower than larvae sired by Great Barrier Reef fresh sperm at 33 °C (27% versus 71%), but did not differ at 27 °C (77% versus 84%). This lack of enhanced thermal tolerance was unlikely due to outbreeding depression as survival was equally poor in larvae sired by Great Barrier Reef cryopreserved sperm. Rather, follow-up tests showed that cryoprotectant exposure during fertilization (0.1% DMSO) has a negative effect on the survival of P. daedalea larvae which is exacerbated at elevated temperature. Collectively, our findings highlight challenges of breeding corals for enhanced thermal tolerance using cryopreserved sperm, which may be overcome by methodological advances in the collection and preservation of high-quality motile sperm and minimizing the exposure time of eggs to cryoprotectants.

The perception that the inheritance of phenotypic traits operates solely through genetic means is slowly being eroded: epigenetic mechanisms have been shown to induce heritable changes in gene activity in plants1,2 and metazoans1,3. Inheritance of DNA methylation patterns provides a potential pathway for environmentally induced phenotypes to contribute to evolution of species and populations1–5. However, in basal metazoans, it is unknown whether inheritance of CpG methylation patterns occurs across the genome (as in plants) or as rare exceptions (as in mammals)4. Here, we show that DNA methylation patterns in a reef-building coral are determined by genotype and developmental stage, as well as by parental environment. Transmission of CpG methylation from adults to their sperm and larvae demonstrates genome-wide inheritance. Variation in the hypermethylation of genes in adults and their sperm from distinct environments suggests intergenerational acclimatization to local temperature and salinity. Furthermore, genotype-independent adjustments of methylation levels in stress-related genes were strongly correlated with offspring survival rates under heat stress. These findings support a role of DNA methylation in the intergenerational inheritance of traits in corals, which could extend to enhancing their capacity to adapt to climate change.Intergenerational inheritance of traits in corals can help species survive environmental change. Examination of intergenerational DNA methylation profiles in a reef-building coral shows there to be genome-wide inheritance, with the potential for adaptive capacity to environmental stressors.

Sustained accretion of calcium carbonate (mostly by scleractinian corals) is fundamental for maintaining the structure and function of coral reef ecosystems, but may be greatly constrained by extreme and rapidly changing environmental conditions. Corals in the southern Persian Gulf already experience extreme temperature ranges (34C), chronic hypersalinity (>43 psu) and frequent light limitation (<100 μmol photons m-2 s-1). We compared annual rates of calcification for two of the most common massive coral species in the region (Platygyra daedalea and Cyphastrea microphthalma) along marked gradients in environmental conditions in the southern Persian Gulf and into the Oman Sea. Overall calcification rates were 32% higher in P. daedalea colonies (x̅ = 1.103 g cm-2 y-1, n = 46) than in C. microphthalma (x̅ = 0.835 g cm-2 y-1, n = 37), probably reflecting inter-specific differences in energy allocation and skeletal density. There was also considerable variation in calcification rates among individual colonies from the same locations that was unrelated to depth or photosymbiont type. However, most interestingly, P. daedalea and C. microphthalma exhibited contrasting trends in mean annual calcification rates across locations. For P. daedalea, calcification rates were lowest at Delma, where the minimum temperatures were lowest and salinity was highest, and increased across the southern Persian Gulf with increases in minimum temperatures and decreases in salinity. These data suggest that calcification rates of P. daedalea are most constrained by minimum temperatures, which is consistent with the strong relationship between annual calcification rates and minimum local temperatures recorded across the Indo-Pacific. Conversely, linear extension and calcification of C. microphthalma in the southern Persian Gulf was lowest at Ras Ghanada, where there was lowest light and highest maximum temperatures. These data reveal striking taxonomic differences in the specific environmental constraints on coral calcification, which will further reinforce changes in the structure of coral assemblages with ongoing global climate change.

The global marine environment has been impacted significantly by climate change. Ocean temperatures are rising, and the frequency, duration and intensity of marine heatwaves are increasing, particularly affecting coral reefs. Coral bleaching events are becoming more common, with less recovery time between events. Anomalous temperatures at the start of 2020 caused widespread bleaching across the Great Barrier Reef (GBR), extending to southern, previously less affected reefs such as One Tree Island. Here, nine video transects were conducted at One Tree Island, in the Capricorn Bunker Group, and analysed for community composition and diversity, and the extent of bleaching across taxa. Average live hard coral cover across the area was 11.62%, and almost half of this was identified as severely bleached. This bleaching event is concerning as it occurred in an area previously considered a potential refuge for corals and associated fauna from the risks of climate warming. Due to the global impacts of COVID-19 during 2020, this report provides one of potentially few monitoring efforts of coral bleaching.

Determining when corals reproduce has clear management and economic implications. Here we document the reproductive condition of corals in the genus Acropora on the island of Socotra in Yemen during February 2014. Twenty percent of colonies (n = 143) contained mature gametes and 28% had immature gametes indicating that spawning will occur in both February and March in 2014, confirming previous anecdotal reports of coral spawning at this time in Socotra. Acropora typically reproduce in synchrony with many other broadcast spawning scleractinian corals, and we therefore predict that many other species are reproductively active at this time of year.