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Climate change accelerates coral reef decline and jeopardizes recruitment essential for ecosystem recovery. Adult corals rely on a vital nutritional exchange with their symbiotic algae (Symbiodiniaceae), but the dynamics of reliance from fertilization to recruitment are understudied. We investigated the physiological, metabolomic, and transcriptomic changes across 13 developmental stages of Montipora capitata, a coral in Hawaiʻi that inherits symbionts from parent to egg. We found that embryonic development depends on maternally provisioned mRNAs and lipids, with a rapid shift to symbiont-derived nutrition in late developmental stages. Symbiont density and photosynthesis peak in swimming larvae to fuel pelagic dispersal. By contrast, respiratory demand increases significantly during metamorphosis and settlement, reflecting this energy-intensive morphological reorganization. Symbiont proliferation is driven by symbiont ammonium assimilation in larval stages with little evidence of nitrogen metabolism in the coral host. As development progresses, the host enhances nitrogen sequestration, regulating symbiont populations, and ensuring the transfer of fixed carbon to support metamorphosis, with both metabolomic and transcriptomic indicators of increased carbohydrate availability. Although algal symbiont community composition remained stable, bacterial communities shifted with ontogeny, associated with holobiont metabolic reorganization. Our study reveals extensive metabolic changes during development with increasing reliance on symbiont nutrition. Metamorphosis and settlement emerge as critical periods of energetic vulnerability to projected climate scenarios that destabilize symbiosis. This highly detailed characterization of symbiotic nutritional exchange during sensitive early life stages provides essential knowledge for understanding and forecasting the function of nutritional symbioses and, specifically, coral survival and recruitment in a future of climate change. 

Abstract Reef-building corals are integral ecosystem engineers in tropical coral reefs worldwide but are increasingly threatened by climate change and rising ocean temperatures. Consequently, there is an urgency to identify genetic, epigenetic, and environmental factors, and how they interact, for species acclimatization and adaptation. The availability of genomic resources is essential for understanding the biology of these organisms and informing future research needs for management and and conservation. The highly diverse coral genusAcroporaboasts the largest number of high-quality coral genomes, but these remain limited to a few geographic regions and highly studied species. Here we present the assembly and annotation of the genome and DNA methylome ofAcropora pulchrafrom Mo’orea, French Polynesia. The genome assembly was created from a combination of long-read PacBio HiFi data, from which DNA methylation data were also called and quantified, and additional Illumina RNASeq data forab initiogene predictions. The work presented here resulted in the most completeAcroporagenome to date, with a BUSCO completeness of 96.7% metazoan genes. The assembly size is 518 Mbp, with 174 scaffolds, and a scaffold N50 of 17 Mbp. Structural and functional annotation resulted in the prediction of a total of 40,518 protein-coding genes, and 16.74% of the genome in repeats. DNA methylation in the CpG context was 14.6% and predominantly found in flanking and gene body regions (61.7%). This reference assembly of theA. pulchragenome and DNA methylome will provide the capacity for further mechanistic studies of a common coastal coral in French Polynesia of great relevance for restoration and improve our capacity for comparative genomics inAcroporaand cnidarians more broadly. 

Reef-building corals are integral ecosystem engineers of tropical reefs but face threats from climate change. Investigating genetic, epigenetic, and environmental factors influencing their adaptation is critical. Genomic resources are essential for understanding coral biology and guiding conservation efforts. However, genomes of the coral genus Acropora are limited to highly-studied species. Here, we present the assembly and annotation of the genome and DNA methylome of Acropora pulchra from Mo’orea, French Polynesia. Using long-read PacBio HiFi and Illumina RNASeq, we generated the most complete Acropora genome to date (BUSCO completeness of 96.7% metazoan genes). The assembly size is 518 Mbp, with 174 scaffolds, and a scaffold N50 of 17 Mbp. We predicted 40,518 protein-coding genes and 16.74% of the genome in repeats. DNA methylation in the CpG context is 14.6%. This assembly of the A. pulchra genome and DNA methylome will support studies of coastal corals in French Polynesia, aiding conservation and comparative studies of Acropora and cnidarians. 

Identifying processes that promote coral reef recovery and resilience is crucial as ocean warming becomes more frequent and severe. Sexual reproduction is essential for the replenishment of coral populations and maintenance of genetic diversity; however, the ability for corals to reproduce may be impaired by marine heatwaves that cause coral bleaching. In 2014 and 2015, the Hawaiian Islands experienced coral bleaching with differential bleaching susceptibility in the speciesMontipora capitata, a dominant reef-building coral in the region. We tested the hypothesis that coral bleaching resistance enhances reproductive capacity and offspring performance by examining the reproductive biology of colonies that bleached and recovered (B) and colonies that did not bleach (NB) in 2015 in the subsequent spawning seasons. The proportion of colonies that spawned was higher in 2016 than in 2017. Regardless of parental bleaching history, we found eggs with higher abnormality and bundles with fewer eggs in 2016 than 2017. While reproductive output was similar between B and NB colonies in 2016, survivorship of offspring that year were significantly influenced by the parental bleaching history (egg donor × sperm donor: B × B, B × NB, NB × B, and NB × NB). Offspring produced by NB egg donors had the highest survivorship, while offspring from previously bleached colonies had the lowest survivorship, highlighting the negative effects of bleaching on parental investment and offspring performance. While sexual reproduction continues inM.capitatapost-bleaching, gametes are differentially impacted by recovery time following a bleaching event and by parental bleaching resistance. Our results demonstrate the importance of identifying bleaching resistant individuals during and after heating events. This study further highlights the significance of maternal effects through potential egg provisioning for offspring survivorship and provides a baseline for human-assisted intervention (i.e., selective breeding) to mitigate the effects of climate change on coral reefs. 

Rising sea surface temperatures are increasingly causing breakdown in the nutritional relationship between corals and algal endosymbionts (Symbiodiniaceae), threatening the basis of coral reef ecosystems and highlighting the critical role of coral reproduction in reef maintenance. The effects of thermal stress on metabolic exchange (i.e., transfer of fixed carbon photosynthates from symbiont to host) during sensitive early life stages, however, remains understudied. We exposed symbiotic Montipora capitata coral larvae in Hawaiʻi to high temperature (+2.5°C for 3 days), assessed rates of photosynthesis and respiration, and used stable isotope tracing (4 mM 13C sodium bicarbonate; 4.5 h) to quantify metabolite exchange. While larvae did not show any signs of bleaching and did not experience declines in survival and settlement, metabolic depression was significant under high temperature, indicated by a 19% reduction in respiration rates, but with no change in photosynthesis. Larvae exposed to high temperature showed evidence for maintained translocation of a major photosynthate, glucose, from the symbiont, but there was reduced metabolism of glucose through central carbon metabolism (i.e., glycolysis). The larval host invested in nitrogen cycling by increasing ammonium assimilation, urea metabolism, and sequestration of nitrogen into dipeptides, a mechanism that may support the maintenance of glucose translocation under thermal stress. Host nitrogen assimilation via dipeptide synthesis appears to be used for nitrogen limitation to the Symbiodiniaceae, and we hypothesize that nitrogen limitation contributes to retention of fixed carbon by favoring photosynthate translocation to the host. Collectively, our findings indicate that although these larvae are susceptible to metabolic stress under high temperature, diverting energy to nitrogen assimilation to maintain symbiont population density, photosynthesis, and carbon translocation may allow larvae to avoid bleaching and highlights potential life stage specific metabolic responses to stress. 

ABSTRACT As climate change increases the rate of environmental change and the frequency and intensity of disturbance events, selective forces intensify. However, given the complicated interplay between plasticity and selection for ecological – and thus evolutionary – outcomes, understanding the proximate signals, molecular mechanisms and the role of environmental history becomes increasingly critical for eco-evolutionary forecasting. To enhance the accuracy of our forecasting, we must characterize environmental signals at a level of resolution that is relevant to the organism, such as the microhabitat it inhabits and its intracellular conditions, while also quantifying the biological responses to these signals in the appropriate cells and tissues. In this Commentary, we provide historical context to some of the long-standing challenges in global change biology that constrain our capacity for eco-evolutionary forecasting using reef-building corals as a focal model. We then describe examples of mismatches between the scales of external signals relative to the sensors and signal transduction cascades that initiate and maintain cellular responses. Studying cellular responses at this scale is crucial because these responses are the basis of acclimation to changing environmental conditions and the potential for environmental ‘memory’ of prior or historical conditions through molecular mechanisms. To challenge the field, we outline some unresolved questions and suggest approaches to align experimental work with an organism's perception of the environment; these aspects are discussed with respect to human interventions. 

Abstract Standing genetic variation is a major driver of fitness and resilience and therefore of fundamental importance for threatened species such as stony corals. We analyzed RNA-seq data generated from 132 Montipora capitata and 119 Pocillopora acuta coral colonies collected from Kāneʻohe Bay, Oʻahu, Hawaiʻi. Our goals were to determine the extent of colony genetic variation and to study reproductive strategies in these two sympatric species. Surprisingly, we found that 63% of the P. acuta colonies were triploid, with putative independent origins of the different triploid clades. These corals have spread primarily via asexual reproduction and are descended from a small number of genotypes, whose diploid ancestor invaded the bay. In contrast, all M. capitata colonies are diploid and outbreeding, with almost all colonies genetically distinct. Only two cases of asexual reproduction, likely via fragmentation, were identified in this species. We report two distinct strategies in sympatric coral species that inhabit the largest sheltered body of water in the main Hawaiian Islands. These data highlight divergence in reproductive behavior and genome biology, both of which contribute to coral resilience and persistence.