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Predicting how reef-building corals will respond to accelerating ocean warming caused by climate change requires knowledge of how acclimation and symbiosis modulate heat tolerance in coral early life-history stages. We assayed transcriptional responses to heat in larvae and juveniles of 11 reproductive crosses of Acropora tenuis colonies along the Great Barrier Reef. Larvae produced from the warmest reef had the highest heat tolerance, although gene expression responses to heat were largely conserved by cross identity. Juvenile transcriptional responses were driven strongly by symbiosis – when in symbiosis with heat-evolved Symbiodiniaceae, hosts displayed intermediate expression between its progenitor Cladocopium and the more stress tolerant Durusdinium , indicating the acquisition of tolerance is a conserved evolutionary process in symbionts. Heat-evolved Symbiodiniaceae facilitated juvenile survival under heat stress, although host transcriptional responses to heat were positively correlated among those hosting different genera of Symbiodiniaceae. These findings reveal the relative contribution of parental environmental history as well as symbiosis establishment in coral molecular responses to heat in early life-history stages. Coral responses to ocean warming depend not only on the coral themselves, but also on their symbionts. Here, the authors experimentally assess how symbiosis and gene expression plasticity contribute to the heat stress responses of a common coral.

The dinoflagellate-coral partnership influences the coral holobiont’s tolerance to thermal stress and bleaching. However, the comparative roles of host genetic versus environmental factors in determining the composition of this symbiosis are largely unknown. Here we quantify the heritability of the initial Symbiodinium communities for two broadcast-spawning corals with different symbiont transmission modes: Acropora tenuis has environmental acquisition, whereas Montipora digitata has maternal transmission. Using high throughput sequencing of the ITS-2 region to characterize communities in parents, juveniles and eggs, we describe previously undocumented Symbiodinium diversity and dynamics in both corals. After one month of uptake in the field, Symbiodinium communities associated with A . tenuis juveniles were dominated by A3, C1, D1, A-type CCMP828, and D1a in proportional abundances conserved between experiments in two years. M . digitata eggs were predominantly characterized by C15, D1, and A3. In contrast to current paradigms, host genetic influences accounted for a surprising 29% of phenotypic variation in Symbiodinium communities in the horizontally-transmitting A . tenuis , but only 62% in the vertically-transmitting M . digitata . Our results reveal hitherto unknown flexibility in the acquisition of Symbiodinium communities and substantial heritability in both species, providing material for selection to produce partnerships that are locally adapted to changing environmental conditions.

Coral-reef ecosystems are experiencing frequent and severe disturbance events that are reducing global coral abundance and potentially overwhelming the natural capacity for reefs to recover. While mitigation strategies for climate warming and other anthropogenic disturbances are implemented, coral restoration programmes are being established worldwide as an additional conservation measure to minimise coral loss and enhance coral recovery. Current restoration efforts predominantly rely on asexually produced coral fragments—a process with inherent practical constraints on the genetic diversity conserved and the spatial scale achieved. Because the resilience of coral communities has hitherto relied on regular renewal with natural recruits, the scaling-up of restoration programmes would benefit from greater use of sexually produced corals, which is an approach that is gaining momentum. Here we review the present state of knowledge of scleractinian coral sexual reproduction in the context of reef restoration, with a focus on broadcast- spawning corals. We identify key knowledge gaps and bottlenecks that currently constrain the sexual production of corals and consider the feasibility of using sexually produced corals for scaling-up restoration to the reef- and reef-system scales.

The capacity of reef-building corals to associate with environmentally-appropriate types of endosymbionts from the dinoflagellate genus Symbiodinium contributes significantly to their success at local scales. Additionally, some corals are able to acclimatize to environmental perturbations by shuffling the relative proportions of different Symbiodinium types hosted. Understanding the dynamics of these symbioses requires a sensitive and quantitative method of Symbiodinium genotyping. Electrophoresis methods, still widely utilized for this purpose, are predominantly qualitative and cannot guarantee detection of a background type below 10% of the total Symbiodinium population. Here, the relative abundances of four Symbiodinium types (A13, C1, C3, and D1) in mixed samples of known composition were quantified using deep sequencing of the internal transcribed spacer of the ribosomal RNA gene (ITS-2) by means of Next Generation Sequencing (NGS) using Roche 454. In samples dominated by each of the four Symbiodinium types tested, background levels of the other three types were detected when present at 5%, 1%, and 0.1% levels, and their relative abundances were quantified with high (A13, C1, D1) to variable (C3) accuracy. The potential of this deep sequencing method for resolving fine-scale genetic diversity within a symbiont type was further demonstrated in a natural symbiosis using ITS-1, and uncovered reef-specific differences in the composition of Symbiodinium microadriaticum in two species of acroporid corals (Acropora digitifera and A. hyacinthus) from Palau. The ability of deep sequencing of the ITS locus (1 and 2) to detect and quantify low-abundant Symbiodinium types, as well as finer-scale diversity below the type level, will enable more robust quantification of local genetic diversity in Symbiodinium populations. This method will help to elucidate the role that background types have in maximizing coral fitness across diverse environments and in response to environmental change.

Adult organisms may “prime” their offspring for environmental change through a number of genetic and non-genetic mechanisms, termed parental effects. Some coral species may shuffle the proportions of Symbiodiniaceae within their endosymbiotic communities, subsequently altering their thermal tolerance, but it is unclear if shuffled communities are transferred to offspring. We evaluated Symbiodiniaceae community composition in tagged colonies of Montipora digitata over two successive annual spawning seasons and the 2016 bleaching event on the Great Barrier Reef. ITS2 amplicon sequencing was applied to four families (four maternal colonies and 10–12 eggs per family) previously sampled and sequenced the year before to characterize shuffling potential in these M. digitata colonies and determine if shuffled abundances were preserved in gametes. Symbiont densities and photochemical efficiencies differed significantly among adults in 2016, suggesting differential responses to increased temperatures. Low-abundance (“background”) sequence variants differed more among years than between maternal colonies and offspring. Results indicate that shuffling can occur in a canonically ‘stable’ symbiosis, and that the shuffled community is heritable. Hence, acclimatory changes like shuffling of the Symbiodiniaceae community are not limited to the lifetime of an adult coral and that shuffled communities are inherited across generations in a species with vertical symbiont transmission. Although previously hypothesized, to our knowledge, this is the first evidence that shuffled Symbiodiniaceae communities (at both the inter- and intra- genera level) can be inherited by offspring and supports the hypothesis that shuffling in microbial communities may serve as a mechanism of rapid coral acclimation to changing environmental conditions.

The speed at which species adapt depends partly on the rates of beneficial adaptation generation and how quickly they spread within and among populations. Natural rates of adaptation of corals may not be able to keep pace with climate warming. Several interventions have been proposed to fast‐track thermal adaptation, including the intentional translocation of warm‐adapted adults or their offspring (assisted gene flow, AGF) and the ex situ crossing of warm‐adapted corals with conspecifics from cooler reefs (hybridization or selective breeding) and field deployment of those offspring. The introgression of temperature tolerance loci into the genomic background of cooler‐environment corals aims to facilitate adaptation to warming while maintaining fitness under local conditions. Here we use research on selective sweeps and connectivity to understand the spread of adaptive variants as it applies to AGF on the Great Barrier Reef (GBR), focusing on the genus Acropora. Using larval biophysical dispersal modeling, we estimate levels of natural connectivity in warm‐adapted northern corals. We then model the spread of adaptive variants from single and multiple reefs and assess if the natural and assisted spread of adaptive variants will occur fast enough to prepare receiving central and southern populations given current rates of warming. We also estimate fixation rates and spatial extent of fixation under multiple release scenarios to inform intervention design. Our results suggest that thermal tolerance is unlikely to spread beyond northern reefs to the central and southern GBR without intervention, and if it does, 30+ generations are needed for adaptive gene variants to reach fixation even under multiple release scenarios. We argue that if translocation, breeding, and reseeding risks are managed, AGF using multiple release reefs can be beneficial for the restoration of coral populations. These interventions should be considered in addition to conventional management and accompanied by strong mitigation of CO2 emissions.

Determining the extent to which Symbiodinium communities in corals are inherited versus environmentally acquired is fundamental to understanding coral resilience and to predicting coral responses to stressors like warming oceans that disrupt this critical endosymbiosis. We examined the fidelity with which Symbiodinium communities in the brooding coral Seriatopora hystrix are vertically transmitted and the extent to which communities are genetically regulated, by genotyping the symbiont communities within 60 larvae and their parents (9 maternal and 45 paternal colonies) using high-throughput sequencing of the ITS2 locus. Unexpectedly, Symbiodinium communities associated with brooded larvae were distinct from those within parent colonies, including the presence of types not detected in adults. Bayesian heritability (h2) analysis revealed that 33% of variability in larval Symbiodinium communities was genetically controlled. Results highlight flexibility in the establishment of larval symbiont communities and demonstrate that symbiont transmission is not exclusively vertical in brooding corals. Instead, we show that Symbiodinium transmission in S. hystrix involves a mixed-mode strategy, similar to many terrestrial invertebrate symbioses. Also, variation in the abundances of common Symbiodinium types among adult corals suggests that microhabitat differences influence the structure of in hospite Symbiodinium communities. Partial genetic regulation coupled with flexibility in the environmentally acquired component of Symbiodinium communities implies that corals with vertical transmission, like S. hystrix, may be more resilient to environmental change than previously thought.

Global climate change is threatening the persistence of coral reefs as associated summer heatwaves trigger the loss of microalgal endosymbionts (Symbiodiniaceae) from the coral tissues, or coral bleaching. We infected aposymbiotic juveniles of the coral Acropora tenuis with either wildtype (WT10) or heat-evolved (SS1 or SS8) Symbiodiniaceae strains Cladocopium proliferum (formerly referred to as Cladocopium goreaui and Cladocopium C1acro). After 10 months at 27 °C, SS8-juveniles were 2 × larger than SS1- or WT10-juveniles. In response to a simulated heatwave (31 °C for 41 days), the WT10-juveniles bleached and showed a decline in respiration while cell densities and respiration in both SS-juvenile groups remained unchanged compared to the controls. These results reveal that some heat-evolved strains can increase the bleaching tolerance of juvenile corals without a trade-off against growth. This response is opposite to the lower nutrient provisioning often reported for naturally thermotolerant Symbiodiniaceae (e.g. genus Durusdinium), thereby offering enhanced fitness to the host without the ecological consequences of diminished growth.

Coral reefs worldwide are threatened by increasing ocean temperatures because of the sensitivity of the coral‐algal symbiosis to thermal stress. Reef‐building corals form symbiotic relationships with dinoflagellates (family Symbiodiniaceae), including those species which acquire their initial symbiont complement predominately from their parents. Changes in the composition of symbiont communities, through the mechanisms of symbiont shuffling or switching, can modulate the host's thermal limits. However, the role of shuffling in coral acclimatization to heat is understudied in coral offspring and to date has largely focused on the adults. To quantify potential fitness benefits and consequences of changes in symbiont communities under a simulated heatwave in coral early life‐history stages, we exposed larvae and juveniles of the widespread, vertically transmitting coral, Montipora digitata, to heat stress (32°C) and tracked changes in their growth, survival, photosynthetic efficiency, and symbiont community composition over time relative to controls. We found negative impacts from warming in all fitness‐related traits, which varied significantly among larval families and across life‐history stages. Larvae that survived heat exposure exhibited changes in symbiont communities that favored symbionts that are canonically more stress tolerant. Compared to larvae, juveniles showed more rapid mortality under heat stress and their symbiont communities were largely fixed regardless of temperature treatment, suggesting an inability to alter their symbiont community as an acclimatory response to heat stress. Taken together, these findings suggest that capacity for symbiont shuffling may be modified through ontogeny, and that the juvenile life stage may be less flexible and more at risk from climate warming in this species. We quantified the fitness consequences of changes in symbiont communities under a simulated heatwave in early life‐history stages of Montipora digitata by tracking changes in their growth, survival, photosynthetic efficiency, and symbiont community composition relative to controls. Surviving larvae exposed to heat exhibited changes in symbiont communities that favored types that are canonically more stress tolerant. We found negative impacts with warming in all fitness‐related traits, which varied significantly among larval families and life stages. Surviving larvae exposed to heat exhibited changes in symbiont communities that favored types that are canonically more stress tolerant. Compared to larvae, juveniles showed more rapid mortality under heat stress and their symbiont communities were largely fixed regardless of temperature treatment, suggesting an inability to alter their symbiont community as an acclimatory response to heat stress.

Interactions between corals and their associated microbial communities (Symbiodiniaceae and prokaryotes) are key to understanding corals' potential for and rate of acclimatory and adaptive responses. However, the establishment of microalgal and bacterial communities is poorly understood during coral ontogeny in the wild. We examined the establishment and co‐occurrence between multiple microbial communities using 16S rRNA (bacterial) and ITS2 rDNA (Symbiodiniaceae) gene amplicon sequencing in juveniles of the common coral, Acropora tenuis, across the first year of development. Symbiodiniaceae communities in juveniles were dominated by Durusdinium trenchii and glynnii (D1 and D1a), with lower abundances of Cladocopium (C1, C1d, C50, and Cspc). Bacterial communities were more diverse and dominated by taxa within Proteobacteria, Cyanobacteria, and Planctomycetes. Both communities were characterized by significant changes in relative abundance and diversity of taxa throughout the year. D1, D1a, and C1 were significantly correlated with multiple bacterial taxa, including Alpha‐, Deltra‐, and Gammaproteobacteria, Planctomycetacia, Oxyphotobacteria, Phycisphaerae, and Rhizobiales. Specifically, D1a tended to associate with Oxyphotobacteria and D1 with Alphaproteobacteria, although these associations may represent correlational and not causal relationships. Bioenergetic modeling combined with physiological measurements of coral juveniles (surface area and Symbiodiniaceae cell densities) identified key periods of carbon limitation and nitrogen assimilation, potentially coinciding with shifts in microbial community composition. These results demonstrate that Symbiodiniaceae and bacterial communities are dynamic throughout the first year of ontology and may vary in tandem, with important fitness effects on host juveniles. We characterized the establishment and maintenance of bacterial and Symbiodiniaceae communities in the coral Acropora tenuis across the first year of juvenile ontogeny, identifying potentially key co‐occurrence patterns using network modeling. Bioenergetic modeling combined with physiological measurements of coral juveniles (surface area and Symbiodiniaceae cell densities) identified periods of carbon limitation and nitrogen assimilation, potentially coinciding with shifts in microbial community composition. These dynamic communities vary in tandem with important fitness effects on host juvenile corals.