Reef-building Coral Acropora Millepora Research Articles

Wound healing and regeneration in the reef building coral Acropora millepora

Branching scleractinian corals are niche-constructing organisms, providing continuously-growing, structural foundation for spectacularly biodiverse coral reef ecosystems. A large part of their success lies in the ability to quickly regenerate following mechanical damage. Even now, when the corals undergo great decline due to anthropogenic weather and storm extremes, it is surprising how little is known about molecular mechanisms governing regeneration in these iconic organisms. In this study, we used RNA-seq to identify genes involved in the regeneration of Acropora millepora, starting with the initial wound closure up to complete rebuilding of lost structures. Many of the differentially expressed genes we found in the wound healing steps are homologues of genes known to be involved in wound healing and regeneration of bilaterian and other cnidarian species, prominently including multiple components of FGF and Wnt signalling pathways. Comparison between genes involved in wound healing and continuous growth of the colony demonstrates both similarity and distinctiveness of the genetic programmes controlling these processes. A striking example is specific expression of c-Fos, a transcription factor with conserved role in early injury response, during the earliest stages of wound healing of A. millepora. By comparing results obtained in diverse experimental conditions including a closed-loop, recirculating aquarium and a flow-through system of marine station, we have demonstrated feasibility of using zooxanthellate scleractinian corals as experimental models in fundamental biology research, including studies of regeneration.

Cellular adaptations leading to coral fragment attachment on artificial substrates in Acropora millepora (Am-CAM)

Reproductive propagation by asexual fragmentation in the reef-building coral Acropora millepora depends on (1) successful attachment to the reef substrate through modification of soft tissues and (2) a permanent bond with skeletal encrustation. Despite decades of research examining asexual propagation in corals, the initial response, cellular reorganisation, and development leading to fragment substrate attachment via a newly formed skeleton has not been documented in its entirety. Here, we establish the first "coral attachment model" for this species ("Am-CAM") by developing novel methods that allow correlation of fluorescence and electron microscopy image data with in vivo microscopic time-lapse imagery. This multi-scale imaging approach identified three distinct phases involved in asexual propagation: (1) the contact response of the coral fragment when contact with the substrate, followed by (2) fragment stabilisation through anchoring by the soft tissue, and (3) formation of a "lappet-like appendage" structure leading to substrate bonding of the tissue for encrustation through the onset of skeletal calcification. In developing Am-CAM, we provide new biological insights that can enable reef researchers, managers and coral restoration practitioners to begin evaluating attachment effectiveness, which is needed to optimise species-substrate compatibility and achieve effective outplanting.

Broad scale proteomic analysis of heat-destabilised symbiosis in the hard coral Acropora millepora

Coral reefs across the globe are threatened by warming oceans. The last few years have seen the worst mass coral bleaching events recorded, with more than one quarter of all reefs irreversibly impacted. Considering the widespread devastation, we need to increase our efforts to understanding the physiological and metabolic shifts underlying the breakdown of this important symbiotic ecosystem. Here, we investigated the proteome (PRIDE accession # PXD011668) of both host and symbionts of the reef-building coral Acropora millepora exposed to ambient (~ 28 °C) and elevated temperature (~ 32 °C for 2 days, following a five-day incremental increase) and explored associated biomolecular changes in the symbiont, with the aim of gaining new insights into the mechanisms underpinning the collapse of the coral symbiosis. We identified 1,230 unique proteins (774 host and 456 symbiont) in the control and thermally stressed corals, of which 107 significantly increased and 125 decreased in abundance under elevated temperature relative to the control. Proteins involved in oxidative stress and proteolysis constituted 29% of the host proteins that increased in abundance, with evidence of impairment to endoplasmic reticulum and cytoskeletal regulation proteins. In the symbiont, we detected a decrease in proteins responsible for photosynthesis and energy production (33% of proteins decreased in abundance), yet minimal signs of oxidative stress or proteolysis. Lipid stores increased > twofold despite reduction in photosynthesis, suggesting reduced translocation of carbon to the host. There were significant changes in proteins related to symbiotic state, including proteins linked to nitrogen metabolism in the host and the V-ATPase (-0.6 fold change) known to control symbiosome acidity. These results highlight key differences in host and symbiont proteomic adjustments under elevated temperature and identify two key proteins directly involved in bilateral nutrient exchange as potential indicators of symbiosis breakdown.

Benchmarking DNA methylation assays in a reef-building coral.

Interrogation of chromatin modifications, such as DNA methylation, has the potential to improve forecasting and conservation of marine ecosystems. The standard method for assaying DNA methylation (whole genome bisulphite sequencing), however, is currently too costly to apply at the scales required for ecological research. Here, we evaluate different methods for measuring DNA methylation for ecological epigenetics. We compare whole genome bisulphite sequencing (WGBS) with methylated CpG binding domain sequencing (MBD-seq), and a modified version of MethylRAD we term methylation-dependent restriction site-associated DNA sequencing (mdRAD). We evaluate these three assays in measuring variation in methylation across the genome, between genotypes, and between polyp types in the reef-building coral Acropora millepora. We find that all three assays measure absolute methylation levels similarly for gene bodies (gbM), as well as exons and 1Kb windows with a minimum Pearson correlation 0.66. Differential gbM estimates were less correlated, but still concurrent across assays. We conclude that MBD-seq and mdRAD are reliable and cost-effective alternatives to WGBS. The considerably lower sequencing effort required for mdRAD to produce comparable methylation estimates makes it particularly useful for ecological epigenetics.

Gametogenesis and reproductive pattern of the reef-building coral Acropora millepora in northwestern Philippines

ABSTRACTCoral populations continue to decline in many regions because of natural and anthropogenic disturbances; and the persistence of coral populations mainly relies on natural recruitment through coral reproduction. However, studies on the reproduction of many important reef-building coral species in one of the most biodiverse region, the Coral Triangle, are very limited. Here, we investigated the reproductive biology of the coral Acropora millepora in Bolinao-Anda Reef Complex, northwestern Philippines from February 2014 to March 2015, through in situ assessment of gamete maturity, histological examination of gamete development and ex situ spawning observations. Results showed that A. millepora exhibited an annual gametogenic cycle. Formation of oocytes took place within 8 months, whereas spermatocytes developed in 3 months before the gamete release. Abundance and size of eggs in A. millepora were greatest during the months nearest to the spawning period, which coincides with the rapid increase in sea surface temperature. Ex situ broadcast spawning occurred around the months of February–March, which suggests an extended spawning pattern. Results provide additional information on coral reproduction in the region and reveal the potential of A. millepora in providing coral propagules for the replenishment and recovery of degraded coral populations.

Molecular characterization of larval development from fertilization to metamorphosis in a reef-building coral

BackgroundMolecular mechanisms underlying coral larval competence, the ability of larvae to respond to settlement cues, determine their dispersal potential and are potential targets of natural selection. Here, we profiled competence, fluorescence and genome-wide gene expression in embryos and larvae of the reef-building coral Acropora millepora daily throughout 12 days post-fertilization.ResultsGene expression associated with competence was positively correlated with transcriptomic response to the natural settlement cue, confirming that mature coral larvae are “primed” for settlement. Rise of competence through development was accompanied by up-regulation of sensory and signal transduction genes such as ion channels, genes involved in neuropeptide signaling, and G-protein coupled receptor (GPCRs). A drug screen targeting components of GPCR signaling pathways confirmed a role in larval settlement behavior and metamorphosis.ConclusionsThese results gives insight into the molecular complexity underlying these transitions and reveals receptors and pathways that, if altered by changing environments, could affect dispersal capabilities of reef-building corals. In addition, this dataset provides a toolkit for asking broad questions about sensory capacity in multicellular animals and the evolution of development.

Density-dependent coral recruitment displays divergent responses during distinct early life-history stages.

Population growth involves demographic bottlenecks that regulate recruitment success during various early life-history stages. The success of each early life-history stage can vary in response to population density, interacting with intrinsic (e.g. behavioural) and environmental (e.g. competition, predation) factors. Here, we used the common reef-building coral Acropora millepora to investigate how density-dependence influences larval survival and settlement in laboratory experiments that isolated intrinsic effects, and post-settlement survival in a field experiment that examined interactions with environmental factors. Larval survival was exceptionally high (greater than 80%) and density-independent from 2.5 to 12 days following spawning. By contrast, there was a weak positive effect of larval density on settlement, driven by gregarious behaviour at the highest density. When larval supply was saturated, settlement was three times higher in crevices compared with exposed microhabitats, but a negative relationship between settler density and post-settlement survival in crevices and density-independent survival on exposed surfaces resulted in similar recruit densities just one month following settlement. Moreover, a negative relationship was found between turf algae and settler survival in crevices, whereas gregarious settlement improved settler survival on exposed surfaces. Overall, our findings reveal divergent responses by coral larvae and newly settled recruits to density-dependent regulation, mediated by intrinsic and environmental interactions.

Red fluorescence in coral larvae is associated with a diapause-like state.

Effective dispersal across environmental gradients is the key to species resilience to environmental perturbation, including climate change. Coral reefs are among the most sensitive ecosystems to global warming, but factors predicting coral dispersal potential remain unknown. In a reef-building coral Acropora millepora, larval fluorescence emerged as a possible indicator of dispersal potential since it correlates with responsiveness to a settlement cue. Here, we show that gene expression in red fluorescent larvae of A.millepora is correlated with diapause-like characteristics highly likely to be associated with extended dispersal. We compared gene expression among three larval fluorescent morphs under three coloured light treatments. While colour morphs did not differ in their gene expression responses to light colour, red larvae demonstrated gene expression signatures of cell cycle arrest and decreased transcription accompanied by elevated ribosome production and heightened defenses against oxidative stress. A meta-analysis revealed that this profile was highly similar to the signatures of elevated thermal tolerance in the same coral species, and moreover, functionally resembled diapause states in an insect and a nematode. Our results support a connection between red fluorescence and long-range dispersal, which offers a new perspective on the molecular underpinnings of coral larval dispersal and the biological function of GFP-like fluorescent proteins.

Expression of calcification and metabolism-related genes in response to elevated pCO2 and temperature in the reef-building coral Acropora millepora

Declining health of scleractinian corals in response to deteriorating environmental conditions is widely acknowledged, however links between physiological and functional genomic responses of corals are less well understood. Here we explore growth and the expression of 20 target genes with putative roles in metabolism and calcification in the branching coral, Acropora millepora, in two separate experiments: 1) elevated pCO2 (464, 822, 1187 and 1638μatm) and ambient temperature (27°C), and 2) elevated pCO2 (490 and 822μatm) and temperature (28 and 31°C). After 14days of exposure to elevated pCO2 and ambient temperatures, no evidence of differential expression of either calcification or metabolism genes was detected between control and elevated pCO2 treatments. After 37days of exposure to control and elevated pCO2, Ubiquinol-Cytochrome-C Reductase Subunit 2 gene (QCR2; a gene involved in complex III of the electron chain transport within the mitochondria and critical for generation of ATP) was significantly down-regulated in the elevated pCO2 treatment in both ambient and elevated temperature treatments. Overall, the general absence of a strong response to elevated pCO2 and temperature by the other 19 targeted calcification and metabolism genes suggests that corals may not be affected by these stressors on longer time scales (37days). These results also highlight the potential for QCR2 to act as a biomarker of coral genomic responses to changing environments.

Quantitative high resolution melting: two methods to determine SNP allele frequencies from pooled samples.

BackgroundThe advent of next-generation sequencing has brought about an explosion of single nucleotide polymorphism (SNP) data in non-model organisms; however, profiling these SNPs across multiple natural populations still requires substantial time and resources.ResultsHere, we introduce two cost-efficient quantitative High Resolution Melting (qHRM) methods for measuring allele frequencies at known SNP loci in pooled DNA samples: the “peaks” method, which can be applied to large numbers of SNPs, and the “curves” method, which is more labor intensive but also slightly more accurate. Using the reef-building coral Acropora millepora, we show that both qHRM methods can recover the allele proportions from mixtures prepared using two or more individuals of known genotype. We further demonstrate advantages of each method over previously published methods; specifically, the “peaks” method can be rapidly scaled to screen several hundred SNPs at once, whereas the “curves” method is better suited for smaller numbers of SNPs.ConclusionsCompared to genotyping individual samples, these methods can save considerable effort and genotyping costs when relatively few candidate SNPs must be profiled across a large number of populations. One of the main applications of this method could be validation of SNPs of interest identified in population genomic studies.Electronic supplementary materialThe online version of this article (doi:10.1186/s12863-015-0222-z) contains supplementary material, which is available to authorized users.

Coral animals combat stress with sulphur

Photosynthetic algal symbionts of corals produce sulphur substances that are involved in the regulation of ocean temperatures. In a twist to the tale, it emerges that coral animals produce the same compounds. See Letter p.677 Dimethylsulphoniopropionate (DMSP) is a widely distributed metabolite that is converted by marine bacteria to the volatile gas dimethylsulphide (DMS), a major contributor of sulphur to the atmosphere that contributes to cloud formation and hence influences climate. Here Jean-Baptiste Raina et al. report DMSP formation by two common reef-building coral species, Acropora millepora and Acropora tenuis. This comes as a surprise — previously it was thought that DMSP was produced solely by algae (including species symbiotic in coral) and some plants. DMSP biosynthesis may help the coral animals to survive conditions of thermal stress. This finding could have implications for how DMSP production responds to the effects of global change on corals and their symbionts.

Gene expression signatures of energetic acclimatisation in the reef building coral Acropora millepora.

BackgroundUnderstanding the mechanisms by which natural populations cope with environmental stress is paramount to predict their persistence in the face of escalating anthropogenic impacts. Reef-building corals are increasingly exposed to local and global stressors that alter nutritional status causing reduced fitness and mortality, however, these responses can vary considerably across species and populations.Methodology/Principal FindingsWe compare the expression of 22 coral host genes in individuals from an inshore and an offshore reef location using quantitative Reverse Transcription-PCR (qRT-PCR) over the course of 26 days following translocation into a shaded, filtered seawater environment. Declines in lipid content and PSII activity of the algal endosymbionts (Symbiodinium ITS-1 type C2) over the course of the experiment indicated that heterotrophic uptake and photosynthesis were limited, creating nutritional deprivation conditions. Regulation of coral host genes involved in metabolism, CO2 transport and oxidative stress could be detected already after five days, whereas PSII activity took twice as long to respond. Opposing expression trajectories of Tgl, which releases fatty acids from the triacylglycerol storage, and Dgat1, which catalyses the formation of triglycerides, indicate that the decline in lipid content can be attributed, at least in part, by mobilisation of triacylglycerol stores. Corals from the inshore location had initially higher lipid content and showed consistently elevated expression levels of two genes involved in metabolism (aldehyde dehydrogenase) and calcification (carbonic anhydrase).Conclusions/SignificanceCoral host gene expression adjusts rapidly upon change in nutritional conditions, and therefore can serve as an early signature of imminent coral stress. Consistent gene expression differences between populations indicate that corals acclimatize and/or adapt to local environments. Our results set the stage for analysis of these processes in natural coral populations, to better understand the responses of coral communities to global climate change and to develop more efficient management strategies.

High natural gene expression variation in the reef-building coral Acropora millepora: potential for acclimative and adaptive plasticity.

BackgroundEcosystems worldwide are suffering the consequences of anthropogenic impact. The diverse ecosystem of coral reefs, for example, are globally threatened by increases in sea surface temperatures due to global warming. Studies to date have focused on determining genetic diversity, the sequence variability of genes in a species, as a proxy to estimate and predict the potential adaptive response of coral populations to environmental changes linked to climate changes. However, the examination of natural gene expression variation has received less attention. This variation has been implicated as an important factor in evolutionary processes, upon which natural selection can act.ResultsWe acclimatized coral nubbins from six colonies of the reef-building coral Acropora millepora to a common garden in Heron Island (Great Barrier Reef, GBR) for a period of four weeks to remove any site-specific environmental effects on the physiology of the coral nubbins. By using a cDNA microarray platform, we detected a high level of gene expression variation, with 17% (488) of the unigenes differentially expressed across coral nubbins of the six colonies (jsFDR-corrected, p < 0.01). Among the main categories of biological processes found differentially expressed were transport, translation, response to stimulus, oxidation-reduction processes, and apoptosis. We found that the transcriptional profiles did not correspond to the genotype of the colony characterized using either an intron of the carbonic anhydrase gene or microsatellite loci markers.ConclusionOur results provide evidence of the high inter-colony variation in A. millepora at the transcriptomic level grown under a common garden and without a correspondence with genotypic identity. This finding brings to our attention the importance of taking into account natural variation between reef corals when assessing experimental gene expression differences. The high transcriptional variation detected in this study is interpreted and discussed within the context of adaptive potential and phenotypic plasticity of reef corals. Whether this variation will allow coral reefs to survive to current challenges remains unknown.

Effects of water turbidity on the symbiotic zooxanthella of hermatypic corals

Five species of reef-building coral (Acropora millepora, Acropora nasuta, Pocillopora damicornis, Galaxea fascicularis and Porites lutea) were used to study the effects of water turbidity stress on the symbiotic zooxanthella. The gradients of water turbidity were simulated using a solution containing different concentrations of inactivated Escherichia coli. The results revealed that the photosynthetic efficiency and density of the symbiotic zooxanthella were both restricted by the water turbidity, and that high turbidity corresponds to high inhibitory action. The results also showed that the tolerance of the five symbiotic zooxanthella to water turbidity differed, with the massive corals Galaxea fascicularis and Porites lutea having strong tolerance, and that of the branching corals Acropora millepora, Acropora nasuta and Pocillopora damicornis being relatively weak.

Historical and contemporary factors shape the population genetic structure of the broadcast spawning coral, Acropora millepora, on the Great Barrier Reef

Effective management of reef corals requires knowledge of the extent to which populations are open or closed and the scales over which genetic exchange occurs, information which is commonly derived from population genetic data. Such data are sparse for Great Barrier Reef (GBR) corals and other organisms, with the studies that are available being mostly based on a small number of sampling locations spanning only part of the GBR. Using 11 microsatellite loci, we genotyped 947 colonies of the reef-building coral Acropora millepora from 20 sites spanning almost the full length of the GBR (∼12° of latitude and ∼1550 km). The results show a major divide between the southernmost central to southern offshore populations and all other sampled populations. We interpret this divide as a signature of allopatric divergence in northern and southern refugia during the Pleistocene glaciations, from which the GBR was subsequently recolonized. Superimposed on this pattern is a cross-shelf genetic division, as well as a separation of inshore populations south of the Cape Clifton Front at ∼21.5-22°S. Most inshore populations north of this, as well as mid-shelf populations in the northern and far northern GBR, are open, exchanging recruits frequently. In contrast, inshore populations south of the Cape Clifton Front and offshore populations in the central and southern GBR are largely self-seeding, at least within the spatial resolution that was achieved given our sampling intensity. Populations that have been impacted by recent disturbance events causing extensive coral mortality show no evidence of reduced genetic diversity.

Profiling gene expression responses of coral larvae (Acropora millepora) to elevated temperature and settlement inducers using a novel RNA-Seq procedure

Elevated temperatures resulting from climate change pose a clear threat to reef-building corals; however, the traits that might influence corals' survival and dispersal during climate change remain poorly understood. Global gene expression profiling is a powerful hypothesis-forming tool that can help elucidate these traits. Here, we applied a novel RNA-Seq protocol to study molecular responses to heat and settlement inducers in aposymbiotic larvae of the reef-building coral Acropora millepora. This analysis of a single full-sibling family revealed contrasting responses between short- (4-h) and long-term (5-day) exposures to elevated temperatures. Heat shock proteins were up-regulated only in the short-term treatment, while the long-term treatment induced the down-regulation of ribosomal proteins and up-regulation of genes associated with ion transport and metabolism (Ca(2+) and CO(3)(2-)). We also profiled responses to settlement cues using a natural cue (crustose coralline algae, CCA) and a synthetic neuropeptide (GLW-amide). Both cues resulted in metamorphosis, accompanied by differential expression of genes with known developmental roles. Some genes were regulated only by the natural cue, which may correspond to the recruitment-associated behaviour and morphology changes that precede metamorphosis under CCA treatment, but are bypassed under GLW-amide treatment. Validation of these expression profiles using qPCR confirmed the quantitative accuracy of our RNA-Seq approach. Importantly, qPCR analysis of different larval families revealed extensive variation in these responses depending on genetic background, including qualitative differences (i.e. up-regulation in one family and down-regulation in another). Future studies of gene expression in corals will have to address this genetic variation, which could have important adaptive consequences for corals during global climate change.

Unexpected complexity of the Reef-Building Coral Acropora millepora transcription factor network

BackgroundCoral reefs are disturbed on a global scale by environmental changes including rising sea surface temperatures and ocean acidification. Little is known about how corals respond or adapt to these environmental changes especially at the molecular level. This is mostly because of the paucity of genome-wide studies on corals and the application of systems approaches that incorporate the latter. Like in any other organism, the response of corals to stress is tightly controlled by the coordinated interplay of many transcription factors.ResultsHere, we develop and apply a new system-wide approach in order to infer combinatorial transcription factor networks of the reef-building coral Acropora millepora. By integrating sequencing-derived transcriptome measurements, a network of physically interacting transcription factors, and phylogenetic network footprinting we were able to infer such a network. Analysis of the network across a phylogenetically broad sample of five species, including human, reveals that despite the apparent simplicity of corals, their transcription factors repertoire and interaction networks seem to be largely conserved. In addition, we were able to identify interactions among transcription factors that appear to be species-specific lending strength to the novel concept of "Taxonomically Restricted Interactions".ConclusionsThis study provides the first look at transcription factor networks in corals. We identified a transcription factor repertoire encoded by the coral genome and found consistencies of the domain architectures of transcription factors and conserved regulatory subnetworks across eumetazoan species, providing insight into how regulatory networks have evolved.

Regulation of Apoptotic Mediators Reveals Dynamic Responses to Thermal Stress in the Reef Building Coral Acropora millepora

BackgroundMass coral bleaching is increasing in scale and frequency across the world's coral reefs and is being driven primarily by increased levels of thermal stress arising from global warming. In order to understand the impacts of projected climate change upon corals reefs, it is important to elucidate the underlying cellular mechanisms that operate during coral bleaching and subsequent mortality. In this respect, increased apoptotic cell death activity is an important cellular process that is associated with the breakdown of the mutualistic symbiosis between the cnidarian host and their dinoflagellate symbionts.Methodology/Principal FindingsThe present study reports the impacts of different stressors (colchicine and heat stress) on three phases of apoptosis: (i) the potential initiation by differential expression of Bcl-2 members, (ii) the execution of apoptotic events by activation of caspase 3-like proteases and (iii) and finally, the cell disposal indicated by DNA fragmentation in the reef building coral Acropora millepora. In corals incubated with colchicine, an increase in caspase 3-like activity and DNA fragmentation was associated with a relative down-regulation of Bcl-2, suggesting that the initiation of apoptosis may be mediated by the suppression of an anti-apoptotic mechanism. In contrast, in the early steps of heat stress, the induction of caspase-dependent apoptosis was related to a relative up-regulation of Bcl-2 consecutively followed by a delayed decrease in apoptosis activity.Conclusions/SignificanceIn the light of these results, we propose a model of heat stress in coral hosts whereby increasing temperatures engage activation of caspase 3-dependent apoptosis in cells designated for termination, but also the onset of a delayed protective response involving overexpression of Bcl-2 in surviving cells. This mitigating response to thermal stress could conceivably be an important regulatory mechanism for cell survival in corals exposed to sudden environmental changes.

Potential Costs of Acclimatization to a Warmer Climate: Growth of a Reef Coral with Heat Tolerant vs. Sensitive Symbiont Types

One of the principle ways in which reef building corals are likely to cope with a warmer climate is by changing to more thermally tolerant endosymbiotic algae (zooxanthellae) genotypes. It is highly likely that hosting a more heat-tolerant algal genotype will be accompanied by tradeoffs in the physiology of the coral. To better understand one of these tradeoffs, growth was investigated in the Indo-Pacific reef-building coral Acropora millepora in both the laboratory and the field. In the Keppel Islands in the southern Great Barrier Reef this species naturally harbors nrDNA ITS1 thermally sensitive type C2 or thermally tolerant type D zooxanthellae of the genus Symbiodinium and can change dominant type following bleaching. We show that under controlled conditions, corals with type D symbionts grow 29% slower than those with type C2 symbionts. In the field, type D colonies grew 38% slower than C2 colonies. These results demonstrate the magnitude of trade-offs likely to be experienced by this species as they acclimatize to warmer conditions by changing to more thermally tolerant type D zooxanthellae. Irrespective of symbiont genotype, corals were affected to an even greater degree by the stress of a bleaching event which reduced growth by more than 50% for up to 18 months compared to pre-bleaching rates. The processes of symbiont change and acute thermal stress are likely to act in concert on coral growth as reefs acclimatize to more stressful warmer conditions, further compromising their regeneration capacity following climate change.

Estimating the potential for adaptation of corals to climate warming.

The persistence of tropical coral reefs is threatened by rapidly increasing climate warming, causing a functional breakdown of the obligate symbiosis between corals and their algal photosymbionts (Symbiodinium) through a process known as coral bleaching. Yet the potential of the coral-algal symbiosis to genetically adapt in an evolutionary sense to warming oceans is unknown. Using a quantitative genetics approach, we estimated the proportion of the variance in thermal tolerance traits that has a genetic basis (i.e. heritability) as a proxy for their adaptive potential in the widespread Indo-Pacific reef-building coral Acropora millepora. We chose two physiologically different populations that associate respectively with one thermo-tolerant (Symbiodinium clade D) and one less tolerant symbiont type (Symbiodinium C2). In both symbiont types, pulse amplitude modulated (PAM) fluorometry and high performance liquid chromatography (HPLC) analysis revealed significant heritabilities for traits related to both photosynthesis and photoprotective pigment profile. However, quantitative real-time polymerase chain reaction (qRT-PCR) assays showed a lack of heritability in both coral host populations for their own expression of fundamental stress genes. Coral colony growth, contributed to by both symbiotic partners, displayed heritability. High heritabilities for functional key traits of algal symbionts, along with their short clonal generation time and high population sizes allow for their rapid thermal adaptation. However, the low overall heritability of coral host traits, along with the corals' long generation time, raise concern about the timely adaptation of the coral-algal symbiosis in the face of continued rapid climate warming.