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The future survival of coral reefs in the Anthropocene depends on the capacity of corals to adapt as oceans warm and extreme weather events become more frequent. Targeted interventions designed to assist evolutionary processes in corals require a comprehensive understanding of the distribution and structure of standing variation, however, efforts to map genomic variation in corals have so far focussed almost exclusively on SNPs, overlooking structural variants that have been shown to drive adaptive processes in other taxa. Here, we show that the reef-building coral, Acropora kenti, harbours at least five large, highly polymorphic structural variants, all of which exhibit signatures of strongly suppressed recombination in heterokaryotypes, a feature commonly associated with chromosomal inversions. Based on their high minor allele frequency, uniform distribution across habitats and elevated genetic load, we propose that these inversions in A. kenti are likely to be under balancing selection. An excess of SNPs with high impact on protein-coding genes within these loci elevates their importance both as potential targets for adaptive selection and as contributors to genetic decline if coral populations become fragmented or inbred in future., (© 2024 The Author(s). Molecular Ecology published by John Wiley & Sons Ltd.)

Marine invertebrates harbour a complex suite of bacterial and archaeal symbionts, a subset of which are probably linked to host health and homeostasis. Within a complex microbiome it can be difficult to tease apart beneficial or parasitic symbionts from nonessential commensal or transient microorganisms; however, one approach is to detect strong cophylogenetic patterns between microbial lineages and their respective hosts. We employed the Procrustean approach to cophylogeny (PACo) on 16S rRNA gene derived microbial community profiles paired with COI, 18S rRNA and ITS1 host phylogenies. Second, we undertook a network analysis to identify groups of microbes that were co-occurring within our host species. Across 12 coral, 10 octocoral and five sponge species, each host group and their core microbiota (50% prevalence within host species replicates) had a significant fit to the cophylogenetic model. Independent assessment of each microbial genus and family found that bacteria and archaea affiliated to Endozoicomonadaceae, Spirochaetaceae and Nitrosopumilaceae have the strongest cophylogenetic signals. Further, local Moran's I measure of spatial autocorrelation identified 14 ASVs, including Endozoicomonadaceae and Spirochaetaceae, whose distributions were significantly clustered by host phylogeny. Four co-occurring subnetworks were identified, each of which was dominant in a different host group. Endozoicomonadaceae and Spirochaetaceae ASVs were abundant among the subnetworks, particularly one subnetwork that was exclusively comprised of these two bacterial families and dominated the octocoral microbiota. Our results disentangle key microbial interactions that occur within complex microbiomes and reveal long-standing, essential microbial symbioses in coral reef invertebrates., (© 2021 John Wiley & Sons Ltd.)

Despite the ecological significance of the mutualistic relationship between Symbiodiniaceae and reef-building corals, the molecular interactions during establishment of this relationship are not well understood. This is particularly true of the transcriptional changes that occur in the symbiont. In the current study, a dual RNA-sequencing approach was used to better understand transcriptional changes on both sides of the coral-symbiont interaction during the colonization of Acropora tenuis by a compatible Symbiodiniaceae strain (Cladocopium goreaui; ITS2 type C1). Comparison of transcript levels of the in hospite symbiont 3, 12, 48 and 72 hr after exposure to those of the same strain in culture revealed that extensive and generalized down-regulation of symbiont gene expression occurred during the infection process. Included in this "symbiosis-derived transcriptional repression" were a range of stress response and immune-related genes. In contrast, a suite of symbiont genes implicated in metabolism was upregulated in the symbiotic state. The coral data support the hypothesis that immune-suppression and arrest of phagosome maturation play important roles during the establishment of compatible symbioses, and additionally imply the involvement of some SCRiP family members in the colonization process. Consistent with previous ecological studies, the transcriptomic data suggest that active translocation of metabolites to the host may begin early in the colonization process, and thus that the mutualistic relationship can be established at the larval stage. This dual RNA-sequencing study provides insights into the transcriptomic remodelling that occurs in C. goreaui during transition to a symbiotic lifestyle and the novel coral genes implicated in symbiosis., (© 2020 John Wiley & Sons Ltd.)

Despite the ecological significance of the relationship between reef-building corals and intracellular photosynthetic dinoflagellates of the genus Symbiodinium, very little is known about the molecular mechanisms involved in its establishment. Indeed, microarray-based analyses point to the conclusion that host gene expression is largely or completely unresponsive during the establishment of symbiosis with a competent strain of Symbiodinium. In this study, the use of Illumina RNA-Seq technology allowed detection of a transient period of differential expression involving a small number of genes (1073 transcripts; <3% of the transcriptome) 4 h after the exposure of Acropora digitifera planulae to a competent strain of Symbiodinium (a clade B strain). This phenomenon has not previously been detected as a consequence of both the lower sensitivity of the microarray approaches used and the sampling times used. The results indicate that complex changes occur, including transient suppression of mitochondrial metabolism and protein synthesis, but are also consistent with the hypothesis that the symbiosome is a phagosome that has undergone early arrest, raising the possibility of common mechanisms in the symbiotic interactions of corals and symbiotic sea anemones with their endosymbionts., (© 2016 John Wiley & Sons Ltd.)

The evolutionary success of reef-building corals is often attributed to their symbiotic relationship with photosynthetic dinoflagellates of the genus Symbiodinium, but metabolic interactions between the partners and the molecular bases of light-enhanced calcification (LEC) are not well understood. Here, the metabolic bases of the interaction between the coral Acropora millepora and its dinoflagellate symbiont were investigated by comparing gene expression levels under light and dark conditions at the whole transcriptome level. Among the 497 differentially expressed genes identified, a suite of genes involved in cholesterol transport was found to be upregulated under light conditions, confirming the significance of this compound in the coral symbiosis. Although ion transporters likely to have roles in calcification were not differentially expressed in this study, expression levels of many genes associated with skeletal organic matrix composition and organization were higher in light conditions. This implies that the rate of organic matrix synthesis is one factor limiting calcification at night. Thus, LEC during the day is likely to be a consequence of increases in both matrix synthesis and the supply of precursor molecules as a result of photosynthetic activity., (© 2015 John Wiley & Sons Ltd.)

Corals play a key role in ocean ecosystems and carbonate balance, but their molecular response to ocean acidification remains unclear. The only previous whole-transcriptome study (Moya et al. Molecular Ecology, 2012; 21, 2440) documented extensive disruption of gene expression, particularly of genes encoding skeletal organic matrix proteins, in juvenile corals (Acropora millepora) after short-term (3 d) exposure to elevated pCO2 . In this study, whole-transcriptome analysis was used to compare the effects of such 'acute' (3 d) exposure to elevated pCO2 with a longer ('prolonged'; 9 d) period of exposure beginning immediately post-fertilization. Far fewer genes were differentially expressed under the 9-d treatment, and although the transcriptome data implied wholesale disruption of metabolism and calcification genes in the acute treatment experiment, expression of most genes was at control levels after prolonged treatment. There was little overlap between the genes responding to the acute and prolonged treatments, but heat shock proteins (HSPs) and heat shock factors (HSFs) were over-represented amongst the genes responding to both treatments. Amongst these was an HSP70 gene previously shown to be involved in acclimation to thermal stress in a field population of another acroporid coral. The most obvious feature of the molecular response in the 9-d treatment experiment was the upregulation of five distinct Bcl-2 family members, the majority predicted to be anti-apoptotic. This suggests that an important component of the longer term response to elevated CO2 is suppression of apoptosis. It therefore appears that juvenile A. millepora have the capacity to rapidly acclimate to elevated pCO2 , a process mediated by upregulation of specific HSPs and a suite of Bcl-2 family members., (© 2014 John Wiley & Sons Ltd.)

The impact of ocean acidification (OA) on coral calcification, a subject of intense current interest, is poorly understood in part because of the presence of symbionts in adult corals. Early life history stages of Acropora spp. provide an opportunity to study the effects of elevated CO(2) on coral calcification without the complication of symbiont metabolism. Therefore, we used the Illumina RNAseq approach to study the effects of acute exposure to elevated CO(2) on gene expression in primary polyps of Acropora millepora, using as reference a novel comprehensive transcriptome assembly developed for this study. Gene ontology analysis of this whole transcriptome data set indicated that CO(2) -driven acidification strongly suppressed metabolism but enhanced extracellular organic matrix synthesis, whereas targeted analyses revealed complex effects on genes implicated in calcification. Unexpectedly, expression of most ion transport proteins was unaffected, while many membrane-associated or secreted carbonic anhydrases were expressed at lower levels. The most dramatic effect of CO(2) -driven acidification, however, was on genes encoding candidate and known components of the skeletal organic matrix that controls CaCO(3) deposition. The skeletal organic matrix effects included elevated expression of adult-type galaxins and some secreted acidic proteins, but down-regulation of other galaxins, secreted acidic proteins, SCRiPs and other coral-specific genes, suggesting specialized roles for the members of these protein families and complex impacts of OA on mineral deposition. This study is the first exhaustive exploration of the transcriptomic response of a scleractinian coral to acidification and provides an unbiased perspective on its effects during the early stages of calcification., (© 2012 Blackwell Publishing Ltd.)

We investigated variation in transcript abundance in the scleractinian coral, Acropora millepora, within and between populations characteristically exposed to different turbidity regimes and hence different levels of light and suspended particulate matter. We examined phenotypic plasticity by comparing levels of gene expression between source populations and following 10 days of acclimatization to a laboratory environment. Analyses of variance revealed that 0.05% of genes were differentially expressed between source populations, 1.32% following translocation into a common laboratory and 0.07% in the interaction (source population-dependent responses to translocation). Functional analyses identified an over-representation of differentially expressed genes associated with metabolism and fluorescence categories (primarily downregulated), and environmental information processing (primarily upregulated) following translocation to a lower light and turbidity environment. Such metabolic downregulation may indicate nonoxidative stress, hibernation or caloric restriction associated with the changed environmental conditions. Green fluorescent protein-related genes were the most differentially expressed and were exclusively downregulated; however, green fluorescent protein levels remained unchanged following translocation. Photophysiological responses of corals from both locations were characterized by a decline when introduced to the common laboratory environment but remained healthy (F(v)/F(m) > 0.6). Declines in total lipid content following translocation were the greatest for inshore corals, suggesting that turbid water corals have a strong reliance on heterotrophic feeding.

Symbiotic relationships have contributed greatly to the evolution and maintenance of biological diversity. On the Great Barrier Reef, species of obligate coral-dwelling fishes (genus Gobiodon) coexist by selectively recruiting to colonies of Acropora nasuta that differ in branch-tip colour. In this study, we investigate genetic variability among sympatric populations of two colour morphs of A. nasuta ('blue-tip' and 'brown-tip') living in symbiosis with two fish species, Gobiodon histrio and G. quinquestrigatus, respectively, to determine whether gobies are selecting between intraspecific colour polymorphisms or cryptic coral species. We also examine genetic differentiation among coral populations containing both these colour morphs that are separated by metres between local sites, tens of kilometres across the continental shelf and hundreds of kilometres along the Great Barrier Reef. We use three nuclear DNA loci, two of which we present here for the first time for Acropora. No significant genetic differentiation was detected between sympatric colour morphs at these three loci. Hence, symbiotic gobies are selecting among colour morphs of A. nasuta, rather than cryptic species. Significant genetic geographical structuring was observed among populations, independent of colour, at regional (i.e. latitudinal separation by < 500 km) and cross-shelf (< 50 km) scales, alongside relative homogeneity between local populations on within reef scales (< 5 km). This contrasts with the reported absence of large-scale genetic structuring in A. valida, which is a member of the same species group as A. nasuta. Apparent differences in biogeographical structuring between species within the A. nasuta group emphasize the need for comparative sampling across both spatial (i.e. within reefs, between reefs and between regions) and taxonomic scales (i.e. within and between closely related species).

Hybridisation between coral species clearly occurs in vitro, but the evolutionary significance of this cross-fertility is still the subject of much debate. Compelling genetic and reproductive evidence support introgressive hybridization amongst Indo-Pacific members of the scleractinian genus Acropora. Although population genetic analyses indicate that interspecific hybridization events are relatively rare, they are likely be important on evolutionary time scales, creating the capacity for adaptive evolution by increasing genomic diversity and heterozygosity. However, in a recent paper based exclusively on the three endemic Caribbean Acropora species, Vollmer and Palumbi (2002) dispute the occurrence of reticulation in corals. Here we use data from both the Vollmer and Palumbi study and our earlier paper on the same species (van Oppen et al., 2000) to show that reticulation has occurred amongst the Caribbean Acropora species. Furthermore, conclusions based on the limited Caribbean Acropora fauna cannot simply be extrapolated to Indo-Pacific corals, and it is inappropriate to view some coral species as 'immortal mules'.

Species boundaries among five sympatric coral species of the Indo-Pacific Acropora aspera group were examined by a combination of in vitro breeding trials, comparisons of spawning times and DNA sequence analysis of ribosomal DNA internal transcribed spacer (rDNA ITS) and 5.8S regions. The breeding trials showed that reproductive compatibility exists between at least some colonies of all the species pairs tested, suggesting a large potential for natural hybridization and introgression. The Acropora ITS regions exhibited extremely high levels of variability (up to approximately 62% for ITS1, approximately 11% for 5.8S and approximately 43% for ITS2), but most of the variation was shared among four of the five species, A. millepora, A. papillare, A. pulchra and A. spathulata, consistent with extensive introgression. Phylogenetic analyses did not resolve these four species as distinct clusters across a wide biogeographic region stretching from the southern Great Barrier Reef to Papua New Guinea. However, most colonies of the fifth species, A. aspera, constituted a distinct clade in phylogenetic analyses. This is consistent with our observations of a semi-permeable temporal barrier involving differences in spawning times between this and the other four species. Although the majority of colonies of all five species generally spawned within 90 min of each other, in two out of four years, gametes were absent prior to mass spawning episodes from at least some A. aspera colonies. Hence, our data suggest that transient reproductive barriers may be the result of year-to-year variation in the date of spawning and that this difference in spawning time contributes to the genetic structure detected among Acropora species in this group. Occasional leakage through the reproductive barrier was confirmed by the observation of A. aspera xA. pulchra F1 hybrids, identified based on additivity of ITS sequences.

A major challenge for understanding the evolutionary genetics of mass-spawning corals is to explain the maintenance of discrete morphospecies in view of high rates of interspecific fertilization in vitro and nonmonophyletic patterns in molecular phylogenies. In this study, we focused on Acropora cytherea and A. hyacinthus, which have one of the highest potentials for interspecific fertilization. Using sequences of a nuclear intron, we performed phylogenetic and nested clade analyses (NCA). Both species were polyphyletic in molecular phylogenies, but the NCA indicated that they constitute statistically distinguishable lineages. Phylogenetic analysis using an intergenic region of the mitochondrial DNA (mtDNA), was inconclusive because of low levels of variability in this marker. The position of these two species differed between the nuclear DNA (nDNA) and mtDNA phylogenies and was also at odds with a cladistic analysis based on morphology. We conclude that despite the potential for high levels of hybridization and introgression, A. cytherea and A. hyacinthus constitute statistically distinguishable lineages and their taxonomic status is consistent with the cohesion species concept.

Although Acropora is the most species-rich genus of the scleractinian (stony) corals, only three species occur in the Caribbean: A. cervicornis, A. palmata and A. prolifera. Based on overall coral morphology, abundance and distribution patterns, it has been suggested that A. prolifera may be a hybrid between A. cervicornis and A. palmata. The species boundaries among these three morphospecies were examined using DNA sequence analyses of the nuclear Pax-C 46/47 intron and the ribosomal DNA Internal Transcribed Spacer (ITS1 and ITS2) and 5.8S regions. Moderate levels of sequence variability were observed in the ITS and 5.8S sequences (up to 5.2% overall sequence difference), but variability within species was as large as between species and all three species carried similar sequences. Since this is unlikely to represent a shared ancestral polymorphism, the data suggest that introgressive hybridization occurs among the three species. For the Pax-C intron, A. cervicornis and A. palmata had very distinct allele frequencies and A. cervicornis carried a unique allele at a frequency of 0.769 (although sequence differences between alleles were small). All A. prolifera colonies examined were heterozygous for the Pax-C intron, whereas heterozygosity was only 0.286 and 0.333 for A. cervicornis and A. palmata, respectively. These data support the hypothesis that A. prolifera is the product of hybridization between two species that have a different allelic composition for the Pax-C intron, i.e. A. cervicornis and A. palmata. We therefore suggest that A. prolifera is a hybrid between A. cervicornis and A. palmata, which backcrosses with the parental species at low frequency.