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Integrated evidence reveals a new species in the ancient blue coral genus Heliopora (Octocorallia).

ABSTRACT: Maintaining the accretion potential and three dimensional structure of coral reefs is a priority but reef-building scleractinian corals are highly threatened and retreating. Hence future reefs are predicted to be dominated by non-constructional taxa. Since the Late Triassic however, other non-scleractinian anthozoans such as Heliopora have contributed to tropical and subtropical reef-building. Heliopora is an ancient and highly conserved reef building octocoral genus within the monospecific Family Helioporidae, represented by a single extant species - H. coerulea, Pallas, 1766. Here we show integrated morphological, genomic and reproductive evidence to substantiate the existence of a second species within the genus Heliopora. Importantly, some individuals of the new species herein described as Heliopora hiberniana sp. nov. feature a white skeleton indicating that the most diagnostic and conserved Heliopora character (the blue skeleton) can be displaced. The new species is currently known only from offshore areas in north Western Australia, which is a part of the world where coral bleaching events have severely impacted the scleractinian community over the last two decades. Field observations indicate individuals of both H. coerulea and H. hiberniana sp. nov. were intact after the 2016 Scott Reef thermal stress event, and we discuss the possibility that bleaching resistant non-scleractinian reef builders such as Heliopora could provide new ecological opportunities for the reconfiguration of future reefs by filling empty niches and functional roles left open by the regression of scleractinian corals.

SUBMITTER: Richards ZT

PROVIDER: S-EPMC6203795 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundHeliopora coerulea, the blue coral, is a reef building octocoral that is reported to have a higher optimum temperature for growth compared to most scleractinian corals. This octocoral has been observed to grow over both live and dead scleractinians and to dominate certain reefs in the Indo-Pacific region. The molecular mechanisms underlying the ability of H. coerulea to tolerate warmer seawater temperatures and to effectively compete for space on the substrate remain to be elucidated.MethodsIn this study, we subjected H. coerulea colonies to various temperatures for up to 3 weeks. The growth and photosynthetic efficiency rates of the coral colonies were measured. We then conducted pairwise comparisons of gene expression among the different coral tissue regions to identify genes and pathways that are expressed under different temperature conditions.ResultsA horizontal growth rate of 1.13 ± 0.25 mm per week was observed for corals subjected to 28 or 31 °C. This growth rate was significantly higher compared to corals exposed at 26 °C. This new growth was characterized by the extension of whitish tissue at the edges of the colony and was enriched for a matrix metallopeptidase, a calcium and integrin binding protein, and other transcripts with unknown function. Tissues at the growth margin and the adjacent calcified encrusting region were enriched for transcripts related to proline and riboflavin metabolism, nitrogen utilization, and organic cation transport. The calcified digitate regions, on the other hand, were enriched for transcripts encoding proteins involved in cell-matrix adhesion, translation, receptor-mediated endocytosis, photosynthesis, and ion transport. Functions related to lipid biosynthesis, extracellular matrix formation, cell migration, and oxidation-reduction processes were enriched at the growth margin in corals subjected for 3 weeks to 28 or 31 °C relative to corals at 26 °C. In the digitate region of the coral, transcripts encoding proteins that protect against oxidative stress, modify cell membrane composition, and mediate intercellular signaling pathways were enriched after just 24 h of exposure to 31 °C compared to corals at 28 °C. The overall downregulation of gene expression observed after 3 weeks of sustained exposure to 31 °C is likely compensated by symbiont metabolism.DiscussionThese findings reveal that the different regions of H. coerulea have variable gene expression profiles and responses to temperature variation. Under warmer conditions, the blue coral invests cellular resources toward extracellular matrix formation and cellular migration at the colony margins, which may promote rapid tissue growth and extension. This mechanism enables the coral to colonize adjacent reef substrates and successfully overgrow slower growing scleractinian corals that may already be more vulnerable to warming ocean waters.

Project description:Most gorgonian octocoral species are described using diagnostic characteristics of their sclerites (microscopic skeletal components). Species in the genus Pterogorgia, however, are separated primarily by differences in their calyx and branch morphology. Specimens of a morphologically unusual Pterogorgia collected from Saba Bank in the NE Caribbean Sea were found with calyx morphology similar to P. citrina and branch morphology similar to P. guadalupensis. In order to test morphological species boundaries, and the validity of calyx and branch morphology as systematic characters, a phylogenetic analysis was undertaken utilizing partial gene fragments of three mitochondrial (mtMutS, cytochrome b, and igr4; 726bp total) and two nuclear (ITS2, 166bp; and SRP54 intron, 143bp) loci. The datasets for nuclear and mitochondrial loci contained few phylogenetically informative sites, and tree topologies did not resolve any of the morphological species as monophyletic groups. Instead, the mitochondrial loci and SRP54 each recovered two clades but were slightly incongruent, with a few individuals of P. guadalupensis represented in both clades with SRP54. A concatenated dataset of these loci grouped all P. anceps and P. guadalupensis in a clade, and P. citrina and the Pterogorgia sp. from Saba Bank in a sister clade, but with minimal variation/resolution within each clade. However, in common with other octocoral taxa, the limited genetic variation may not have been able to resolve whether branch variation represents intraspecific variation or separate species. Therefore, these results suggest that there are at least two phylogenetic lineages of Pterogorgia at the species level, and the atypical Pterogorgia sp. may represent an unusual morphotype of P. citrina, possibly endemic to Saba Bank. Branch morphology does not appear to be a reliable morphological character to differentiate Pterogorgia species (e.g., branches "flat" or "3-4 edges" in P. guadalupensis and P. anceps, respectively), and a re-evaluation of species-level characters (e.g., sclerites) is needed.

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Integrated evidence reveals a new species in the ancient blue coral genus Heliopora (Octocorallia).

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