Evolution of bioluminescence in Anthozoa with emphasis on Octocorallia.

Bioluminescence is a widespread phenomenon that has evolved multiple times across the tree of life, converging among diverse fauna and habitat types. The ubiquity of bioluminescence, particularly in marine environments where it is commonly used for communication and defense, highlights the adaptive value of this trait, though the evolutionary origins and timing of emergence remain elusive for a majority of luminous organisms. Anthozoan cnidarians are a diverse group of animals with numerous bioluminescent species found throughout the world's oceans, from shallow waters to the light-limited deep sea where bioluminescence is particularly prominent. This study documents the presence of bioluminescent Anthozoa across depth and explores the diversity and evolutionary origins of bioluminescence among Octocorallia-a major anthozoan group of marine luminous organisms. Using a phylogenomic approach and ancestral state reconstruction, we provide evidence for a single origin of bioluminescence in Octocorallia and infer the age of occurrence to around the Cambrian era, approximately 540 Ma-setting a new record for the earliest timing of emergence of bioluminescence in the marine environment. Our results further suggest this trait was largely maintained in descendants of a deep-water ancestor and bioluminescent capabilities may have facilitated anthozoan diversification in the deep sea.

A new genus of soft coral (Octocorallia, Malacalcyonacea, Cladiellidae) and three new species from Indo-Pacific coral reefs.

Molecular systematic studies of the anthozoan class Octocorallia have revealed widespread incongruence between phylogenetic relationships and taxonomic classification at all levels of the Linnean hierarchy. Among the soft coral taxa in order Malacalcyonacea, the family Alcyoniidae and its type genus Alcyonium have both been recognised to be highly polyphyletic. A recent family-level revision of Octocorallia established a number of new families for genera formerly considered to belong to Alcyoniidae, but revision of Alcyonium is not yet complete. Previous molecular studies have supported the placement of Alcyoniumverseveldti (Benayahu, 1982) in family Cladiellidae rather than Alcyoniidae, phylogenetically distinct from the other three genera in that family. Here we describe a new genus, Ofwegenumgen. nov. to accommodate O.verseveldticomb. nov. and three new species of that genus, O.coronalucissp. nov., O.kloogisp. nov., and O.collisp. nov., bringing the total number of species in this genus to four. Ofwegenumgen. nov. is a rarely encountered genus so far known from only a few locations spanning the Indian and western Pacific Oceans. We present the morphological characters of each species and use molecular data from both DNA barcoding and target-enrichment of conserved elements to explore species boundaries and phylogenetic relationships within the genus.

Expanding our view of the cold-water coral niche and accounting of the ecosystem services of the reef habitat.

Coral reefs are iconic ecosystems that support diverse, productive communities in both shallow and deep waters. However, our incomplete knowledge of cold-water coral (CWC) niche space limits our understanding of their distribution and precludes a complete accounting of the ecosystem services they provide. Here, we present the results of recent surveys of the CWC mound province on the Blake Plateau off the U.S. east coast, an area of intense human activity including fisheries and naval operations, and potentially energy and mineral extraction. At one site, CWC mounds are arranged in lines that total over 150 km in length, making this one of the largest reef complexes discovered in the deep ocean. This site experiences rapid and extreme shifts in temperature between 4.3 and 10.7 °C, and currents approaching 1 m s-1. Carbon is transported to depth by mesopelagic micronekton and nutrient cycling on the reef results in some of the highest nitrate concentrations recorded in the region. Predictive models reveal expanded areas of highly suitable habitat that currently remain unexplored. Multidisciplinary exploration of this new site has expanded understanding of the cold-water coral niche, improved our accounting of the ecosystem services of the reef habitat, and emphasizes the importance of properly managing these systems.

Non-native coral species dominate the fouling community on a semi-submersible platform in the southern Caribbean.

A coral community was examined on a semi-submersible platform that was moored at the leeward side of Curaçao, in the southern Caribbean, from August 2016 until August 2017. This community included several non-native or cryptogenic species. Among them were two scleractinian corals (Tubastraea coccinea and T. tagusensis) and two octocorals (Chromonephthea sp. and an unidentified Nephtheidae sp.). This is the first reported presence of T. tagusensis in the southern Caribbean, and the genus Chromonephthea in the Caribbean region. An ascidian, Perophora cf. regina, is also reported from the southern Caribbean for the first time, as well as a coral-associated vermetid gastropod, Petaloconchus sp., first recorded in the Caribbean in 2014. Lack of biofouling management could potentially harm indigenous marine fauna through the introduction of non-native species. Therefore monitoring communities associated with semi-submersible platforms is essential to track the presence and dispersal of non-native, potentially invasive species.

Bamboozled! Resolving deep evolutionary nodes within the phylogeny of bamboo corals (Octocorallia: Scleralcyonacea: Keratoisididae).

Keratoisididae is a globally distributed, and exclusively deep-sea, family of octocorals that contains species and genera that are polyphyletic. An alphanumeric system, based on a three-gene-region phylogeny, is widely used to describe the biodiversity within this family. That phylogeny identified 12 major groups although it did not have enough signal to explore the relationships among groups. Using increased phylogenomic resolution generated from Ultraconserved Elements and exons (i.e. conserved elements), we aim to resolve deeper nodes within the family and investigate the relationships among those predefined groups. In total, 109 libraries of conserved elements were generated from individuals representing both the genetic and morphological diversity of our keratoisidids. In addition, the conserved element data of 12 individuals from previous studies were included. Our taxon sampling included 11 of the 12 keratoisidid groups. We present two phylogenies, constructed from a 75% (231 loci) and 50% (1729 loci) taxon occupancy matrix respectively, using both Maximum Likelihood and Multiple Species Coalescence methods. These trees were congruent at deep nodes. As expected, S1 keratoisidids were recovered as a well-supported sister clade to the rest of the bamboo corals. S1 corals do not share the same mitochondrial gene arrangement found in other members of Keratoisididae. All other bamboo corals were recovered within two major clades. Clade I comprises individuals assigned to alphanumeric groups B1, C1, D1&D2, F1, H1, I4, and J3 while Clade II contains representatives from A1, I1, and M1. By combining genomics with already published morphological data, we provide evidence that group H1 is not monophyletic, and that the division between other groups - D1 and D2, and A1 and M1 - needs to be reconsidered. Overall, there is a lack of robust morphological markers within Keratoisididae, but subtle characters such as sclerite microstructure and ornamentation seem to be shared within groups and warrant further investigation as taxonomically diagnostic characters.

An enigmatic new octocoral species (Anthozoa, Octocorallia, Malacalcyonacea) from Isla del Coco National Park.

Alienaparvagen. et sp. nov. is described from Cocos Island, Costa Rica. The species was found at various islets and rocky outcrops north and northwest of the island, 20-30 m in depth. The genus is characterised by polyps, retracting into calyces, that form thin encrusting mats extending on dead or live substrates. Sclerites are mostly asymmetrical spindles. Anthocodial rods are arranged in points, not forming a collaret. Colonies and coenenchymal sclerites are red, and polyps are transparent. Using an integrative taxonomic approach, we found the new genus to morphologically and genetically differ from all other described taxa. The molecular phylogenetic analyses provide strong support for the placement of this new genus in the family Pterogorgiidae. Morphologically it is unlike any of the other members of this family, necessitating an amendment to the diagnosis of Pterogorgiidae. Like several other known taxa of octocorals with encrusting growth forms, Alienagen. nov. appears to have evolved from a gorgonian ancestor by loss of an internal skeletal axis. It is the first member of Pterogorgiidae to be reported from the eastern Pacific, contributing further to the knowledge of marine biodiversity in the eastern tropical Pacific and to the octocoral biodiversity of Cocos Island in particular.

Mito-nuclear discordance within Anthozoa, with notes on unique properties of their mitochondrial genomes.

Whole mitochondrial genomes are often used in phylogenetic reconstruction. However, discordant patterns in species relationships between mitochondrial and nuclear phylogenies are commonly observed. Within Anthozoa (Phylum Cnidaria), mitochondrial (mt)-nuclear discordance has not yet been examined using a large and comparable dataset. Here, we used data obtained from target-capture enrichment sequencing to assemble and annotate mt genomes and reconstruct phylogenies for comparisons to phylogenies inferred from hundreds of nuclear loci obtained from the same samples. The datasets comprised 108 hexacorals and 94 octocorals representing all orders and > 50% of extant families. Results indicated rampant discordance between datasets at every taxonomic level. This discordance is not attributable to substitution saturation, but rather likely caused by introgressive hybridization and unique properties of mt genomes, including slow rates of evolution driven by strong purifying selection and substitution rate variation. Strong purifying selection across the mt genomes caution their use in analyses that rely on assumptions of neutrality. Furthermore, unique properties of the mt genomes were noted, including genome rearrangements and the presence of nad5 introns. Specifically, we note the presence of the homing endonuclease in ceriantharians. This large dataset of mitochondrial genomes further demonstrates the utility of off-target reads generated from target-capture data for mt genome assembly and adds to the growing knowledge of anthozoan evolution.

Selection in coral mitogenomes, with insights into adaptations in the deep sea.

Corals are a dominant benthic fauna that occur across a vast range of depths from just below the ocean's surface to the abyssopelagic zone. However, little is known about the evolutionary mechanisms that enable them to inhabit such a wide range of environments. The mitochondrial (mt) genome, which is involved in energetic pathways, may be subject to selection pressures at greater depths to meet the metabolic demands of that environment. Here, we use a phylogenomic framework combined with codon-based models to evaluate whether mt protein-coding genes (PCGs) associated with cellular energy functions are under positive selection across depth in three groups of corals: Octocorallia, Scleractinia, and Antipatharia. The results demonstrated that mt PCGs of deep- and shallow-water species of all three groups were primarily under strong purifying selection (0.0474 < ω < 0.3123), with the exception of positive selection in atp6 (ω = 1.3263) of deep-sea antipatharians. We also found evidence for positive selection at fifteen sites across cox1, mtMutS, and nad1 in deep-sea octocorals and nad3 of deep-sea antipatharians. These results contribute to our limited understanding of mt adaptations as a function of depth and provide insight into the molecular response of corals to the extreme deep-sea environment.

In the aftermath of Hurricane Irma: Colonization of a 4-year-old shipwreck by native and non-native corals, including a new cryptogenic species for the Caribbean.

Little is known about early coral settlement on shipwrecks with regard to their species and size compositions. Hurricanes in the Caribbean have a long history of sinking ships but a link with new coral settlement is understudied. In 2017, Hurricane Irma caused the sinking of over 300 vessels in the coastal waters of Saint Martin, eastern Caribbean. In 2021, coral settlement was studied on one of them, which included two native, one non-native, and two cryptogenic species. The corals were smaller than 8 cm in diameter. The invasive Tubastraea coccinea was the most abundant scleractinian and was predominantly represented by juveniles. A cryptogenic species, Stragulum bicolor, new for the Caribbean, was the most common octocoral. Because they can be harmful to the environment, shipwrecks should be monitored frequently for the occurrence of non-native species, especially when they are only a few years old.

Temperature Controls eDNA Persistence across Physicochemical Conditions in Seawater.

Environmental DNA (eDNA) quantification and sequencing are emerging techniques for assessing biodiversity in marine ecosystems. Environmental DNA can be transported by ocean currents and may remain at detectable concentrations far from its source depending on how long it persist. Thus, predicting the persistence time of eDNA is crucial to defining the spatial context of the information derived from it. To investigate the physicochemical controls of eDNA persistence, we performed degradation experiments at temperature, pH, and oxygen conditions relevant to the open ocean and the deep sea. The eDNA degradation process was best explained by a model with two phases with different decay rate constants. During the initial phase, eDNA degraded rapidly, and the rate was independent of physicochemical factors. During the second phase, eDNA degraded slowly, and the rate was strongly controlled by temperature, weakly controlled by pH, and not controlled by dissolved oxygen concentration. We demonstrate that marine eDNA can persist at quantifiable concentrations for over 2 weeks at low temperatures (≤10 °C) but for a week or less at ≥20 °C. The relationship between temperature and eDNA persistence is independent of the source species. We propose a general temperature-dependent model to predict the maximum persistence time of eDNA detectable through single-species eDNA quantification methods.

On some encrusting Xeniidae (Octocorallia): Re-examination of the type material of Sansibia flava (May, 1898) and a description of new taxa.

The type of the xeniid soft coral Sansibia flava (May, 1898) is re-described for the first time and its morphological diagnosis is presented. A subsequent integrated analysis of molecular and morphological characters of related Xeniidae, including species indigenous to the Indo-Pacific Ocean and invasive in the Atlantic (Brazil), led to the description of a new Sansibia species, as well as two new genera comprising an additional three new species. All of these taxa are encrusting, with polyps arising directly from a spreading basal membrane. Molecular phylogenetic analyses show that these genera are not sister taxa, thus further emphasizing the remarkable phylogenetic diversity of xeniids with such a growth form. The sclerites of all species are uniformly ellipsoid platelets, abundant throughout the colony. The species exhibit restricted, non-overlapping geographic ranges, with distinct genotypes (molecular operational taxonomic units) found in different marine realms. The results emphasize the importance of re-examination of original old type material while applying molecular phylogenetic analyses in order to delineate species boundaries and to recognize biodiversity patterns.

Rhodolitica on rhodoliths: a new stoloniferan genus (Anthozoa, Octocorallia, Alcyonacea).

Rhodolitica occulta gen. nov. et sp. nov. (Clavulariidae) is described from Cocos Island National Park, Pacific Ocean, Costa Rica. The species was found at various islets and rocky outcrops around the island, 20-55 m in depth. The genus is characterised by tubular, single, erect anthosteles interconnected by thin basal ribbon-like stolons on the surfaces of living rhodoliths. The anthosteles are devoid of fused sclerites, which are only present in the stolons. Coenenchymal sclerites are mostly spindles of various shapes, with a characteristic cylindrical warty type in the outer layer, crosses and radiates. Anthocodiae are armed with points, lacking collarets. Colonies and sclerites are red. Using an integrative taxonomic approach, we separate the new genus from similar genera through both morphological comparison and a molecular phylogenetic analysis. This research is a contribution to the knowledge of the octocoral biodiversity in Cocos Island and marine biodiversity in the eastern tropical Pacific.

Revisiting the type of Cespitularia stolonifera/ Gohar, 1938 leads to the description of a new genus and a species of the family Xeniidae (Octocorallia, Alcyonacea).

Because of the problematical identity and status of the type of the xeniid soft coral genus Cespitularia Milne-Edwards Haime, 1850, the species C. stolonifera Gohar, 1938 is revised. Examination of the type colonies has led to the establishment of the new genus Unomia gen. n. which is described and depicted. This genus features a stalk, commonly divided into branches featuring a diffuse polypiferous part consisting of distal clustered polyps and proximal individual ones on the stalk or the basal membranous part of the colonies. The sclerites are ellipsoid platelets composed of dendritic calcite rods whose tips are distinct on the surface of the platelets. Freshly collected material from Venezuelan reefs where the species is invasive was subjected to molecular phylogenetic analysis, the results of which substantiate the taxonomic assignment of the new genus under U. stolonifera comb. n. A new species, U. complanatis, from Japan and Green Island (Taiwan) is described and further illustrates the extent of the interspecific morphological variation within the genus. The results reveal that the biogeographic distribution of Unomia gen. n. includes Pacific Ocean reefs in addition to the previously reported invaded Caribbean reefs.

Phylogenomics, Origin, and Diversification of Anthozoans (Phylum Cnidaria).

Anthozoan cnidarians (corals and sea anemones) include some of the world's most important foundation species, capable of building massive reef complexes that support entire ecosystems. Although previous molecular phylogenetic analyses have revealed widespread homoplasy of the morphological characters traditionally used to define orders and families of anthozoans, analyses using mitochondrial genes or rDNA have failed to resolve many key nodes in the phylogeny. With a fully resolved, time-calibrated phylogeny for 234 species constructed from hundreds of ultraconserved elements and exon loci, we explore the evolutionary origins of the major clades of Anthozoa and some of their salient morphological features. The phylogeny supports reciprocally monophyletic Hexacorallia and Octocorallia, with Ceriantharia as the earliest diverging hexacorals; two reciprocally monophyletic clades of Octocorallia; and monophyly of all hexacoral orders with the exception of the enigmatic sea anemone Relicanthus daphneae. Divergence dating analyses place Anthozoa in the Cryogenian to Tonian periods (648-894 Ma), older than has been suggested by previous studies. Ancestral state reconstructions indicate that the ancestral anthozoan was a solitary polyp that had bilateral symmetry and lacked a skeleton. Colonial growth forms and the ability to precipitate calcium carbonate evolved in the Ediacaran (578 Ma) and Cambrian (503 Ma) respectively; these hallmarks of reef-building species have subsequently arisen multiple times independently in different orders. Anthozoans formed associations with photosymbionts by the Devonian (383 Ma), and photosymbioses have been gained and lost repeatedly in all orders. Together, these results have profound implications for the interpretation of the Precambrian environment and the early evolution of metazoans.[Bilateral symmetry; coloniality; coral; early metazoans; exon capture; Hexacorallia; Octocorallia photosymbiosis; sea anemone; ultraconserved elements.].

A modern scleractinian coral with a two-component calcite-aragonite skeleton.

One of the most conserved traits in the evolution of biomineralizing organisms is the taxon-specific selection of skeletal minerals. All modern scleractinian corals are thought to produce skeletons exclusively of the calcium-carbonate polymorph aragonite. Despite strong fluctuations in ocean chemistry (notably the Mg/Ca ratio), this feature is believed to be conserved throughout the coral fossil record, spanning more than 240 million years. Only one example, the Cretaceous scleractinian coral Coelosmilia (ca. 70 to 65 Ma), is thought to have produced a calcitic skeleton. Here, we report that the modern asymbiotic scleractinian coral Paraconotrochus antarcticus living in the Southern Ocean forms a two-component carbonate skeleton, with an inner structure made of high-Mg calcite and an outer structure composed of aragonite. P. antarcticus and Cretaceous Coelosmilia skeletons share a unique microstructure indicating a close phylogenetic relationship, consistent with the early divergence of P. antarcticus within the Vacatina (i.e., Robusta) clade, estimated to have occurred in the Mesozoic (ca. 116 Mya). Scleractinian corals thus join the group of marine organisms capable of forming bimineralic structures, which requires a highly controlled biomineralization mechanism; this capability dates back at least 100 My. Due to its relatively prolonged isolation, the Southern Ocean stands out as a repository for extant marine organisms with ancient traits.

Overview of the genus Sympodium Ehrenberg, 1834 (Octocorallia, Alcyonacea, Xeniidae), with the description of new species, revealing regional endemism.

The oldest existing type material for any of the xeniid soft corals, Sympodium caeruleum Ehrenberg, 1834, is re-described. An integrated analysis of molecular and morphological characters of Indo-Pacific Xeniidae support the description of seven new species of that genus. The extent of interspecific morphological variation within the genus is extensive; colonies arise from an encrusting membrane of variable thickness that can be either mat-like or may have ribbon-like extensions or irregularly shaped low mounds. The polyps can either arise separately from the membrane or may be arranged into clusters of polyps that bud off at different levels to form small branched groups. The sclerites of all species are uniformly ellipsoid platelets, abundant throughout the colony. The genetic results suggest that Sympodium species demonstrate restricted geographic ranges and regional endemism, with distinct genotypes (molecular operational taxonomic units) each mostly found at a single Indo-Pacific location. The results emphasize the importance of integrating classical taxonomy with a re-examination of original old type material and molecular phylogenetic analyses, in order to delineate species boundaries and to recognize biodiversity patterns.

New approaches to species delimitation and population structure of anthozoans: Two case studies of octocorals using ultraconserved elements and exons.

As coral populations decline worldwide in the face of ongoing environmental change, documenting their distribution, diversity and conservation status is now more imperative than ever. Accurate delimitation and identification of species is a critical first step. This task, however, is not trivial as morphological variation and slowly evolving molecular markers confound species identification. New approaches to species delimitation in corals are needed to overcome these challenges. Here, we test whether target enrichment of ultraconserved elements (UCEs) and exons can be used for delimiting species boundaries and population structure within species of corals by focusing on two octocoral genera, Alcyonium and Sinularia, as exemplary case studies. We designed an updated bait set (29,181 baits) to target-capture 3,023 UCE and exon loci, recovering a mean of 1,910 ± 168 SD per sample with a mean length of 1,055 ± 208 bp. Similar numbers of loci were recovered from Sinularia (1,946 ± 227 SD) and Alcyonium (1,863 ± 177 SD). Species-level phylogenies were highly supported for both genera. Clustering methods based on filtered single nucleotide polymorphisms delimited species and populations that are congruent with previous allozyme, DNA barcoding, reproductive and ecological data for Alcyonium, and offered further evidence of hybridization among species. For Sinularia, results were congruent with those obtained from a previous study using restriction site associated DNA sequencing. Both case studies demonstrate the utility of target-enrichment of UCEs and exons to address a wide range of evolutionary and taxonomic questions across deep to shallow timescales in corals.

Palaeoclimate ocean conditions shaped the evolution of corals and their skeletons through deep time.

Identifying how past environmental conditions shaped the evolution of corals and their skeletal traits provides a framework for predicting their persistence and that of their non-calcifying relatives under impending global warming and ocean acidification. Here we show that ocean geochemistry, particularly aragonite-calcite seas, drives patterns of morphological evolution in anthozoans (corals, sea anemones) by examining skeletal traits in the context of a robust, time-calibrated phylogeny. The lability of skeletal composition among octocorals suggests a greater ability to adapt to changes in ocean chemistry compared with the homogeneity of the aragonitic skeleton of scleractinian corals. Pulses of diversification in anthozoans follow mass extinctions and reef crises, with sea anemones and proteinaceous corals filling empty niches as tropical reef builders went extinct. Changing environmental conditions will likely diminish aragonitic reef-building scleractinians, but the evolutionary history of the Anthozoa suggests other groups will persist and diversify in their wake.

An enhanced target-enrichment bait set for Hexacorallia provides phylogenomic resolution of the staghorn corals (Acroporidae) and close relatives.

Targeted enrichment of genomic DNA can profoundly increase the phylogenetic resolution of clades and inform taxonomy. Here, we redesign a custom bait set previously developed for the cnidarian class Anthozoa to more efficiently target and capture ultraconserved elements (UCEs) and exonic loci within the subclass Hexacorallia. We test this enhanced bait set (targeting 2476 loci) on 99 specimens of scleractinian corals spanning both the "complex" (Acroporidae, Agariciidae) and "robust" (Fungiidae) clades. Focused sampling in the staghorn corals (genus Acropora) highlights the ability of sequence capture to inform the taxonomy of a clade previously deficient in molecular resolution. A mean of 1850 (±298) loci were captured per taxon (955 UCEs, 894 exons), and a 75% complete concatenated alignment of 96 samples included 1792 loci (991 UCE, 801 exons) and ~1.87 million base pairs. Maximum likelihood and Bayesian analyses recovered robust molecular relationships and revealed that species-level relationships within the Acropora are incongruent with traditional morphological groupings. Both UCE and exon datasets delineated six well-supported clades within Acropora. The enhanced bait set will facilitate investigations of the evolutionary history of many important groups of reef corals, particularly where previous molecular marker development has been unsuccessful.