Ameripathidae, a new family of antipatharian corals (Cnidaria, Anthozoa, Hexacorallia, Antipatharia).

A new family of antipatharian corals, Ameripathidae (Cnidaria: Anthozoa: Antipatharia), is established for Ameripathespseudomyriophylla Opresko & Horowitz, gen. et sp. nov. The new family resembles Myriopathidae and Stylopathidae in terms of the morphology of the polyps and tentacles and the pinnulate branching of the corallum. Phylogenetic analysis using a genomic data set of 741 conserved element loci indicates that the new family is sister to a clade containing the Myriopathidae, Stylopathidae, Antipathidae, and Aphanipathidae.

Sea anemone (Anthozoa, Actiniaria) diversity in Mo'orea (French Polynesia).

Sea anemones (Order Actiniaria) are a diverse group of marine invertebrates ubiquitous across marine ecosystems. Despite their wide distribution and success, a knowledge gap persists in our understanding of their diversity within tropical systems, owed to sampling bias of larger and more charismatic species overshadowing cryptic lineages. This study aims to delineate the sea anemone diversity in Mo'orea (French Polynesia) with the use of a dataset from the Mo'orea Biocode's "BioBlitz" initiative, which prioritized the sampling of more cryptic and understudied taxa. Implementing a target enrichment approach, we integrate 71 newly sequenced samples into an expansive phylogenetic framework and contextualize Mo'orea's diversity within global distribution patterns of sea anemones. Our analysis corroborates the presence of several previously documented sea anemones in French Polynesia and identifies for the first time the occurrence of members of genera Andvakia and Aiptasiomorpha. This research unveils the diverse sea anemone ecosystem in Mo'orea, spotlighting the area's ecological significance and emphasizing the need for continued exploration. Our methodology, encompassing a broad BLAST search coupled with phylogenetic analysis, proved to be a practical and effective approach for overcoming the limitations posed by the lack of comprehensive sequence data for sea anemones. We discuss the merits and limitations of current molecular methodologies and stress the importance of further research into lesser-studied marine organisms like sea anemones. Our work sets a precedent for future phylogenetic studies stemming from BioBlitz endeavors.

Skimming genomes for systematics and DNA barcodes of corals.

Numerous genomic methods developed over the past two decades have enabled the discovery and extraction of orthologous loci to help resolve phylogenetic relationships across various taxa and scales. Genome skimming (or low-coverage genome sequencing) is a promising method to not only extract high-copy loci but also 100s to 1000s of phylogenetically informative nuclear loci (e.g., ultraconserved elements [UCEs] and exons) from contemporary and museum samples. The subphylum Anthozoa, including important ecosystem engineers (e.g., stony corals, black corals, anemones, and octocorals) in the marine environment, is in critical need of phylogenetic resolution and thus might benefit from a genome-skimming approach. We conducted genome skimming on 242 anthozoan corals collected from 1886 to 2022. Using existing target-capture baitsets, we bioinformatically obtained UCEs and exons from the genome-skimming data and incorporated them with data from previously published target-capture studies. The mean number of UCE and exon loci extracted from the genome skimming data was 1837 ± 662 SD for octocorals and 1379 ± 476 SD loci for hexacorals. Phylogenetic relationships were well resolved within each class. A mean of 1422 ± 720 loci was obtained from the historical specimens, with 1253 loci recovered from the oldest specimen collected in 1886. We also obtained partial to whole mitogenomes and nuclear rRNA genes from >95% of samples. Bioinformatically pulling UCEs, exons, mitochondrial genomes, and nuclear rRNA genes from genome skimming data is a viable and low-cost option for phylogenetic studies. This approach can be used to review and support taxonomic revisions and reconstruct evolutionary histories, including historical museum and type specimens.

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.

How long have we been mistaken? Multi-tools shedding light into the systematics of the widespread deep-water genus Madrepora Linnaeus, 1758 (Scleractinia).

Deep-water coral reefs are found worldwide and harbor biodiversity levels that are comparable to their shallow-water counterparts. However, the genetic diversity and population structure of deep-water species remain poorly explored, and historical taxonomical issues still need to be resolved. Here we used microsatellite markers as well as ultraconserved elements (UCE) and exons to shed light on the population structure, genetic diversity, and phylogenetic position of the genus Madrepora, which contains M. oculata, one of the most widespread scleractinian species. Population structure of 107 samples from three Southwestern Atlantic sedimentary basins revealed the occurrence of a cryptic species, herein named M. piresae sp. nov. (authored by Kitahara, Capel and Zilberberg), which can be found in sympatry with M. oculata. Phylogeny reconstructions based on 134 UCEs and exon regions corroborated the population genetic data, with the recovery of two well-supported groups, and reinforced the polyphyly of the family Oculinidae. In order to better accommodate the genus Madrepora, while reducing taxonomical confusion associated with the name Madreporidae, we propose the monogeneric family Bathyporidae fam. nov. (authored by Kitahara, Capel, Zilberberg and Cairns). Our findings advance the knowledge on the widespread deep-water genus Madrepora, resolve a long-standing question regarding the phylogenetic position of the genus, and highlight the need of a worldwide review of 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.

Bathymetric evolution of black corals through deep time.

Deep-sea lineages are generally thought to arise from shallow-water ancestors, but this hypothesis is based on a relatively small number of taxonomic groups. Anthozoans, which include corals and sea anemones, are significant contributors to the faunal diversity of the deep sea, but the timing and mechanisms of their invasion into this biome remain elusive. Here, we reconstruct a fully resolved, time-calibrated phylogeny of 83 species in the order Antipatharia (black coral) to investigate their bathymetric evolutionary history. Our reconstruction indicates that extant black coral lineages first diversified in continental slope depths (∼250-3000 m) during the early Silurian (∼437 millions of years ago (Ma)) and subsequently radiated into, and diversified within, both continental shelf (less than 250 m) and abyssal (greater than 3000 m) habitats. Ancestral state reconstruction analysis suggests that the appearance of morphological features that enhanced the ability of black corals to acquire nutrients coincided with their invasion of novel depths. Our findings have important conservation implications for anthozoan lineages, as the loss of 'source' slope lineages could threaten millions of years of evolutionary history and confound future invasion events, thereby warranting protection.

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.

Description of a new species of black coral in the family Aphanipathidae (Anthozoa, Antipatharia) from Puerto Rico.

Black corals (Anthozoa: Antipatharia) are an anthozoan lineage in the class Hexacorallia that occur across a wide range of habitats from the tropics to the poles and from surface waters to depths deeper than 8000 m. A new species of black coral, Aphanipathespuertoricoensissp. nov., collected with a remotely operated vehicle 357 m deep off Puerto Rico is recognized in the family Aphanipathidae. The new species is characterized by very long and loosely coiled primary branches and up to 0.5 mm tall spines with as many as 40 or more small conical tubercles. A phylogeny composed of 13 taxa that are closely related to the new species was reconstructed from 793 nuclear loci to show their systematic relationships. Our study integrated morphological and genomic data to show that this new species is distinct from other species in the genus Aphanipathes. Furthermore, our results add to the growing knowledge of black coral diversity, while further demonstrating the need for exploration in deep waters of the Caribbean Sea.

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.

Target-capture probes for phylogenomics of the Caenogastropoda.

Target-capture approaches have facilitated a rapid growth in the field of phylogenomics but few probe sets exist for molluscs, an exceptionally rich phylum with unparalleled ecological and morphological diversity. We designed and tested the first universal probe set using Phyluce to capture ultraconserved elements (UCEs) and exon loci from the Subclass Caenogastropoda - one of six major lineages of gastropods. The probe set consists of 29,441 probes designed to target 1142 UCE loci and 1933 exon loci (3075 total). In silico analyses of our probe set yielded an average of 2110 loci from genomes and 1389 loci from transcriptomes of diverse caenogastropods, from which an average of 1669 and 849 loci were retained respectively after screening to remove those that matched multiple contigs. Phylogenetic analyses of the loci extracted from transcriptomes produced well-supported trees very similar to those published based on transcriptomic analyses. Phylogenetic relationships estimated from loci extracted from genomes recover similar phylogenetic relationships, and indicate that the loci targeted with this probe set are informative for resolving deep phylogenetic relationships. An in vitro analysis of the probe set with the Epitoniidae, a diverse caenogastropod family of uncertain affinity and with poorly resolved evolutionary relationships, recovered a total of 2850 loci. Although preliminary, the analysis of loci captured by our probe set for a small number of epitoniid taxa produced a well-resolved tree indicating that this probe set is also able to resolve relationships at shallower hierarchical scales. Together, the in silico and in vitro analyses indicate that target-capture enrichment with this probe set is a useful tool for reconstructing phylogenetic relationships across taxonomic levels and evolutionary time scales.

Genetic diversity and connectivity of chemosynthetic cold seep mussels from the U.S. Atlantic margin.

BACKGROUND: Deep-sea mussels in the subfamily Bathymodiolinae have unique adaptations to colonize hydrothermal-vent and cold-seep environments throughout the world ocean. These invertebrates function as important ecosystem engineers, creating heterogeneous habitat and promoting biodiversity in the deep sea. Despite their ecological significance, efforts to assess the diversity and connectivity of this group are extremely limited. Here, we present the first genomic-scale diversity assessments of the recently discovered bathymodioline cold-seep communities along the U.S. Atlantic margin, dominated by Gigantidas childressi and Bathymodiolus heckerae. RESULTS: A Restriction-site Associated DNA Sequencing (RADSeq) approach was used on 177 bathymodiolines to examine genetic diversity and population structure within and between seep sites. Assessments of genetic differentiation using single-nucleotide polymorphism (SNP) data revealed high gene flow among sites, with the shallower and more northern sites serving as source populations for deeper occurring G. childressi. No evidence was found for genetic diversification across depth in G. childressi, likely due to their high dispersal capabilities. Kinship analyses indicated a high degree of relatedness among individuals, and at least 10-20% of local recruits within a particular site. We also discovered candidate adaptive loci in G. childressi and B. heckerae that suggest differences in developmental processes and depth-related and metabolic adaptations to chemosynthetic environments. CONCLUSIONS: These results highlight putative source communities for an important ecosystem engineer in the deep sea that may be considered in future conservation efforts. Our results also provide clues into species-specific adaptations that enable survival and potential speciation within chemosynthetic ecosystems.

Solving the Coral Species Delimitation Conundrum.

Distinguishing coral species is not only crucial for physiological, ecological, and evolutionary studies but also to enable effective management of threatened reef ecosystems. However, traditional hypotheses that delineate coral species based on morphological traits from the coral skeleton are frequently at odds with tree-based molecular approaches. Additionally, a dearth of species-level molecular markers has made species delimitation particularly challenging in species-rich coral genera, leading to the widespread assumption that interspecific hybridization might be responsible for this apparent conundrum. Here, we used three lines of evidence-morphology, breeding trials, and molecular approaches-to identify species boundaries in a group of ecologically important tabular Acropora corals. In contrast to previous studies, our morphological analysis yielded groups that were congruent with experimental crosses as well as with coalescent-based and allele sharing-based multilocus approaches to species delimitation. Our results suggest that species of the genus Acropora are reproductively isolated and independently evolving units that can be distinguished morphologically. These findings not only pave the way for a taxonomic revision of coral species but also outline an approach that can provide a solid basis to address species delimitation and provide conservation support to a wide variety of keystone organisms. [Acropora; coral reefs; hybridization; reproductive isolation; taxonomy.].

Moving conferences online: lessons learned from an international virtual meeting.

We consider the opportunities and challenges associated with organizing a conference online, using a case study of a medium-sized (approx. 400 participants) international conference held virtually in August 2020. In addition, we present quantifiable evidence of the participants' experience using the results from an online post-conference questionnaire. Although the virtual meeting was not able to replicate the in-person experience in some aspects (e.g. less engagement between participants) the overwhelming majority of respondents found the meeting an enjoyable experience and would join similar events again. Notably, there was a strong desire for future in-person meetings to have at least some online component. Online attendance by lower-income researchers was higher compared with a past, similar-themed in-person meeting held in a high-income nation, but comparable to one held in an upper-middle-income nation. This indicates that online conferences are not a panacea for diversity and inclusivity, and that holding in-person meetings in developing economies can be at least as effective. Given that it is now relatively easy to stream contents of meetings online using low-cost methods, there are clear benefits in making all presented content accessible online, as well as organizing online networking events for those unable to attend in person.

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.

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.