Timothy D. O'Hara

Global Diversity of Brittle Stars (Echinodermata: Ophiuroidea)

This review presents a comprehensive overview of the current status regarding the global diversity of the echinoderm class Ophiuroidea, focussing on taxonomy and distribution patterns, with brief introduction to their anatomy, biology, phylogeny, and palaeontological history. A glossary of terms is provided. Species names and taxonomic decisions have been extracted from the literature and compiled in The World Ophiuroidea Database, part of the World Register of Marine Species (WoRMS). Ophiuroidea, with 2064 known species, are the largest class of Echinodermata. A table presents 16 families with numbers of genera and species. The largest are Amphiuridae (467), Ophiuridae (344 species) and Ophiacanthidae (319 species). A biogeographic analysis for all world oceans and all accepted species was performed, based on published distribution records. Approximately similar numbers of species were recorded from the shelf (n = 1313) and bathyal depth strata (1297). The Indo-Pacific region had the highest species richness overall (825 species) and at all depths. Adjacent regions were also relatively species rich, including the North Pacific (398), South Pacific (355) and Indian (316) due to the presence of many Indo-Pacific species that partially extended into these regions. A secondary region of enhanced species richness was found in the West Atlantic (335). Regions of relatively low species richness include the Arctic (73 species), East Atlantic (118), South America (124) and Antarctic (126).

Species composition and molecular phylogeny of the Indo-Pacific teatfish (Echinodermata : Holothuroidea) bêche-de-mer fishery

Using mtDNA sequences we found that the Indo-Pacific teatfish fishery comprises at least three species, clarifying confusion on the taxonomic status of these commercially important holothurians. Traditional taxonomic characters, including the morphology of skeletal structures, could not be used to differentiate the species. Sequences of the COI gene (529 bp) distinguished three haplotype clusters, corresponding to distinct colour forms and, to some extent, previously described species. The white teatfish, Holothuria fuscogilva, comprises a range of colour morphs and has a wide distribution over the tropical Indo-Pacific region. The large sequence divergence indicates potential for the presence of several cryptic species in the white teatfish complex. In contrast to current taxonomy, we identified two species of black teatfish that appear to be allopatric: H. whitmaei is entirely black and has a Pacific distribution; whereas H. nobilis has white ventro-lateral dots and only occurs in the Indian Ocean. There is evidence for allopatric speciation between the black teatfish species, possibly driven by separation of the oceans and altered current patterns during the Pliocene, resulting in relatively young species with low intraspecific sequence divergence. These results provide insight into speciation in these tropical holothurians and are crucial for their conservation management.

A Southern Hemisphere Bathyal Fauna Is Distributed in Latitudinal Bands

The large-scale spatial distribution of seafloor fauna is still poorly understood. In particular, the bathyal zone has been identified as the key depth stratum requiring further macroecological research, particularly in the Southern Hemisphere. Here we analyze a large biological data set derived from 295 research expeditions, across an equator-to-pole sector of the Indian, Pacific, and Southern oceans, to show that the bathyal ophiuroid fauna is distributed in three broad latitudinal bands and not primarily differentiated by oceanic basins as previously assumed. Adjacent faunas form transitional ecoclines rather than biogeographical breaks. This pattern is similar to that in shallow water despite the order-of-magnitude reduction in the variability of environmental parameters at bathyal depths. A reliable biogeography is fundamental to establishing a representative network of marine reserves across the worlds oceans.

Endemism, rarity and vulnerability of marine species along a temperate coastline

The marine decapod, echinoderm and mollusc fauna from the State of Victoria, Australia, was systematically assessed for species that are potentially vulnerable to extinction. Species were identified that are short-range endemics, restricted to isolated populations, restricted to vulnerable habitats, or vulnerable to a rise in sea temperature from global warming. Of the 1650 species assessed, 3.7% were potentially endemic to Victoria, although many of these were known from few records and their described distribution may reflect collection or taxonomic artefacts. More species were restricted to vulnerable habitats: 0.7% to seagrass beds; 3% to embayments; 3.5% to the trawled area of continental shelf off east Gippsland; and 6% to the intertidal/shallow subtidal zone (0–3 m). Up to 14% of species are confined to the cool temperate waters of south-eastern Australia and could become locally extinct within Victoria from a sea temperature rise of 1–2°C. The potential for biodiversity loss from Victorian marine waters is discussed.

Origin of Macquarie Island echinoderms

Abstract The origin of echinoderms from Macquarie Island in the Southern Ocean is analysed through a novel application of multivariate statistics. Ordinations are produced from a combination of species distribution, bathymetric, habitat and life history data in order to assess patterns of migration. The analyses distinguish groups of species derived from the Kerguelen Plateau, New Zealand and eastern Antarctica. These groups correlate with attributes expected for epiplanktonic dispersal and range expansion along the North and South Macquarie Ridges respectively. There is no convincing evidence for long-distance pelagic dispersal, migration from the abyssal plain or for human translocation of species. The results indicate that taxonomic groups differ in their ability to disperse, and emphasize the importance of depth in biogeographical analyses. Dispersal by range expansion appears to have been more significant than epiplanktonic dispersal and vicariant rather than long-distance dispersal mechanisms are the preferred explanation for some disjunct distribution patterns.

Restructuring higher taxonomy using broad-scale phylogenomics: The living Ophiuroidea

The power and throughput of next-generation sequencing is instigating a major transformation in our understanding of evolution and classification of life on our planet. The new trees of life are robust and comprehensive. Here we provide a landmark phylogeny of the living ophiuroids and use it as the basis for a major revision of the higher classification of this class of marine invertebrates. We used an exon-capture system to generate a 1484 exon (273kbp) data-matrix from DNA extracted from ethanol-preserved museum samples. We successfully obtained an average of 90% of our target sequence from 576 species spread across the known taxonomic diversity. The topology of the major lineages was robust to taxon sampling, exon-sampling, models and methods. However, estimates of node age were much less precise, varying by about a quarter of mean age. We used a combination of phylogenetic distinctiveness and temporal-banding to guide our revision of the family-level classification. Empirically, we determined that limiting family crown age to 110±10Ma (mid Cretaceous) selected phylogenetically distinct nodes while minimising disruption to the existing taxonomy. The resulting scheme of 32 families and six orders considerably expands the number of higher taxa. The families are generally longitudinally widespread across the worlds oceans, although 17 are largely confined to temperate and equatorial latitudes and six to relatively shallow water (less than 1000m depth).

A new brooding species of the biscuit star Tosia (Echinodermata : Asteroidea : Goniasteridae), distinguished by molecular, morphological and larval characters

The biscuit star Tosia australis Gray, 1840 is a well known component of the shallow rocky reef fauna of south-eastern Australia. The putative T. australis species complex was subjected to reproductive, morphometric and molecular analyses. Molecular analyses of the data from three markers (mitochondrial COI and 16S rRNA and the nuclear non-coding region ITS2) confirmed the presence of a cryptic species, the morphology of which does not agree with any of the existing nominal species. Two separate reproductive modes were observed within the complex and documented via scanning electron microscopy. T. neossia, sp. nov., described herein from south-eastern Australia, is shown to release gametes from gonopores on the actinal surface. Embryos develop first into non-feeding, non-swimming brachiolaria, and then into tripod brachiolaria before metamorphosis. No surface cilia are present at any point throughout development of T. neossia. T. australis sensu stricto is shown to release gametes from the abactinal surface. Embryos develop into non-feeding, swimming brachiolaria before metamorphosis. Whereas T. australis var. astrologorum is confirmed as synonymous with T. australis, the status of the putative Western Australian taxon T. nobilis remains unresolved.

Discovery of novel representatives of bilaterian neuropeptide families and reconstruction of neuropeptide precursor evolution in ophiuroid echinoderms

Neuropeptides are a diverse class of intercellular signalling molecules that mediate neuronal regulation of many physiological and behavioural processes. Recent advances in genome/transcriptome sequencing are enabling identification of neuropeptide precursor proteins in species from a growing variety of animal taxa, providing new insights into the evolution of neuropeptide signalling. Here, detailed analysis of transcriptome sequence data from three brittle star species, Ophionotus victoriae, Amphiura filiformis and Ophiopsila aranea, has enabled the first comprehensive identification of neuropeptide precursors in the class Ophiuroidea of the phylum Echinodermata. Representatives of over 30 bilaterian neuropeptide precursor families were identified, some of which occur as paralogues. Furthermore, homologues of endothelin/CCHamide, eclosion hormone, neuropeptide-F/Y and nucleobinin/nesfatin were discovered here in a deuterostome/echinoderm for the first time. The majority of ophiuroid neuropeptide precursors contain a single copy of a neuropeptide, but several precursors comprise multiple copies of identical or non-identical, but structurally related, neuropeptides. Here, we performed an unprecedented investigation of the evolution of neuropeptide copy number over a period of approximately 270 Myr by analysing sequence data from over 50 ophiuroid species, with reference to a robust phylogeny. Our analysis indicates that the composition of neuropeptide ‘cocktails’ is functionally important, but with plasticity over long evolutionary time scales.

Identification and qualification of 500 nuclear, single-copy, orthologous genes for the Eupulmonata (Gastropoda) using transcriptome sequencing and exon capture.

The qualification of orthology is a significant challenge when developing large, multiloci phylogenetic data sets from assembled transcripts. Transcriptome assemblies have various attributes, such as fragmentation, frameshifts and mis‐indexing, which pose problems to automated methods of orthology assessment. Here, we identify a set of orthologous single‐copy genes from transcriptome assemblies for the land snails and slugs (Eupulmonata) using a thorough approach to orthology determination involving manual alignment curation, gene tree assessment and sequencing from genomic DNA. We qualified the orthology of 500 nuclear, protein‐coding genes from the transcriptome assemblies of 21 eupulmonate species to produce the most complete phylogenetic data matrix for a major molluscan lineage to date, both in terms of taxon and character completeness. Exon capture targeting 490 of the 500 genes (those with at least one exon >120 bp) from 22 species of Australian Camaenidae successfully captured sequences of 2825 exons (representing all targeted genes), with only a 3.7% reduction in the data matrix due to the presence of putative paralogs or pseudogenes. The automated pipeline Agalma retrieved the majority of the manually qualified 500 single‐copy gene set and identified a further 375 putative single‐copy genes, although it failed to account for fragmented transcripts resulting in lower data matrix completeness when considering the original 500 genes. This could potentially explain the minor inconsistencies we observed in the supported topologies for the 21 eupulmonate species between the manually curated and ‘Agalma‐equivalent’ data set (sharing 458 genes). Overall, our study confirms the utility of the 500 gene set to resolve phylogenetic relationships at a range of evolutionary depths and highlights the importance of addressing fragmentation at the homolog alignment stage for probe design.

Abyssal fauna of the UK-1 polymetallic nodule exploration claim, Clarion-Clipperton Zone, central Pacific Ocean: Echinodermata

Abstract We present data from a DNA taxonomy register of the abyssal benthic Echinodermata collected as part of the Abyssal Baseline (ABYSSLINE) environmental survey cruise ‘AB01’ to the UK Seabed Resources Ltd (UKSRL) polymetallic-nodule exploration claim ‘UK-1’ in the eastern Clarion-Clipperton Zone (CCZ), central Pacific Ocean abyssal plain. Morphological and genetic data are presented for 17 species (4 Asteroidea, 4 Crinoidea, 2 Holothuroidea and 7 Ophiuroidea) identified by a combination of morphological and genetic data. No taxa matched previously published genetic sequences, but 8 taxa could be assigned to previously-described species based on morphology, although here we have used a precautionary approach in taxon assignments to avoid over-estimating species ranges. The Clarion-Clipperton Zone is a region undergoing intense exploration for potential deep-sea mineral extraction. We present these data to facilitate future taxonomic and environmental impact study by making both data and voucher materials available through curated and accessible biological collections.