Timothy D. O’Hara

Phylogenomic Resolution of the Class Ophiuroidea Unlocks a Global Microfossil Record

Our understanding of the origin, evolution, and biogeography of seafloor fauna is limited because we have insufficient spatial and temporal data to resolve underlying processes. The abundance and wide distribution of modern and disarticulated fossil Ophiuroidea, including brittle stars and basket stars, make them an ideal model system for global marine biogeography if we have the phylogenetic framework necessary to link extant and fossil morphology in an evolutionary context. Here we construct a phylogeny from a highly complete 425-gene, 61-taxa transcriptome-based data set covering 15 of the 18 ophiuroid families and representatives of all extant echinoderm classes. We calibrate our phylogeny with a series of novel fossil discoveries from the early Mesozoic. We confirm the traditional paleontological view that ophiuroids are sister to the asteroids and date the crown group Ophiuroidea to the mid-Permian (270 ± 30 mega-annum). We refute all historical classification schemes of the Ophiuroidea based on gross structural characters but find strong congruence with schemes based on lateral arm plate microstructure and the temporal appearance of various plate morphologies in the fossil record. The verification that these microfossils contain phylogenetically informative characters unlocks their potential to advance our understanding of marine biogeographical processes.

Commonness and rarity in the marine biosphere

Significance Tests of biodiversity theory have been controversial partly because alternative formulations of the same theory seemingly yield different conclusions. This has been a particular challenge for neutral theory, which has dominated tests of biodiversity theory over the last decade. Neutral theory attributes differences in species abundances to chance variation in individuals’ fates, rather than differences in species traits. By identifying common features of different neutral models, we conduct a uniquely robust test of neutral theory across a global dataset of marine assemblages. Consistently, abundances vary more among species than neutral theory predicts, challenging the hypothesis that community dynamics are approximately neutral, and implicating species differences as a key driver of community structure in nature. Explaining patterns of commonness and rarity is fundamental for understanding and managing biodiversity. Consequently, a key test of biodiversity theory has been how well ecological models reproduce empirical distributions of species abundances. However, ecological models with very different assumptions can predict similar species abundance distributions, whereas models with similar assumptions may generate very different predictions. This complicates inferring processes driving community structure from model fits to data. Here, we use an approximation that captures common features of “neutral” biodiversity models—which assume ecological equivalence of species—to test whether neutrality is consistent with patterns of commonness and rarity in the marine biosphere. We do this by analyzing 1,185 species abundance distributions from 14 marine ecosystems ranging from intertidal habitats to abyssal depths, and from the tropics to polar regions. Neutrality performs substantially worse than a classical nonneutral alternative: empirical data consistently show greater heterogeneity of species abundances than expected under neutrality. Poor performance of neutral theory is driven by its consistent inability to capture the dominance of the communities’ most-abundant species. Previous tests showing poor performance of a neutral model for a particular system often have been followed by controversy about whether an alternative formulation of neutral theory could explain the data after all. However, our approach focuses on common features of neutral models, revealing discrepancies with a broad range of empirical abundance distributions. These findings highlight the need for biodiversity theory in which ecological differences among species, such as niche differences and demographic trade-offs, play a central role.

Deep-sea diversity patterns are shaped by energy availability

The deep ocean is the largest and least-explored ecosystem on Earth, and a uniquely energy-poor environment. The distribution, drivers and origins of deep-sea biodiversity remain unknown at global scales. Here we analyse a database of more than 165,000 distribution records of Ophiuroidea (brittle stars), a dominant component of sea-floor fauna, and find patterns of biodiversity unlike known terrestrial or coastal marine realms. Both patterns and environmental predictors of deep-sea (2,000–6,500 m) species richness fundamentally differ from those found in coastal (0–20 m), continental shelf (20–200 m), and upper-slope (200–2,000 m) waters. Continental shelf to upper-slope richness consistently peaks in tropical Indo-west Pacific and Caribbean (0–30°) latitudes, and is well explained by variations in water temperature. In contrast, deep-sea species show maximum richness at higher latitudes (30–50°), concentrated in areas of high carbon export flux and regions close to continental margins. We reconcile this structuring of oceanic biodiversity using a species–energy framework, with kinetic energy predicting shallow-water richness, while chemical energy (export productivity) and proximity to slope habitats drive deep-sea diversity. Our findings provide a global baseline for conservation efforts across the sea floor, and demonstrate that deep-sea ecosystems show a biodiversity pattern consistent with ecological theory, despite being different from other planetary-scale habitats.

An Exon-Capture System for the Entire Class Ophiuroidea

Exon-capture studies have typically been restricted to relatively shallow phylogenetic scales due primarily to hybridization constraints. Here, we present an exon-capture system for an entire class of marine invertebrates, the Ophiuroidea, built upon a phylogenetically diverse transcriptome foundation. The system captures approximately 90% of the 1,552 exon target, across all major lineages of the quarter-billion-year-old extant crown group. Key features of our system are 1) basing the target on an alignment of orthologous genes determined from 52 transcriptomes spanning the phylogenetic diversity and trimmed to remove anything difficult to capture, map, or align; 2) use of multiple artificial representatives based on ancestral state reconstructions rather than exemplars to improve capture and mapping of the target; 3) mapping reads to a multi-reference alignment; and 4) using patterns of site polymorphism to distinguish among paralogy, polyploidy, allelic differences, and sample contamination. The resulting data give a well-resolved tree (currently standing at 417 samples, 275,352 sites, 91% data-complete) that will transform our understanding of ophiuroid evolution and biogeography.

Molecular phylogeny of the order Euryalida (Echinodermata: Ophiuroidea), based on mitochondrial and nuclear ribosomal genes

The existing taxonomy of Euryalida, one of the two orders of the Ophiuroidea (Echinodermata), is uncertain and characterized by controversial delimitation of taxonomic ranks from genus to family-level. Their phylogeny was not studied in detail until now. We investigated a dataset of sequence from a mitochondrial gene (16S rRNA) and two nucleic genes (18S rRNA and 28S rRNA) for 49 euryalid ophiuroids and four outgroup species from the order Ophiurida. The monophyly of the order Euryalida was supported as was the monophyly of Asteronychidae, Gorgonocephalidae and an Asteroschematidae+Euryalidae clade. However, the group currently known as the Asteroschematidae was paraphyletic with respect to the Euryalidae. The Asteroschematidae+Euryalidae clade, which we recognise as an enlarged Euryalidae, contains three natural groups: the Asteroschematinae (Asteroschema and Ophiocreas), a new subfamily Astrocharinae (Astrocharis) and the Euryalinae with remaining genera. These subfamilies can be distinguished by internal ossicle morphology.

When Ontogeny Matters: A New Japanese Species of Brittle Star Illustrates the Importance of Considering both Adult and Juvenile Characters in Taxonomic Practice

Current taxonomy offers numerous approaches and methods for species delimitation and description. However, most of them are based on the adult characters and rarely suggest a dynamic representation of developmental transformations of taxonomically important features. Here we show how the underestimation of ontogenetic changes may result in long term lack of recognition of a new species of one of the most common ophiacanthid brittle stars (Echinodermata: Ophiuroidea) from the North Pacific. Based on vast material collected predominantly by various Japanese expeditions in the course of more than 50 years, and thorough study of appropriate type material, we revise the complex of three common species of the ophiuroid genus Ophiacantha which have been persistently confused with each other. The present study thus reveals the previously unrecognized new species Ophiacantha kokusai sp.nov. which is commonly distributed off the Pacific coast of Japan. The new species shows developmental differentiation from the closely related species Ophiacantha rhachophora H. L. Clark, 1911 and retains clearly expressed early juvenile features in the adult morphology. Another species, Ophiacantha clypeata Kyte, 1977, which had been separated from O. rhachophora, is in turn shown to be just a juvenile stage of another North Pacific species, Ophiacantha trachybactra H.L. Clark, 1911. For every species, detailed morphological data from both adult and juvenile specimens based on scanning electron microscopy are presented. A special grinding method showing complex internal features has been utilized for the first time. For all three species in this complex, a clear bathymetric differentiation is revealed: O. rhachophora predominantly inhabits shallow waters, 0–250 m, the new species O. kokusai lives deeper, at 250–600 m, and the third species, O. trachybactra, is found at 500–2,000 m. The present case clearly highlights the importance of considering developmental transformations, not only for a limited number of model organisms, but as part of the taxonomic process.

Apartment-style living on a kebab sponge

Sponges are important three-dimensional habitats for other organisms such as polychaetes, crustaceans, echinoderms and fish that often live or breed on preferred parts of a sponge, thus reflecting functional relationships (e.g. Koukouras et al. 1995). Most Caulospongia spp. (Demospongiae: Suberitida) have morphologies supportive of epibiosis. They are characterized by an erect axis and basal stalk, with a reticulate body with lumina, or horizontal, disc-like lobes arranged along the axis (Fromont 1998). This tiered morphology led to our field name ‘kebab sponge’ (Fig. 1a–c). We sampled a specimen of Caulospongia pennatula (Lamarck, 1814) at Ningaloo Reef, northwestern Australia, that had wide horizontal surfaces, and on the edges underneath each tier, one or two—never more—porce la in crabs Pis id ia cf . streptochiroides (Johnson, 1970) were found (Fig. 1c–e). Porcelain crabs can be vividly coloured, mimicking the appearance of the surface they live on (Haig 1981). Here they were of a slightly lighter ochre colour than the sponge and thus well camouflaged (Fig. 1d–f). The hollow, lattice-like axis of the sponge was inhabited by Ophiothrix sp. brittlestars, whose bodies were lodged within, with their arms extending onto the lobes, also of a similar colour (Fig. 1g–k). Brittlestars are known to feed on detritus on benthic invertebrate surfaces (Stewart 1998), while porcelain crabs can scavenge or feed on host exudates, but mostly filter the water column using modified mouthparts (Kropp 1981). Presumably, the porcelain crabs colonise the sponge in order to be elevated above the seafloor to gain access to water currents, and may also benefit from the sponge’s feeding currents. We counted 19 crabs (seven males, seven egg-carrying females, five juveniles) and three brittlestars on this sponge. Thus, the morphology of a kebab sponge has microhabitats that offer shelter and possibly enhanced nutrition, while allowing epibionts to be elevated in the water column.

Dendrogramma is a siphonophore

Dendrogramma was the iconic deep-sea animal of 2014, voted among the top-ten new species described that year [1]. The two species described are mushroom shaped animals, diploblastic, with an apparent gastrovascular system that extends from the base of the stalk to bifurcating canals that radiate through the flat disc [2]. The authors could not assign the new genus to any known animal group with certainty, leading to numerous media reports that it belonged to an entirely new phylum. Here we use phylogenomic data from newly collected specimens to show that Dendrogramma is a cnidarian, specifically a benthic siphonophore in the family Rhodaliidae. Although an entire Dendrogramma colony has not been found, we hypothesise that the mushroom-like bodies are bracts, possibly used to aid buoyancy or as defensive appendages to protect feeding gastrozooids or gonads.