Abstract

BackgroundEchinoidea is a clade of marine animals including sea urchins, heart urchins, sand dollars and sea biscuits. Found in benthic habitats across all latitudes, echinoids are key components of marine communities such as coral reefs and kelp forests. A little over 1000 species inhabit the oceans today, a diversity that traces its roots back at least to the Permian. Although much effort has been devoted to elucidating the echinoid tree of life using a variety of morphological data, molecular attempts have relied on only a handful of genes. Both of these approaches have had limited success at resolving the deepest nodes of the tree, and their disagreement over the positions of a number of clades remains unresolved.ResultsWe performed de novo sequencing and assembly of 17 transcriptomes to complement available genomic resources of sea urchins and produce the first phylogenomic analysis of the clade. Multiple methods of probabilistic inference recovered identical topologies, with virtually all nodes showing maximum support. In contrast, the coalescent-based method ASTRAL-II resolved one node differently, a result apparently driven by gene tree error induced by evolutionary rate heterogeneity. Regardless of the method employed, our phylogenetic structure deviates from the currently accepted classification of echinoids, with neither Acroechinoidea (all euechinoids except echinothurioids), nor Clypeasteroida (sand dollars and sea biscuits) being monophyletic as currently defined. We show that phylogenetic signal for novel resolutions of these lineages is strong and distributed throughout the genome, and fail to recover systematic biases as drivers of our results.ConclusionsOur investigation substantially augments the molecular resources available for sea urchins, providing the first transcriptomes for many of its main lineages. Using this expanded genomic dataset, we resolve the position of several clades in agreement with early molecular analyses but in disagreement with morphological data. Our efforts settle multiple phylogenetic uncertainties, including the position of the enigmatic deep-sea echinothurioids and the identity of the sister clade to sand dollars. We offer a detailed assessment of evolutionary scenarios that could reconcile our findings with morphological evidence, opening up new lines of research into the development and evolutionary history of this ancient clade.

Highlights

  • Echinoidea is a clade of marine animals including sea urchins, heart urchins, sand dollars and sea biscuits

  • We find no evidence that this signal is restricted to a few “outlier” genes or that it stems from systematic biases, but rather it appears to be the result of true phylogenetic signal distributed throughout the genome (Figs. 4 and 5)

  • This study expands the set of transcriptomic resources for sea urchins, providing the first available data for many distinct lineages

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Summary

Introduction

Echinoidea is a clade of marine animals including sea urchins, heart urchins, sand dollars and sea biscuits. Echinoidea Leske, 1778 is a clade of marine animals including species commonly known as sea urchins, heart urchins, sand dollars and sea biscuits. It constitutes one of the five main clades of extant Echinodermata, typically pentaradially symmetric animals, which includes highly distinctive components of the marine fauna such as Mongiardino Koch et al BMC Evolutionary Biology (2018) 18:189 as between asteroids and ophiuroids, with crinoids as sister to them all [3,4,5]. This line of research was radically expanded recently through the application of massive sequencing methods, resulting in major breakthroughs in our understanding of the organization of deuterostome genomes and the gene regulatory networks that underlie embryogenesis [21, 22]

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