A phylogenomic resolution of the sea urchin tree of life

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.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1300-4) contains supplementary material, which is available to authorized users.

A Total-Evidence Dated Phylogeny of Echinoids and the Evolution of Body Size across Adaptive Landscape

“…Given the supposedly primitive nature of this condition, other unique characteristics of echinothurioids were also interpreted as plesiomorphic. Molecular evidence, on the other hand, supported a derived position of echinothurioids (Smith et al 2006; Thompson et al 2017; Mongiardino Koch et al 2018), nested in a clade that includes lineages characterized by a unique dental morphology (aspidodiadematoids, diadematoids, pedinoids and micropygoids). This clade was also favored by some early systematists (Jackson 1912; Durham and Melville 1957), and has since been named Aulodonta (Kroh 2020).…”

“…However, the resolution of a few key regions of the echinoid tree of life systematically disagreed. Although initially disregarded as artifacts of poor sampling or low phylogenetic signal in molecular datasets, the consistent recovery of nodes not supported by morphology (Littlewood and Smith 1995; Smith et al 1995; Smith et al 2006; Smith and Kroh 2013; Thompson et al 2017; Mongiardino Koch et al 2018) eventually cast doubt on morphological topologies.…”

“…This clade was also favored by some early systematists (Jackson 1912; Durham and Melville 1957), and has since been named Aulodonta (Kroh 2020). Under this alternative scenario, the evolution of test flexibility among echinothurioids, along with the other unique features of the clade, likely constitute autapomorphies (Mongiardino Koch et al 2018). Given that the deepest euechinoid lineages likely diverged during the Triassic (Kier 1977; Smith et al 2006; Thompson et al 2017), conflicting solutions between morphological and ribosomal datasets are not surprising.…”

“…Numerous synapomorphies unite clypeasteroids to the exclusion of “cassiduloids” (e.g., extreme flattening and internal reinforcement of the test, multiplication of tube feet per plate, presence of an Aristotle’s lantern in adults; Mooi 1990b; Kroh and Smith 2010). Nonetheless, all previous molecular studies have yielded a paraphyletic Clypeasteroida (Littlewood and Smith 1995; Smith et al 1995; Smith et al 2006; Nowak et al 2013; Smith and Kroh 2013; Thompson et al 2017; Mongiardino Koch et al 2018), with at least one extant “cassiduloid” nested inside the clade. This resolution strongly conflicts with morphological evidence, and implies substantially longer ghost ranges for clypeasteroids, a clade with a remarkable fossil record (Kroh and Smith 2010).…”

“…It was therefore deemed too problematic and disregarded in favor of the morphological hypothesis (Kroh and Smith 2010; Smith and Kroh 2013). More recently, the strong support for a sister group relationship between echinolampadoids and sand dollars prompted Mongiardino Koch et al (2018) to restrict Clypeasteroida to include only the sea biscuits (henceforth, the usage given to this name), and reclassify the sand dollars in a separate order (Scutelloida), a nomenclatural change followed by Kroh (2020). The implications of this topology for the position of the remaining “cassiduloids” remain unclear, however, as well as leaving open questions regarding the evolution of the many morphological features that conflict with it.…”