Mongiardino Koch N et al. (2018), A phylogenomic resolution of the sea urchin tre...

ECB-ART-46826

BMC Evol Biol 2018 Dec 13;181:189. doi: 10.1186/s12862-018-1300-4.

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A phylogenomic resolution of the sea urchin tree of life.

Mongiardino Koch N , Coppard SE , Lessios HA , Briggs DEG , Mooi R , Rouse GW .

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BACKGROUND: Echinoidea 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. RESULTS: We 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. CONCLUSIONS: Our 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.

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Genes referenced: LOC100887844 LOC100888042 LOC100893907

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	Fig. 1. Morphological and taxonomic diversity of echinoids included in this study. a Prionocidaris baculosa. b Lissodiadema lorioli. c Caenopedina hawaiiensis. d Asthenosoma varium. e Colobocentrotus atratus. f Strongylocentrotus purpuratus. g Pilematechinus sp. h Brissus obesus. i Dendraster excentricus. j Clypeaster subdepressus. k Conolampas sigsbei. l Current echinoid classification, modified from [6]. Clade width is proportional to the number of described extant species; clades shown in white have representatives included in this study (see Table 1). Colored pentagons are used to identify the clade to which each specimen belongs, and also correspond to the colors used in Fig. 2. Throughout, nomenclatural usage follows that of [6], in which full citations to authorities and dates for scientific names can be found. Photo credits: G.W. Rouse (a, c, e-i), FLMNH-IZ team (b), R. Mooi (d, j), H.A. Lessios (k)
	Fig. 2. a Maximum likelihood phylogram corresponding to the unpartitioned analysis. The topology was identical across all five probabilistic methods employed, and all nodes attained maximum support except for the node at the base of Scutellina, which received a bootstrap frequency of 97 and 98 in the maximum likelihood analyses under the LG4X and PMSF mixture models, respectively (see Methods). Circles represent number of genes per terminal. Numbered nodes denote novel taxon names proposed or nomenclatural amendments (see Discussion), and are defined on the top right corner. b Distance of each ingroup species to the most recent common ancestor of echinoids, which provides a metric for the relative rate of molecular evolution. Dots correspond to mean values out of 2000 estimates obtained by randomly sampling topologies from the post burn-in trees from PhyloBayes (using the CAT-Poisson model), which better accommodates scenarios of rate variation across lineages. Lines show the 95% confidence interval
	Fig. 3. Phylogenetic inference using the coalescent-based summary method ASTRAL-II. a Phylogeny obtained using all 1040 gene trees. The phylogeny conflicts with that obtained using all other methods by placing Conolampas sigsbei inside Scutellina, sister to Scutelliformes. The neognathostomate section of a supernetwork built from gene tree quartets is also depicted, showing a reticulation involving Conolampas, Echinocyamus and scutelliforms. b Phylogeny obtained using 354 gene trees, selected to minimize the negative effects of saturation and across-lineage rate heterogeneity. The position of Conolampas shifts to become sister to Scutellina (as in all other methods), with relatively strong support. To emphasize the shift in topology between the two, only neognathostomate clades have been colored (as in Fig. 2), and nodes have maximum local posterior probability unless shown. c Values of the two potentially confounding factors across all genes. Genes in red were excluded from the analysis leading to the topology shown in b. Histograms for both variables are shown next to the axes. d Summary of the results obtained performing inference with ASTRAL-II after deleting 66% of genes selected at random (100 replicates). Most replicates showed the same topology as in a. Only 16% placed Conolampas as sister to Scutellina (top), and even among them the support for this resolution was generally weak (bottom)
	Fig. 4. Distribution of phylogenetic signal for novel resolutions obtained in our phylogenomic analyses. Signal is measured as the difference in gene-wise log-likelihood scores (δ values) for the unconstrained (green) and constrained topologies enforcing monophyly of Acroechinoidea (top, red) or Clypeasteroida (bottom, blue). The same results are shown on the right, except that values are expressed as absolute differences and genes are ordered following decreasing δ values to show the overall difference in support for both alternatives
	Fig. 5. Exploration of potential non-phylogenetic signals biasing inference. Gene-wise δ values obtained by constraining acroechinoid (top) and clypeasteroid (bottom) monophyly are shown using dot size and color (as in Fig. 4, see legend). Root-to-tip variance axs were truncated to show the region in which most data points lie. The relative support for these topological alternatives does not depend on the four potentially biasing factors explored, as seen by the lack of clustering of genes with similar δ values along the axes

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