A phylogenomic resolution of the sea urchin tree of life

Abstract 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...

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Main Authors: Nicolás Mongiardino Koch, Simon E. Coppard, Harilaos A. Lessios, Derek E. G. Briggs, Rich Mooi, Greg W. Rouse
Format: Article
Language:English
Published: BMC 2018-12-01
Series:BMC Evolutionary Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12862-018-1300-4
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author Nicolás Mongiardino Koch
Simon E. Coppard
Harilaos A. Lessios
Derek E. G. Briggs
Rich Mooi
Greg W. Rouse
author_facet Nicolás Mongiardino Koch
Simon E. Coppard
Harilaos A. Lessios
Derek E. G. Briggs
Rich Mooi
Greg W. Rouse
author_sort Nicolás Mongiardino Koch
collection DOAJ
description Abstract 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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spelling doaj.art-7d78a28e10b04486a1ded5b4979a59d82022-12-21T21:47:29ZengBMCBMC Evolutionary Biology1471-21482018-12-0118111810.1186/s12862-018-1300-4A phylogenomic resolution of the sea urchin tree of lifeNicolás Mongiardino Koch0Simon E. Coppard1Harilaos A. Lessios2Derek E. G. Briggs3Rich Mooi4Greg W. Rouse5Department of Geology and Geophysics, Yale UniversityDepartment of Biology, Hamilton CollegeSmithsonian Tropical Research InstituteDepartment of Geology and Geophysics, Yale UniversityDepartment of Invertebrate Zoology and Geology, California Academy of SciencesScripps Institution of Oceanography, UC San DiegoAbstract 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.http://link.springer.com/article/10.1186/s12862-018-1300-4EchinoideaSea urchinsSand dollarsPhylogenomicsGenomeTranscriptome
spellingShingle Nicolás Mongiardino Koch
Simon E. Coppard
Harilaos A. Lessios
Derek E. G. Briggs
Rich Mooi
Greg W. Rouse
A phylogenomic resolution of the sea urchin tree of life
BMC Evolutionary Biology
Echinoidea
Sea urchins
Sand dollars
Phylogenomics
Genome
Transcriptome
title A phylogenomic resolution of the sea urchin tree of life
title_full A phylogenomic resolution of the sea urchin tree of life
title_fullStr A phylogenomic resolution of the sea urchin tree of life
title_full_unstemmed A phylogenomic resolution of the sea urchin tree of life
title_short A phylogenomic resolution of the sea urchin tree of life
title_sort phylogenomic resolution of the sea urchin tree of life
topic Echinoidea
Sea urchins
Sand dollars
Phylogenomics
Genome
Transcriptome
url http://link.springer.com/article/10.1186/s12862-018-1300-4
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