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Phylogenomics provides a robust topology of the major cnidarian lineages and insights on the origins of key organismal traits

BACKGROUND: The phylogeny of Cnidaria has been a source of debate for decades, during which nearly all-possible relationships among the major lineages have been proposed. The ecological success of Cnidaria is predicated on several fascinating organismal innovations including stinging cells, symbiosi...

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Autores principales: Kayal, Ehsan, Bentlage, Bastian, Sabrina Pankey, M., Ohdera, Aki H., Medina, Monica, Plachetzki, David C., Collins, Allen G., Ryan, Joseph F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5932825/
http://dx.doi.org/10.1186/s12862-018-1142-0
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author Kayal, Ehsan
Bentlage, Bastian
Sabrina Pankey, M.
Ohdera, Aki H.
Medina, Monica
Plachetzki, David C.
Collins, Allen G.
Ryan, Joseph F.
author_facet Kayal, Ehsan
Bentlage, Bastian
Sabrina Pankey, M.
Ohdera, Aki H.
Medina, Monica
Plachetzki, David C.
Collins, Allen G.
Ryan, Joseph F.
author_sort Kayal, Ehsan
collection PubMed
description BACKGROUND: The phylogeny of Cnidaria has been a source of debate for decades, during which nearly all-possible relationships among the major lineages have been proposed. The ecological success of Cnidaria is predicated on several fascinating organismal innovations including stinging cells, symbiosis, colonial body plans and elaborate life histories. However, understanding the origins and subsequent diversification of these traits remains difficult due to persistent uncertainty surrounding the evolutionary relationships within Cnidaria. While recent phylogenomic studies have advanced our knowledge of the cnidarian tree of life, no analysis to date has included genome-scale data for each major cnidarian lineage. RESULTS: Here we describe a well-supported hypothesis for cnidarian phylogeny based on phylogenomic analyses of new and existing genome-scale data that includes representatives of all cnidarian classes. Our results are robust to alternative modes of phylogenetic estimation and phylogenomic dataset construction. We show that two popular phylogenomic matrix construction pipelines yield profoundly different datasets, both in the identities and in the functional classes of the loci they include, but resolve the same topology. We then leverage our phylogenetic resolution of Cnidaria to understand the character histories of several critical organismal traits. Ancestral state reconstruction analyses based on our phylogeny establish several notable organismal transitions in the evolutionary history of Cnidaria and depict the ancestral cnidarian as a solitary, non-symbiotic polyp that lacked a medusa stage. In addition, Bayes factor tests strongly suggest that symbiosis has evolved multiple times independently across the cnidarian radiation. CONCLUSIONS: Cnidaria have experienced more than 600 million years of independent evolution and in the process generated an array of organismal innovations. Our results add significant clarification on the cnidarian tree of life and the histories of some of these innovations. Further, we confirm the existence of Acraspeda (staurozoans plus scyphozoans and cubozoans), thus reviving an evolutionary hypothesis put forward more than a century ago. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12862-018-1142-0) contains supplementary material, which is available to authorized users.
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spelling pubmed-59328252018-05-09 Phylogenomics provides a robust topology of the major cnidarian lineages and insights on the origins of key organismal traits Kayal, Ehsan Bentlage, Bastian Sabrina Pankey, M. Ohdera, Aki H. Medina, Monica Plachetzki, David C. Collins, Allen G. Ryan, Joseph F. BMC Evol Biol Research Article BACKGROUND: The phylogeny of Cnidaria has been a source of debate for decades, during which nearly all-possible relationships among the major lineages have been proposed. The ecological success of Cnidaria is predicated on several fascinating organismal innovations including stinging cells, symbiosis, colonial body plans and elaborate life histories. However, understanding the origins and subsequent diversification of these traits remains difficult due to persistent uncertainty surrounding the evolutionary relationships within Cnidaria. While recent phylogenomic studies have advanced our knowledge of the cnidarian tree of life, no analysis to date has included genome-scale data for each major cnidarian lineage. RESULTS: Here we describe a well-supported hypothesis for cnidarian phylogeny based on phylogenomic analyses of new and existing genome-scale data that includes representatives of all cnidarian classes. Our results are robust to alternative modes of phylogenetic estimation and phylogenomic dataset construction. We show that two popular phylogenomic matrix construction pipelines yield profoundly different datasets, both in the identities and in the functional classes of the loci they include, but resolve the same topology. We then leverage our phylogenetic resolution of Cnidaria to understand the character histories of several critical organismal traits. Ancestral state reconstruction analyses based on our phylogeny establish several notable organismal transitions in the evolutionary history of Cnidaria and depict the ancestral cnidarian as a solitary, non-symbiotic polyp that lacked a medusa stage. In addition, Bayes factor tests strongly suggest that symbiosis has evolved multiple times independently across the cnidarian radiation. CONCLUSIONS: Cnidaria have experienced more than 600 million years of independent evolution and in the process generated an array of organismal innovations. Our results add significant clarification on the cnidarian tree of life and the histories of some of these innovations. Further, we confirm the existence of Acraspeda (staurozoans plus scyphozoans and cubozoans), thus reviving an evolutionary hypothesis put forward more than a century ago. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12862-018-1142-0) contains supplementary material, which is available to authorized users. BioMed Central 2018-04-13 /pmc/articles/PMC5932825/ http://dx.doi.org/10.1186/s12862-018-1142-0 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Kayal, Ehsan
Bentlage, Bastian
Sabrina Pankey, M.
Ohdera, Aki H.
Medina, Monica
Plachetzki, David C.
Collins, Allen G.
Ryan, Joseph F.
Phylogenomics provides a robust topology of the major cnidarian lineages and insights on the origins of key organismal traits
title Phylogenomics provides a robust topology of the major cnidarian lineages and insights on the origins of key organismal traits
title_full Phylogenomics provides a robust topology of the major cnidarian lineages and insights on the origins of key organismal traits
title_fullStr Phylogenomics provides a robust topology of the major cnidarian lineages and insights on the origins of key organismal traits
title_full_unstemmed Phylogenomics provides a robust topology of the major cnidarian lineages and insights on the origins of key organismal traits
title_short Phylogenomics provides a robust topology of the major cnidarian lineages and insights on the origins of key organismal traits
title_sort phylogenomics provides a robust topology of the major cnidarian lineages and insights on the origins of key organismal traits
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5932825/
http://dx.doi.org/10.1186/s12862-018-1142-0
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