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An integrative systematic framework helps to reconstruct skeletal evolution of glass sponges (Porifera, Hexactinellida)

BACKGROUND: Glass sponges (Class Hexactinellida) are important components of deep-sea ecosystems and are of interest from geological and materials science perspectives. The reconstruction of their phylogeny with molecular data has only recently begun and shows a better agreement with morphology-base...

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Autores principales: Dohrmann, Martin, Kelley, Christopher, Kelly, Michelle, Pisera, Andrzej, Hooper, John N. A., Reiswig, Henry M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5359874/
https://www.ncbi.nlm.nih.gov/pubmed/28331531
http://dx.doi.org/10.1186/s12983-017-0191-3
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author Dohrmann, Martin
Kelley, Christopher
Kelly, Michelle
Pisera, Andrzej
Hooper, John N. A.
Reiswig, Henry M.
author_facet Dohrmann, Martin
Kelley, Christopher
Kelly, Michelle
Pisera, Andrzej
Hooper, John N. A.
Reiswig, Henry M.
author_sort Dohrmann, Martin
collection PubMed
description BACKGROUND: Glass sponges (Class Hexactinellida) are important components of deep-sea ecosystems and are of interest from geological and materials science perspectives. The reconstruction of their phylogeny with molecular data has only recently begun and shows a better agreement with morphology-based systematics than is typical for other sponge groups, likely because of a greater number of informative morphological characters. However, inconsistencies remain that have far-reaching implications for hypotheses about the evolution of their major skeletal construction types (body plans). Furthermore, less than half of all described extant genera have been sampled for molecular systematics, and several taxa important for understanding skeletal evolution are still missing. Increased taxon sampling for molecular phylogenetics of this group is therefore urgently needed. However, due to their remote habitat and often poorly preserved museum material, sequencing all 126 currently recognized extant genera will be difficult to achieve. Utilizing morphological data to incorporate unsequenced taxa into an integrative systematics framework therefore holds great promise, but it is unclear which methodological approach best suits this task. RESULTS: Here, we increase the taxon sampling of four previously established molecular markers (18S, 28S, and 16S ribosomal DNA, as well as cytochrome oxidase subunit I) by 12 genera, for the first time including representatives of the order Aulocalycoida and the type genus of Dactylocalycidae, taxa that are key to understanding hexactinellid body plan evolution. Phylogenetic analyses suggest that Aulocalycoida is diphyletic and provide further support for the paraphyly of order Hexactinosida; hence these orders are abolished from the Linnean classification. We further assembled morphological character matrices to integrate so far unsequenced genera into phylogenetic analyses in maximum parsimony (MP), maximum likelihood (ML), Bayesian, and morphology-based binning frameworks. We find that of these four approaches, total-evidence analysis using MP gave the most plausible results concerning congruence with existing phylogenetic and taxonomic hypotheses, whereas the other methods, especially ML and binning, performed more poorly. We use our total-evidence phylogeny of all extant glass sponge genera for ancestral state reconstruction of morphological characters in MP and ML frameworks, gaining new insights into the evolution of major hexactinellid body plans and other characters such as different spicule types. CONCLUSIONS: Our study demonstrates how a comprehensive, albeit in some parts provisional, phylogeny of a larger taxon can be achieved with an integrative approach utilizing molecular and morphological data, and how this can be used as a basis for understanding phenotypic evolution. The datasets and associated trees presented here are intended as a resource and starting point for future work on glass sponge evolution. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12983-017-0191-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-53598742017-03-22 An integrative systematic framework helps to reconstruct skeletal evolution of glass sponges (Porifera, Hexactinellida) Dohrmann, Martin Kelley, Christopher Kelly, Michelle Pisera, Andrzej Hooper, John N. A. Reiswig, Henry M. Front Zool Research BACKGROUND: Glass sponges (Class Hexactinellida) are important components of deep-sea ecosystems and are of interest from geological and materials science perspectives. The reconstruction of their phylogeny with molecular data has only recently begun and shows a better agreement with morphology-based systematics than is typical for other sponge groups, likely because of a greater number of informative morphological characters. However, inconsistencies remain that have far-reaching implications for hypotheses about the evolution of their major skeletal construction types (body plans). Furthermore, less than half of all described extant genera have been sampled for molecular systematics, and several taxa important for understanding skeletal evolution are still missing. Increased taxon sampling for molecular phylogenetics of this group is therefore urgently needed. However, due to their remote habitat and often poorly preserved museum material, sequencing all 126 currently recognized extant genera will be difficult to achieve. Utilizing morphological data to incorporate unsequenced taxa into an integrative systematics framework therefore holds great promise, but it is unclear which methodological approach best suits this task. RESULTS: Here, we increase the taxon sampling of four previously established molecular markers (18S, 28S, and 16S ribosomal DNA, as well as cytochrome oxidase subunit I) by 12 genera, for the first time including representatives of the order Aulocalycoida and the type genus of Dactylocalycidae, taxa that are key to understanding hexactinellid body plan evolution. Phylogenetic analyses suggest that Aulocalycoida is diphyletic and provide further support for the paraphyly of order Hexactinosida; hence these orders are abolished from the Linnean classification. We further assembled morphological character matrices to integrate so far unsequenced genera into phylogenetic analyses in maximum parsimony (MP), maximum likelihood (ML), Bayesian, and morphology-based binning frameworks. We find that of these four approaches, total-evidence analysis using MP gave the most plausible results concerning congruence with existing phylogenetic and taxonomic hypotheses, whereas the other methods, especially ML and binning, performed more poorly. We use our total-evidence phylogeny of all extant glass sponge genera for ancestral state reconstruction of morphological characters in MP and ML frameworks, gaining new insights into the evolution of major hexactinellid body plans and other characters such as different spicule types. CONCLUSIONS: Our study demonstrates how a comprehensive, albeit in some parts provisional, phylogeny of a larger taxon can be achieved with an integrative approach utilizing molecular and morphological data, and how this can be used as a basis for understanding phenotypic evolution. The datasets and associated trees presented here are intended as a resource and starting point for future work on glass sponge evolution. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12983-017-0191-3) contains supplementary material, which is available to authorized users. BioMed Central 2017-03-21 /pmc/articles/PMC5359874/ /pubmed/28331531 http://dx.doi.org/10.1186/s12983-017-0191-3 Text en © The Author(s). 2017 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
Dohrmann, Martin
Kelley, Christopher
Kelly, Michelle
Pisera, Andrzej
Hooper, John N. A.
Reiswig, Henry M.
An integrative systematic framework helps to reconstruct skeletal evolution of glass sponges (Porifera, Hexactinellida)
title An integrative systematic framework helps to reconstruct skeletal evolution of glass sponges (Porifera, Hexactinellida)
title_full An integrative systematic framework helps to reconstruct skeletal evolution of glass sponges (Porifera, Hexactinellida)
title_fullStr An integrative systematic framework helps to reconstruct skeletal evolution of glass sponges (Porifera, Hexactinellida)
title_full_unstemmed An integrative systematic framework helps to reconstruct skeletal evolution of glass sponges (Porifera, Hexactinellida)
title_short An integrative systematic framework helps to reconstruct skeletal evolution of glass sponges (Porifera, Hexactinellida)
title_sort integrative systematic framework helps to reconstruct skeletal evolution of glass sponges (porifera, hexactinellida)
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5359874/
https://www.ncbi.nlm.nih.gov/pubmed/28331531
http://dx.doi.org/10.1186/s12983-017-0191-3
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