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Embracing the comparative approach: how robust phylogenies and broader developmental sampling impacts the understanding of nervous system evolution

Molecular biology has provided a rich dataset to develop hypotheses of nervous system evolution. The startling patterning similarities between distantly related animals during the development of their central nervous system (CNS) have resulted in the hypothesis that a CNS with a single centralized m...

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Autores principales: Hejnol, Andreas, Lowe, Christopher J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4650123/
https://www.ncbi.nlm.nih.gov/pubmed/26554039
http://dx.doi.org/10.1098/rstb.2015.0045
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author Hejnol, Andreas
Lowe, Christopher J.
author_facet Hejnol, Andreas
Lowe, Christopher J.
author_sort Hejnol, Andreas
collection PubMed
description Molecular biology has provided a rich dataset to develop hypotheses of nervous system evolution. The startling patterning similarities between distantly related animals during the development of their central nervous system (CNS) have resulted in the hypothesis that a CNS with a single centralized medullary cord and a partitioned brain is homologous across bilaterians. However, the ability to precisely reconstruct ancestral neural architectures from molecular genetic information requires that these gene networks specifically map with particular neural anatomies. A growing body of literature representing the development of a wider range of metazoan neural architectures demonstrates that patterning gene network complexity is maintained in animals with more modest levels of neural complexity. Furthermore, a robust phylogenetic framework that provides the basis for testing the congruence of these homology hypotheses has been lacking since the advent of the field of ‘evo-devo’. Recent progress in molecular phylogenetics is refining the necessary framework to test previous homology statements that span large evolutionary distances. In this review, we describe recent advances in animal phylogeny and exemplify for two neural characters—the partitioned brain of arthropods and the ventral centralized nerve cords of annelids—a test for congruence using this framework. The sequential sister taxa at the base of Ecdysozoa and Spiralia comprise small, interstitial groups. This topology is not consistent with the hypothesis of homology of tripartitioned brain of arthropods and vertebrates as well as the ventral arthropod and rope-like ladder nervous system of annelids. There can be exquisite conservation of gene regulatory networks between distantly related groups with contrasting levels of nervous system centralization and complexity. Consequently, the utility of molecular characters to reconstruct ancestral neural organization in deep time is limited.
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spelling pubmed-46501232015-12-19 Embracing the comparative approach: how robust phylogenies and broader developmental sampling impacts the understanding of nervous system evolution Hejnol, Andreas Lowe, Christopher J. Philos Trans R Soc Lond B Biol Sci Articles Molecular biology has provided a rich dataset to develop hypotheses of nervous system evolution. The startling patterning similarities between distantly related animals during the development of their central nervous system (CNS) have resulted in the hypothesis that a CNS with a single centralized medullary cord and a partitioned brain is homologous across bilaterians. However, the ability to precisely reconstruct ancestral neural architectures from molecular genetic information requires that these gene networks specifically map with particular neural anatomies. A growing body of literature representing the development of a wider range of metazoan neural architectures demonstrates that patterning gene network complexity is maintained in animals with more modest levels of neural complexity. Furthermore, a robust phylogenetic framework that provides the basis for testing the congruence of these homology hypotheses has been lacking since the advent of the field of ‘evo-devo’. Recent progress in molecular phylogenetics is refining the necessary framework to test previous homology statements that span large evolutionary distances. In this review, we describe recent advances in animal phylogeny and exemplify for two neural characters—the partitioned brain of arthropods and the ventral centralized nerve cords of annelids—a test for congruence using this framework. The sequential sister taxa at the base of Ecdysozoa and Spiralia comprise small, interstitial groups. This topology is not consistent with the hypothesis of homology of tripartitioned brain of arthropods and vertebrates as well as the ventral arthropod and rope-like ladder nervous system of annelids. There can be exquisite conservation of gene regulatory networks between distantly related groups with contrasting levels of nervous system centralization and complexity. Consequently, the utility of molecular characters to reconstruct ancestral neural organization in deep time is limited. The Royal Society 2015-12-19 /pmc/articles/PMC4650123/ /pubmed/26554039 http://dx.doi.org/10.1098/rstb.2015.0045 Text en © 2015 The Authors. http://creativecommons.org/licenses/by/4.0/ Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.
spellingShingle Articles
Hejnol, Andreas
Lowe, Christopher J.
Embracing the comparative approach: how robust phylogenies and broader developmental sampling impacts the understanding of nervous system evolution
title Embracing the comparative approach: how robust phylogenies and broader developmental sampling impacts the understanding of nervous system evolution
title_full Embracing the comparative approach: how robust phylogenies and broader developmental sampling impacts the understanding of nervous system evolution
title_fullStr Embracing the comparative approach: how robust phylogenies and broader developmental sampling impacts the understanding of nervous system evolution
title_full_unstemmed Embracing the comparative approach: how robust phylogenies and broader developmental sampling impacts the understanding of nervous system evolution
title_short Embracing the comparative approach: how robust phylogenies and broader developmental sampling impacts the understanding of nervous system evolution
title_sort embracing the comparative approach: how robust phylogenies and broader developmental sampling impacts the understanding of nervous system evolution
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4650123/
https://www.ncbi.nlm.nih.gov/pubmed/26554039
http://dx.doi.org/10.1098/rstb.2015.0045
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