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Testing hypotheses of developmental constraints on mammalian brain partition evolution, using marsupials

There is considerable debate about whether the partition volumes of the mammalian brain (e.g. cerebrum, cerebellum) evolve according to functional selection, or whether developmental constraints of conserved neurogenetic scheduling cause predictable partition scaling with brain size. Here we provide...

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Autores principales: Carlisle, Alison, Selwood, Lynne, Hinds, Lyn A., Saunders, Norman, Habgood, Mark, Mardon, Karine, Weisbecker, Vera
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5484667/
https://www.ncbi.nlm.nih.gov/pubmed/28652619
http://dx.doi.org/10.1038/s41598-017-02726-9
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author Carlisle, Alison
Selwood, Lynne
Hinds, Lyn A.
Saunders, Norman
Habgood, Mark
Mardon, Karine
Weisbecker, Vera
author_facet Carlisle, Alison
Selwood, Lynne
Hinds, Lyn A.
Saunders, Norman
Habgood, Mark
Mardon, Karine
Weisbecker, Vera
author_sort Carlisle, Alison
collection PubMed
description There is considerable debate about whether the partition volumes of the mammalian brain (e.g. cerebrum, cerebellum) evolve according to functional selection, or whether developmental constraints of conserved neurogenetic scheduling cause predictable partition scaling with brain size. Here we provide the first investigation of developmental constraints on partition volume growth, derived from contrast-enhanced micro-computed tomography of hydrogel-stabilized brains from three marsupial species. ANCOVAs of partition vs. brain volume scaling, as well as growth curve comparisons, do not support several hypotheses consistent with developmental constraints: brain partition growth significantly differs between species, or between developing vs. adult marsupials. Partition growth appears independent of adult brain volume, with no discernable growth spurts/lags relatable to internal structural change. Rather, adult proportion differences appear to arise through growth rate/duration heterochrony. Substantial phylogenetic signal in adult brain partitions scaling with brain volume also counters expectations of development-mediated partition scaling conservatism. However, the scaling of olfactory bulb growth is markedly irregular, consistent with suggestions that it is less constrained. The very regular partition growth curves suggest intraspecific developmental rigidity. We speculate that a rigid, possibly neuromer-model-like early molecular program might be responsible both for regular growth curves within species and impressions of a link between neurogenesis and partition evolution.
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spelling pubmed-54846672017-06-30 Testing hypotheses of developmental constraints on mammalian brain partition evolution, using marsupials Carlisle, Alison Selwood, Lynne Hinds, Lyn A. Saunders, Norman Habgood, Mark Mardon, Karine Weisbecker, Vera Sci Rep Article There is considerable debate about whether the partition volumes of the mammalian brain (e.g. cerebrum, cerebellum) evolve according to functional selection, or whether developmental constraints of conserved neurogenetic scheduling cause predictable partition scaling with brain size. Here we provide the first investigation of developmental constraints on partition volume growth, derived from contrast-enhanced micro-computed tomography of hydrogel-stabilized brains from three marsupial species. ANCOVAs of partition vs. brain volume scaling, as well as growth curve comparisons, do not support several hypotheses consistent with developmental constraints: brain partition growth significantly differs between species, or between developing vs. adult marsupials. Partition growth appears independent of adult brain volume, with no discernable growth spurts/lags relatable to internal structural change. Rather, adult proportion differences appear to arise through growth rate/duration heterochrony. Substantial phylogenetic signal in adult brain partitions scaling with brain volume also counters expectations of development-mediated partition scaling conservatism. However, the scaling of olfactory bulb growth is markedly irregular, consistent with suggestions that it is less constrained. The very regular partition growth curves suggest intraspecific developmental rigidity. We speculate that a rigid, possibly neuromer-model-like early molecular program might be responsible both for regular growth curves within species and impressions of a link between neurogenesis and partition evolution. Nature Publishing Group UK 2017-06-26 /pmc/articles/PMC5484667/ /pubmed/28652619 http://dx.doi.org/10.1038/s41598-017-02726-9 Text en © The Author(s) 2017 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Carlisle, Alison
Selwood, Lynne
Hinds, Lyn A.
Saunders, Norman
Habgood, Mark
Mardon, Karine
Weisbecker, Vera
Testing hypotheses of developmental constraints on mammalian brain partition evolution, using marsupials
title Testing hypotheses of developmental constraints on mammalian brain partition evolution, using marsupials
title_full Testing hypotheses of developmental constraints on mammalian brain partition evolution, using marsupials
title_fullStr Testing hypotheses of developmental constraints on mammalian brain partition evolution, using marsupials
title_full_unstemmed Testing hypotheses of developmental constraints on mammalian brain partition evolution, using marsupials
title_short Testing hypotheses of developmental constraints on mammalian brain partition evolution, using marsupials
title_sort testing hypotheses of developmental constraints on mammalian brain partition evolution, using marsupials
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5484667/
https://www.ncbi.nlm.nih.gov/pubmed/28652619
http://dx.doi.org/10.1038/s41598-017-02726-9
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