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Molecular and morphological analysis of the developing nemertean brain indicates convergent evolution of complex brains in Spiralia

BACKGROUND: The brain anatomy in the clade Spiralia can vary from simple, commissural brains (e.g., gastrotrichs, rotifers) to rather complex, partitioned structures (e.g., in cephalopods and annelids). How often and in which lineages complex brains evolved still remains unclear. Nemerteans are a cl...

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Autores principales: Gąsiorowski, Ludwik, Børve, Aina, Cherneva, Irina A., Orús-Alcalde, Andrea, Hejnol, Andreas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8400761/
https://www.ncbi.nlm.nih.gov/pubmed/34452633
http://dx.doi.org/10.1186/s12915-021-01113-1
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author Gąsiorowski, Ludwik
Børve, Aina
Cherneva, Irina A.
Orús-Alcalde, Andrea
Hejnol, Andreas
author_facet Gąsiorowski, Ludwik
Børve, Aina
Cherneva, Irina A.
Orús-Alcalde, Andrea
Hejnol, Andreas
author_sort Gąsiorowski, Ludwik
collection PubMed
description BACKGROUND: The brain anatomy in the clade Spiralia can vary from simple, commissural brains (e.g., gastrotrichs, rotifers) to rather complex, partitioned structures (e.g., in cephalopods and annelids). How often and in which lineages complex brains evolved still remains unclear. Nemerteans are a clade of worm-like spiralians, which possess a complex central nervous system (CNS) with a prominent brain, and elaborated chemosensory and neuroglandular cerebral organs, which have been previously suggested as homologs to the annelid mushroom bodies. To understand the developmental and evolutionary origins of the complex brain in nemerteans and spiralians in general, we investigated details of the neuroanatomy and gene expression in the brain and cerebral organs of the juveniles of nemertean Lineus ruber. RESULTS: In the juveniles, the CNS is already composed of all major elements present in the adults, including the brain, paired longitudinal lateral nerve cords, and an unpaired dorsal nerve cord, which suggests that further neural development is mostly related with increase in the size but not in complexity. The ultrastructure of the juvenile cerebral organ revealed that it is composed of several distinct cell types present also in the adults. The 12 transcription factors commonly used as brain cell type markers in bilaterians show region-specific expression in the nemertean brain and divide the entire organ into several molecularly distinct areas, partially overlapping with the morphological compartments. Additionally, several of the mushroom body-specific genes are expressed in the developing cerebral organs. CONCLUSIONS: The dissimilar expression of molecular brain markers between L. ruber and the annelid Platynereis dumerilii indicates that the complex brains present in those two species evolved convergently by independent expansions of non-homologous regions of a simpler brain present in their last common ancestor. Although the same genes are expressed in mushroom bodies and cerebral organs, their spatial expression within organs shows apparent differences between annelids and nemerteans, indicating convergent recruitment of the same genes into patterning of non-homologous organs or hint toward a more complicated evolutionary process, in which conserved and novel cell types contribute to the non-homologous structures. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-01113-1.
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spelling pubmed-84007612021-08-30 Molecular and morphological analysis of the developing nemertean brain indicates convergent evolution of complex brains in Spiralia Gąsiorowski, Ludwik Børve, Aina Cherneva, Irina A. Orús-Alcalde, Andrea Hejnol, Andreas BMC Biol Research Article BACKGROUND: The brain anatomy in the clade Spiralia can vary from simple, commissural brains (e.g., gastrotrichs, rotifers) to rather complex, partitioned structures (e.g., in cephalopods and annelids). How often and in which lineages complex brains evolved still remains unclear. Nemerteans are a clade of worm-like spiralians, which possess a complex central nervous system (CNS) with a prominent brain, and elaborated chemosensory and neuroglandular cerebral organs, which have been previously suggested as homologs to the annelid mushroom bodies. To understand the developmental and evolutionary origins of the complex brain in nemerteans and spiralians in general, we investigated details of the neuroanatomy and gene expression in the brain and cerebral organs of the juveniles of nemertean Lineus ruber. RESULTS: In the juveniles, the CNS is already composed of all major elements present in the adults, including the brain, paired longitudinal lateral nerve cords, and an unpaired dorsal nerve cord, which suggests that further neural development is mostly related with increase in the size but not in complexity. The ultrastructure of the juvenile cerebral organ revealed that it is composed of several distinct cell types present also in the adults. The 12 transcription factors commonly used as brain cell type markers in bilaterians show region-specific expression in the nemertean brain and divide the entire organ into several molecularly distinct areas, partially overlapping with the morphological compartments. Additionally, several of the mushroom body-specific genes are expressed in the developing cerebral organs. CONCLUSIONS: The dissimilar expression of molecular brain markers between L. ruber and the annelid Platynereis dumerilii indicates that the complex brains present in those two species evolved convergently by independent expansions of non-homologous regions of a simpler brain present in their last common ancestor. Although the same genes are expressed in mushroom bodies and cerebral organs, their spatial expression within organs shows apparent differences between annelids and nemerteans, indicating convergent recruitment of the same genes into patterning of non-homologous organs or hint toward a more complicated evolutionary process, in which conserved and novel cell types contribute to the non-homologous structures. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-01113-1. BioMed Central 2021-08-27 /pmc/articles/PMC8400761/ /pubmed/34452633 http://dx.doi.org/10.1186/s12915-021-01113-1 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Gąsiorowski, Ludwik
Børve, Aina
Cherneva, Irina A.
Orús-Alcalde, Andrea
Hejnol, Andreas
Molecular and morphological analysis of the developing nemertean brain indicates convergent evolution of complex brains in Spiralia
title Molecular and morphological analysis of the developing nemertean brain indicates convergent evolution of complex brains in Spiralia
title_full Molecular and morphological analysis of the developing nemertean brain indicates convergent evolution of complex brains in Spiralia
title_fullStr Molecular and morphological analysis of the developing nemertean brain indicates convergent evolution of complex brains in Spiralia
title_full_unstemmed Molecular and morphological analysis of the developing nemertean brain indicates convergent evolution of complex brains in Spiralia
title_short Molecular and morphological analysis of the developing nemertean brain indicates convergent evolution of complex brains in Spiralia
title_sort molecular and morphological analysis of the developing nemertean brain indicates convergent evolution of complex brains in spiralia
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8400761/
https://www.ncbi.nlm.nih.gov/pubmed/34452633
http://dx.doi.org/10.1186/s12915-021-01113-1
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