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Reconstructing the ancestral vertebrate brain using a lamprey neural cell type atlas

View ORCID ProfileFrancesco Lamanna, Francisca Hervas-Sotomayor, A. Phillip Oel, David Jandzik, Daniel Sobrido-Cameán, Megan L. Martik, Stephen A. Green, Thoomke Brüning, Katharina Mößinger, Julia Schmidt, Celine Schneider, Mari Sepp, Florent Murat, Jeramiah J. Smith, View ORCID ProfileMarianne E. Bronner, María Celina Rodicio, Antón Barreiro-Iglesias, Daniel M. Medeiros, View ORCID ProfileDetlev Arendt, Henrik Kaessmann
doi: https://doi.org/10.1101/2022.02.28.482278
Francesco Lamanna
1Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance, D-69120 Heidelberg, Germany
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  • ORCID record for Francesco Lamanna
  • For correspondence: f.lamanna@zmbh.uni-heidelberg.de f.hervas@zmbh.uni-heidelberg.de h.kaessmann@zmbh.uni-heidelberg.de
Francisca Hervas-Sotomayor
1Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance, D-69120 Heidelberg, Germany
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  • For correspondence: f.lamanna@zmbh.uni-heidelberg.de f.hervas@zmbh.uni-heidelberg.de h.kaessmann@zmbh.uni-heidelberg.de
A. Phillip Oel
1Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance, D-69120 Heidelberg, Germany
2Developmental Biology Unit, European Molecular Biology Laboratory, D-69012 Heidelberg, Germany
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David Jandzik
3Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado 80309, USA
4Department of Zoology, Comenius University, Bratislava, Slovakia
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Daniel Sobrido-Cameán
5Department of Functional Biology, CIBUS, Faculty of Biology, Universidade de Santiago de Compostela, 15782 Santiago de Compostela, Spain
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Megan L. Martik
6Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA
7Department of Molecular and Cell Biology, University of California, Berkeley, CA, USA
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Stephen A. Green
6Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA
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Thoomke Brüning
1Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance, D-69120 Heidelberg, Germany
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Katharina Mößinger
1Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance, D-69120 Heidelberg, Germany
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Julia Schmidt
1Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance, D-69120 Heidelberg, Germany
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Celine Schneider
1Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance, D-69120 Heidelberg, Germany
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Mari Sepp
1Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance, D-69120 Heidelberg, Germany
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Florent Murat
1Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance, D-69120 Heidelberg, Germany
8INRAE, LPGP, 35000 Rennes, France
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Jeramiah J. Smith
9Department of Biology, University of Kentucky, Lexington, Kentucky
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Marianne E. Bronner
6Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA
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  • ORCID record for Marianne E. Bronner
María Celina Rodicio
5Department of Functional Biology, CIBUS, Faculty of Biology, Universidade de Santiago de Compostela, 15782 Santiago de Compostela, Spain
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Antón Barreiro-Iglesias
5Department of Functional Biology, CIBUS, Faculty of Biology, Universidade de Santiago de Compostela, 15782 Santiago de Compostela, Spain
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Daniel M. Medeiros
3Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado 80309, USA
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Detlev Arendt
2Developmental Biology Unit, European Molecular Biology Laboratory, D-69012 Heidelberg, Germany
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  • ORCID record for Detlev Arendt
Henrik Kaessmann
1Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance, D-69120 Heidelberg, Germany
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  • For correspondence: f.lamanna@zmbh.uni-heidelberg.de f.hervas@zmbh.uni-heidelberg.de h.kaessmann@zmbh.uni-heidelberg.de
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Abstract

The vertebrate brain emerged more than ∼500 million years ago in common evolutionary ancestors. To systematically trace its cellular and molecular origins, we established a spatially resolved cell type atlas of the entire brain of the sea lamprey – a jawless species whose phylogenetic position affords the reconstruction of ancestral vertebrate traits – based on extensive single-cell RNA-seq and in situ sequencing data. Comparisons of this atlas to neural data from the mouse and other jawed vertebrates unveiled various shared features that enabled the reconstruction of the core cell type composition, tissue structures, and gene expression programs of the ancestral brain. However, our analyses also revealed key tissues and cell types that arose later in evolution. For example, the ancestral vertebrate brain was likely devoid of cerebellar cell types and oligodendrocytes (myelinating cells); our data suggest that the latter emerged from astrocyte-like evolutionary precursors on the jawed vertebrate lineage. Our work illuminates the cellular and molecular architecture of the ancestral vertebrate brain and provides a foundation for exploring its diversification during evolution.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://lampreybrain.kaessmannlab.org/

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted March 01, 2022.
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Reconstructing the ancestral vertebrate brain using a lamprey neural cell type atlas
Francesco Lamanna, Francisca Hervas-Sotomayor, A. Phillip Oel, David Jandzik, Daniel Sobrido-Cameán, Megan L. Martik, Stephen A. Green, Thoomke Brüning, Katharina Mößinger, Julia Schmidt, Celine Schneider, Mari Sepp, Florent Murat, Jeramiah J. Smith, Marianne E. Bronner, María Celina Rodicio, Antón Barreiro-Iglesias, Daniel M. Medeiros, Detlev Arendt, Henrik Kaessmann
bioRxiv 2022.02.28.482278; doi: https://doi.org/10.1101/2022.02.28.482278
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Reconstructing the ancestral vertebrate brain using a lamprey neural cell type atlas
Francesco Lamanna, Francisca Hervas-Sotomayor, A. Phillip Oel, David Jandzik, Daniel Sobrido-Cameán, Megan L. Martik, Stephen A. Green, Thoomke Brüning, Katharina Mößinger, Julia Schmidt, Celine Schneider, Mari Sepp, Florent Murat, Jeramiah J. Smith, Marianne E. Bronner, María Celina Rodicio, Antón Barreiro-Iglesias, Daniel M. Medeiros, Detlev Arendt, Henrik Kaessmann
bioRxiv 2022.02.28.482278; doi: https://doi.org/10.1101/2022.02.28.482278

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