Cellular development and evolution of the mammalian cerebellum

Mari Sepp (), Kevin Leiss (), Florent Murat, Konstantin Okonechnikov, Piyush Joshi, Evgeny Leushkin, Lisa Spänig, Noe Mbengue, Céline Schneider, Julia Schmidt, Nils Trost, Maria Schauer, Philipp Khaitovich, Steven Lisgo, Miklós Palkovits, Peter Giere, Lena M. Kutscher, Simon Anders, Margarida Cardoso-Moreira, Ioannis Sarropoulos (), Stefan M. Pfister () and Henrik Kaessmann ()
Additional contact information
Mari Sepp: Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance
Kevin Leiss: Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance
Florent Murat: Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance
Konstantin Okonechnikov: Hopp-Children’s Cancer Center Heidelberg (KiTZ)
Piyush Joshi: Hopp-Children’s Cancer Center Heidelberg (KiTZ)
Evgeny Leushkin: Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance
Lisa Spänig: Hopp-Children’s Cancer Center Heidelberg (KiTZ)
Noe Mbengue: Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance
Céline Schneider: Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance
Julia Schmidt: Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance
Nils Trost: Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance
Maria Schauer: Leibniz Institute for Evolution and Biodiversity Science
Philipp Khaitovich: The First Affiliated Hospital of Chongqing Medical University
Steven Lisgo: Newcastle University
Miklós Palkovits: Semmelweis University
Peter Giere: Leibniz Institute for Evolution and Biodiversity Science
Lena M. Kutscher: Hopp-Children’s Cancer Center Heidelberg (KiTZ)
Simon Anders: Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance
Margarida Cardoso-Moreira: Francis Crick Institute
Ioannis Sarropoulos: Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance
Stefan M. Pfister: Hopp-Children’s Cancer Center Heidelberg (KiTZ)
Henrik Kaessmann: Center for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance

Nature, 2024, vol. 625, issue 7996, 788-796

Abstract: Abstract The expansion of the neocortex, a hallmark of mammalian evolution1,2, was accompanied by an increase in cerebellar neuron numbers3. However, little is known about the evolution of the cellular programmes underlying the development of the cerebellum in mammals. In this study we generated single-nucleus RNA-sequencing data for around 400,000 cells to trace the development of the cerebellum from early neurogenesis to adulthood in human, mouse and the marsupial opossum. We established a consensus classification of the cellular diversity in the developing mammalian cerebellum and validated it by spatial mapping in the fetal human cerebellum. Our cross-species analyses revealed largely conserved developmental dynamics of cell-type generation, except for Purkinje cells, for which we observed an expansion of early-born subtypes in the human lineage. Global transcriptome profiles, conserved cell-state markers and gene-expression trajectories across neuronal differentiation show that cerebellar cell-type-defining programmes have been overall preserved for at least 160 million years. However, we also identified many orthologous genes that gained or lost expression in cerebellar neural cell types in one of the species or evolved new expression trajectories during neuronal differentiation, indicating widespread gene repurposing at the cell-type level. In sum, our study unveils shared and lineage-specific gene-expression programmes governing the development of cerebellar cells and expands our understanding of mammalian brain evolution.

Date: 2024
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DOI: 10.1038/s41586-023-06884-x

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