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Developmental system drift in one tooth facilitates the adaptation of the other

View ORCID ProfileMarie Sémon, Laurent Guéguen, Klara Steklikova, Marion Mouginot, Manon Peltier, Philippe Veber, View ORCID ProfileSophie Pantalacci
doi: https://doi.org/10.1101/2020.04.22.043422
Marie Sémon
1Laboratoire de Biologie et Modelisation de la Cellule, Ecole Normale Superieure de Lyon, CNRS, UMR 5239, Inserm, U1293, Universite Claude Bernard Lyon 1, 46 allee d’Italie F-69364 Lyon, France
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  • For correspondence: sophie.pantalacci@ens-lyon.fr marie.semon@ens-lyon.fr
Laurent Guéguen
2Univ Lyon, Université Claude Bernard Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive, F-69100, Villeurbanne, France
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Klara Steklikova
3Institute of Histology and Embryology, First Faculty of Medicine, Charles University, Prague, Czech Republic
4Department of Cell Biology, Faculty of Science, Charles University, Prague, Czech Republic
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Marion Mouginot
1Laboratoire de Biologie et Modelisation de la Cellule, Ecole Normale Superieure de Lyon, CNRS, UMR 5239, Inserm, U1293, Universite Claude Bernard Lyon 1, 46 allee d’Italie F-69364 Lyon, France
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Manon Peltier
1Laboratoire de Biologie et Modelisation de la Cellule, Ecole Normale Superieure de Lyon, CNRS, UMR 5239, Inserm, U1293, Universite Claude Bernard Lyon 1, 46 allee d’Italie F-69364 Lyon, France
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Philippe Veber
2Univ Lyon, Université Claude Bernard Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive, F-69100, Villeurbanne, France
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Sophie Pantalacci
1Laboratoire de Biologie et Modelisation de la Cellule, Ecole Normale Superieure de Lyon, CNRS, UMR 5239, Inserm, U1293, Universite Claude Bernard Lyon 1, 46 allee d’Italie F-69364 Lyon, France
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  • ORCID record for Sophie Pantalacci
  • For correspondence: sophie.pantalacci@ens-lyon.fr marie.semon@ens-lyon.fr
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SUMMARY

Serial organs, such as limbs or teeth, develop with the same sets of genes and regulatory sequences. Correlated evolution is expected by default, but decoupled evolution is often achieved, as in mouse with a morphological innovation in the upper, but not the lower molar. We studied developmental evolution of hamster and mouse molars with transcriptome data. We reveal a combination of three morphogenetic changes likely causing the new morphology of the mouse upper molar. Surprisingly, most of these changes are common with the lower molar and lower molar gene expression diverged as much as, and coevolved with, the upper molar.

Hence, adaptation of the upper molar has involved changes in pleiotropic genes that also modified lower molar development but preserved its final phenotype. From the lower molar point of view, it is a case of Developmental systems drift (DSD). We think that DSD accommodates pleiotropy, explaining why in teeth and more generally in the body, the evolution of developmental gene expression is fast and correlates between organs.

HIGHLIGHTS

  • - The evolutionary innovation of mouse upper molar involves several morphogenetic changes

  • - Most of the associated gene expression changes are shared with the mouse lower molar

  • - Lower molar’s phenotype is conserved, thus its developmental gene expression drifted

  • - Adaptation with pleiotropic genes drove developmental system drift in the other tooth

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
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 4.0 International license.
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Posted April 08, 2022.
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Developmental system drift in one tooth facilitates the adaptation of the other
Marie Sémon, Laurent Guéguen, Klara Steklikova, Marion Mouginot, Manon Peltier, Philippe Veber, Sophie Pantalacci
bioRxiv 2020.04.22.043422; doi: https://doi.org/10.1101/2020.04.22.043422
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Developmental system drift in one tooth facilitates the adaptation of the other
Marie Sémon, Laurent Guéguen, Klara Steklikova, Marion Mouginot, Manon Peltier, Philippe Veber, Sophie Pantalacci
bioRxiv 2020.04.22.043422; doi: https://doi.org/10.1101/2020.04.22.043422

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