1. Developmental Biology
  2. Evolutionary Biology
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Developmental variability channels mouse molar evolution

  1. Luke Hayden
  2. Katerina Lochovska
  3. Marie Sémon
  4. Sabrina Renaud
  5. Marie-Laure Delignette-Muller
  6. Maurine Vilcot
  7. Renata Peterkova
  8. Maria Hovorakova  Is a corresponding author
  9. Sophie Pantalacci  Is a corresponding author
  1. ENS de Lyon, France
  2. Charles University, Czech Republic
  3. Université Lyon 1, CNRS, VetAgro Sup, UMR 5558, France
  4. The Czech Academy of Sciences, Czech Republic
Research Article
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Cite this article as: eLife 2020;9:e50103 doi: 10.7554/eLife.50103

Abstract

Do developmental systems preferentially produce certain types of variation that orient phenotypic evolution along preferred directions? At different scales, from the intra-population to the interspecific, the murine first upper molar shows repeated anterior elongation. Using a novel quantitative approach to compare the development of two mouse strains with short or long molars, we identified temporal, spatial and functional differences in tooth signaling center activity, that arise from differential tuning of the activation-inhibition mechanisms underlying tooth patterning. By tracing their fate, we could explain why only the upper first molar reacts via elongation of its anterior part. Despite a lack of genetic variation, individuals of the elongated strain varied in tooth length and the temporal dynamics of their signaling centers, highlighting the intrinsic instability of the upper molar developmental system. Collectively, these results reveal the variational properties of murine molar development that drive morphological evolution along a line of least resistance.

Data availability

- Sequencing data have been deposited in GEO under accession codes GSE135432.- All data generated or analyzed during this study are included in the manuscript and supporting files. Sources and codes are available on githubhttps://github.com/msemon/cdpchttps://github.com/luke-hayden/dvpap/devstatehttps://github.com/luke-hayden/dvpap/devmorph

The following data sets were generated

Article and author information

Author details

  1. Luke Hayden

    Laboratoire de Biologie et Modélisation de la Cellule, ENS de Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.

  2. Katerina Lochovska

    1st Department of Medicine, First Faculty of Medicine, Charles University, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4142-4531

  3. Marie Sémon

    Laboratoire de Biologie et Modélisation de la Cellule, ENS de Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3479-7524

  4. Sabrina Renaud

    Laboratoire de Biométrie et Biologie Evolutive, Université Lyon 1, CNRS, VetAgro Sup, UMR 5558, Villeurbanne, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8730-3113

  5. Marie-Laure Delignette-Muller

    Laboratoire de Biométrie et Biologie Évolutive, Université Lyon 1, CNRS, VetAgro Sup, UMR 5558, Villeurbanne, France
    Competing interests
    The authors declare that no competing interests exist.

  6. Maurine Vilcot

    Laboratoire de Biologie et Modélisation de la Cellule, ENS de Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.

  7. Renata Peterkova

    Department of Histology and Embryology, Third Faculty of Medicine, Charles University, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.

  8. Maria Hovorakova

    Department of Developmental Biology, Institute of Experimental Medicine, The Czech Academy of Sciences, Prague, Czech Republic
    For correspondence
    maria.hovorakova@iem.cas.cz
    Competing interests
    The authors declare that no competing interests exist.

  9. Sophie Pantalacci

    Laboratoire de Biologie et Modélisation de la Cellule, ENS de Lyon, Lyon, France
    For correspondence
    sophie.pantalacci@ens-lyon.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0771-8985

Funding

Agence Nationale de la Recherche (ANR-11-BSV7-008)

  • Sophie Pantalacci

Agence Nationale de la Recherche (ANR-11-BSV7-008)

  • Sabrina Renaud

Fondation pour la Recherche Médicale (SPF20140129165)

  • Luke Hayden

Grant Agency of the Czech Republic (14-37368G)

  • Renata Peterkova

Czech Ministry of Education, Youth and Sports (8J19FR032)

  • Maria Hovorakova

Grant Agency of the Czech Republic (18-04859S)

  • Maria Hovorakova

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was performed in a strict accordance with European guidelines (2010/63/UE). It was approved by the CECCAPP Animal Experimentation Ethics Committee (Lyon, France; reference ENS_2014_022), by the Professional committee for guarantee of good life-conditions of experimental animals at the Institute of Experimental Medicine IEM CAS, Prague, Czech Republic) and by the Expert Committee at the Czech Academy of Sciences (permit number: 027/ 2011).

Reviewing Editor

  1. Karen E Sears, University of California, Los Angeles, United States

Publication history

  1. Received: July 11, 2019
  2. Accepted: February 2, 2020
  3. Accepted Manuscript published: February 12, 2020 (version 1)
  4. Version of Record published: April 24, 2020 (version 2)

Copyright

© 2020, Hayden et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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