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

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.

Metrics

  • 1,416
    Page views
  • 236
    Downloads
  • 9
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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
  9. Sophie Pantalacci
(2020)
Developmental variability channels mouse molar evolution
eLife 9:e50103.
https://doi.org/10.7554/eLife.50103

Further reading

    1. Cell Biology
    2. Developmental Biology
    Anna Keppner et al.
    Research Article Updated

    Spermatogenesis is a highly specialized differentiation process driven by a dynamic gene expression program and ending with the production of mature spermatozoa. Whereas hundreds of genes are known to be essential for male germline proliferation and differentiation, the contribution of several genes remains uncharacterized. The predominant expression of the latest globin family member, androglobin (Adgb), in mammalian testis tissue prompted us to assess its physiological function in spermatogenesis. Adgb knockout mice display male infertility, reduced testis weight, impaired maturation of elongating spermatids, abnormal sperm shape, and ultrastructural defects in microtubule and mitochondrial organization. Epididymal sperm from Adgb knockout animals display multiple flagellar malformations including coiled, bifid or shortened flagella, and erratic acrosomal development. Following immunoprecipitation and mass spectrometry, we could identify septin 10 (Sept10) as interactor of Adgb. The Sept10-Adgb interaction was confirmed both in vivo using testis lysates and in vitro by reciprocal co-immunoprecipitation experiments. Furthermore, the absence of Adgb leads to mislocalization of Sept10 in sperm, indicating defective manchette and sperm annulus formation. Finally, in vitro data suggest that Adgb contributes to Sept10 proteolysis in a calmodulin-dependent manner. Collectively, our results provide evidence that Adgb is essential for murine spermatogenesis and further suggest that Adgb is required for sperm head shaping via the manchette and proper flagellum formation.

    1. Developmental Biology
    2. Evolutionary Biology
    Alexandre P Thiery et al.
    Research Article Updated

    Development of tooth shape is regulated by the enamel knot signalling centre, at least in mammals. Fgf signalling regulates differential proliferation between the enamel knot and adjacent dental epithelia during tooth development, leading to formation of the dental cusp. The presence of an enamel knot in non-mammalian vertebrates is debated given differences in signalling. Here, we show the conservation and restriction of fgf3, fgf10, and shh to the sites of future dental cusps in the shark (Scyliorhinus canicula), whilst also highlighting striking differences between the shark and mouse. We reveal shifts in tooth size, shape, and cusp number following small molecule perturbations of canonical Wnt signalling. Resulting tooth phenotypes mirror observed effects in mammals, where canonical Wnt has been implicated as an upstream regulator of enamel knot signalling. In silico modelling of shark dental morphogenesis demonstrates how subtle changes in activatory and inhibitory signals can alter tooth shape, resembling developmental phenotypes and cusp shapes observed following experimental Wnt perturbation. Our results support the functional conservation of an enamel knot-like signalling centre throughout vertebrates and suggest that varied tooth types from sharks to mammals follow a similar developmental bauplan. Lineage-specific differences in signalling are not sufficient in refuting homology of this signalling centre, which is likely older than teeth themselves.