Developmental variability channels mouse molar evolution
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
Article and author information
Author details
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.
Reviewing Editor
- Karen E Sears, University of California, Los Angeles, United States
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).
Version history
- Received: July 11, 2019
- Accepted: February 2, 2020
- Accepted Manuscript published: February 12, 2020 (version 1)
- 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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