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A shark-inspired general model of tooth morphogenesis unveils developmental asymmetries in phenotype transitions

Developmental complexity stemming from the dynamic interplay between genetic and biomechanic factors canalizes the ways genotypes and phenotypes can change in evolution. As a paradigmatic system, we explore how changes in developmental factors generate typical tooth shape transitions. Since tooth de...

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Autores principales: Zimm, Roland, Berio, Fidji, Debiais-Thibaud, Mélanie, Goudemand, Nicolas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10104537/
https://www.ncbi.nlm.nih.gov/pubmed/37027430
http://dx.doi.org/10.1073/pnas.2216959120
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author Zimm, Roland
Berio, Fidji
Debiais-Thibaud, Mélanie
Goudemand, Nicolas
author_facet Zimm, Roland
Berio, Fidji
Debiais-Thibaud, Mélanie
Goudemand, Nicolas
author_sort Zimm, Roland
collection PubMed
description Developmental complexity stemming from the dynamic interplay between genetic and biomechanic factors canalizes the ways genotypes and phenotypes can change in evolution. As a paradigmatic system, we explore how changes in developmental factors generate typical tooth shape transitions. Since tooth development has mainly been researched in mammals, we contribute to a more general understanding by studying the development of tooth diversity in sharks. To this end, we build a general, but realistic, mathematical model of odontogenesis. We show that it reproduces key shark-specific features of tooth development as well as real tooth shape variation in small-spotted catsharks Scyliorhinus canicula. We validate our model by comparison with experiments in vivo. Strikingly, we observe that developmental transitions between tooth shapes tend to be highly degenerate, even for complex phenotypes. We also discover that the sets of developmental parameters involved in tooth shape transitions tend to depend asymmetrically on the direction of that transition. Together, our findings provide a valuable base for furthering our understanding of how developmental changes can lead to both adaptive phenotypic change and trait convergence in complex, phenotypically highly diverse, structures.
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spelling pubmed-101045372023-10-07 A shark-inspired general model of tooth morphogenesis unveils developmental asymmetries in phenotype transitions Zimm, Roland Berio, Fidji Debiais-Thibaud, Mélanie Goudemand, Nicolas Proc Natl Acad Sci U S A Biological Sciences Developmental complexity stemming from the dynamic interplay between genetic and biomechanic factors canalizes the ways genotypes and phenotypes can change in evolution. As a paradigmatic system, we explore how changes in developmental factors generate typical tooth shape transitions. Since tooth development has mainly been researched in mammals, we contribute to a more general understanding by studying the development of tooth diversity in sharks. To this end, we build a general, but realistic, mathematical model of odontogenesis. We show that it reproduces key shark-specific features of tooth development as well as real tooth shape variation in small-spotted catsharks Scyliorhinus canicula. We validate our model by comparison with experiments in vivo. Strikingly, we observe that developmental transitions between tooth shapes tend to be highly degenerate, even for complex phenotypes. We also discover that the sets of developmental parameters involved in tooth shape transitions tend to depend asymmetrically on the direction of that transition. Together, our findings provide a valuable base for furthering our understanding of how developmental changes can lead to both adaptive phenotypic change and trait convergence in complex, phenotypically highly diverse, structures. National Academy of Sciences 2023-04-07 2023-04-11 /pmc/articles/PMC10104537/ /pubmed/37027430 http://dx.doi.org/10.1073/pnas.2216959120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Zimm, Roland
Berio, Fidji
Debiais-Thibaud, Mélanie
Goudemand, Nicolas
A shark-inspired general model of tooth morphogenesis unveils developmental asymmetries in phenotype transitions
title A shark-inspired general model of tooth morphogenesis unveils developmental asymmetries in phenotype transitions
title_full A shark-inspired general model of tooth morphogenesis unveils developmental asymmetries in phenotype transitions
title_fullStr A shark-inspired general model of tooth morphogenesis unveils developmental asymmetries in phenotype transitions
title_full_unstemmed A shark-inspired general model of tooth morphogenesis unveils developmental asymmetries in phenotype transitions
title_short A shark-inspired general model of tooth morphogenesis unveils developmental asymmetries in phenotype transitions
title_sort shark-inspired general model of tooth morphogenesis unveils developmental asymmetries in phenotype transitions
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10104537/
https://www.ncbi.nlm.nih.gov/pubmed/37027430
http://dx.doi.org/10.1073/pnas.2216959120
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