Elastic instability during branchial ectoderm development causes folding of the Chlamydosaurus erectile frill

We study the morphogenesis and evolutionary origin of the spectacular erectile ruff of the frilled dragon (Chlamydosaurus kingii). Our comparative developmental analyses of multiple species suggest that the ancestor of Episquamata reptiles developed a neck fold from the hyoid branchial arch by preve...

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Main Authors: Sophie A Montandon, Anamarija Fofonjka, Michel C Milinkovitch
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-06-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/44455
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author Sophie A Montandon
Anamarija Fofonjka
Michel C Milinkovitch
author_facet Sophie A Montandon
Anamarija Fofonjka
Michel C Milinkovitch
author_sort Sophie A Montandon
collection DOAJ
description We study the morphogenesis and evolutionary origin of the spectacular erectile ruff of the frilled dragon (Chlamydosaurus kingii). Our comparative developmental analyses of multiple species suggest that the ancestor of Episquamata reptiles developed a neck fold from the hyoid branchial arch by preventing it to fully fuse with posterior arches. We also show that the Chlamydosaurus embryonic neck fold dramatically enlarges and its anterior surface wrinkles, establishing three convex ridges on each lobe of the frill. We suggest that this robust folding pattern is not due to localised increased growth at the positions of the ridges, but emerges from an elastic instability during homogeneous growth of the frill skin frustrated by its attachment to adjacent tissues. Our physical analog experiments and 3D computational simulations, using realistic embryonic tissue growth, thickness and stiffness values, recapitulate the transition from two to three ridges observed during embryonic development of the dragon’s frill.
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spelling doaj.art-61f85714ccfe443b8534ac222cd483992022-12-22T03:52:58ZengeLife Sciences Publications LtdeLife2050-084X2019-06-01810.7554/eLife.44455Elastic instability during branchial ectoderm development causes folding of the Chlamydosaurus erectile frillSophie A Montandon0Anamarija Fofonjka1Michel C Milinkovitch2https://orcid.org/0000-0002-2553-0724Laboratory of Artificial & Natural Evolution (LANE), Department of Genetics & Evolution, University of Geneva, Geneva, SwitzerlandLaboratory of Artificial & Natural Evolution (LANE), Department of Genetics & Evolution, University of Geneva, Geneva, Switzerland; SIB Swiss Institute of Bioinformatics, Geneva, SwitzerlandLaboratory of Artificial & Natural Evolution (LANE), Department of Genetics & Evolution, University of Geneva, Geneva, Switzerland; SIB Swiss Institute of Bioinformatics, Geneva, SwitzerlandWe study the morphogenesis and evolutionary origin of the spectacular erectile ruff of the frilled dragon (Chlamydosaurus kingii). Our comparative developmental analyses of multiple species suggest that the ancestor of Episquamata reptiles developed a neck fold from the hyoid branchial arch by preventing it to fully fuse with posterior arches. We also show that the Chlamydosaurus embryonic neck fold dramatically enlarges and its anterior surface wrinkles, establishing three convex ridges on each lobe of the frill. We suggest that this robust folding pattern is not due to localised increased growth at the positions of the ridges, but emerges from an elastic instability during homogeneous growth of the frill skin frustrated by its attachment to adjacent tissues. Our physical analog experiments and 3D computational simulations, using realistic embryonic tissue growth, thickness and stiffness values, recapitulate the transition from two to three ridges observed during embryonic development of the dragon’s frill.https://elifesciences.org/articles/44455Chamydosaurusfrilled dragonelastic instabilitypatterningphysics of living systemsevolutionary developmental biology
spellingShingle Sophie A Montandon
Anamarija Fofonjka
Michel C Milinkovitch
Elastic instability during branchial ectoderm development causes folding of the Chlamydosaurus erectile frill
eLife
Chamydosaurus
frilled dragon
elastic instability
patterning
physics of living systems
evolutionary developmental biology
title Elastic instability during branchial ectoderm development causes folding of the Chlamydosaurus erectile frill
title_full Elastic instability during branchial ectoderm development causes folding of the Chlamydosaurus erectile frill
title_fullStr Elastic instability during branchial ectoderm development causes folding of the Chlamydosaurus erectile frill
title_full_unstemmed Elastic instability during branchial ectoderm development causes folding of the Chlamydosaurus erectile frill
title_short Elastic instability during branchial ectoderm development causes folding of the Chlamydosaurus erectile frill
title_sort elastic instability during branchial ectoderm development causes folding of the chlamydosaurus erectile frill
topic Chamydosaurus
frilled dragon
elastic instability
patterning
physics of living systems
evolutionary developmental biology
url https://elifesciences.org/articles/44455
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AT anamarijafofonjka elasticinstabilityduringbranchialectodermdevelopmentcausesfoldingofthechlamydosauruserectilefrill
AT michelcmilinkovitch elasticinstabilityduringbranchialectodermdevelopmentcausesfoldingofthechlamydosauruserectilefrill