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...
Main Authors: | , , |
---|---|
Format: | Article |
Language: | English |
Published: |
eLife Sciences Publications Ltd
2019-06-01
|
Series: | eLife |
Subjects: | |
Online Access: | https://elifesciences.org/articles/44455 |
_version_ | 1811199510566666240 |
---|---|
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. |
first_indexed | 2024-04-12T01:49:21Z |
format | Article |
id | doaj.art-61f85714ccfe443b8534ac222cd48399 |
institution | Directory Open Access Journal |
issn | 2050-084X |
language | English |
last_indexed | 2024-04-12T01:49:21Z |
publishDate | 2019-06-01 |
publisher | eLife Sciences Publications Ltd |
record_format | Article |
series | eLife |
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 |
work_keys_str_mv | AT sophieamontandon elasticinstabilityduringbranchialectodermdevelopmentcausesfoldingofthechlamydosauruserectilefrill AT anamarijafofonjka elasticinstabilityduringbranchialectodermdevelopmentcausesfoldingofthechlamydosauruserectilefrill AT michelcmilinkovitch elasticinstabilityduringbranchialectodermdevelopmentcausesfoldingofthechlamydosauruserectilefrill |