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

ABSTRACT: 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.

SUBMITTER: Montandon SA

PROVIDER: S-EPMC6592688 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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

Montandon Sophie A SA Fofonjka Anamarija A Milinkovitch Michel C MC

eLife 20190625

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 ...[more]

PMID: 31234965

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Project description:Wnt/β-catenin signaling is an ancient pathway in metazoans and controls various developmental processes, in particular the establishment and patterning of the embryonic primary axis. In vertebrates, a graded Wnt activity from posterior to anterior endows cells with positional information in the central nervous system. Recent studies in hemichordates support a conserved role for Wnt/β-catenin in ectoderm antero-posterior patterning at the base of the deuterostomes. Ascidians are marine invertebrates and the closest relatives of vertebrates. By combining gain- and loss-of-function approaches, we have determined the role of Wnt/β-catenin in patterning the three ectoderm derivatives of the ascidian Ciona intestinalis, central nervous system, peripheral nervous system and epidermis. Activating Wnt/β-catenin signaling from gastrulation led to a dramatic transformation of the ectoderm with a loss of anterior identities and a reciprocal anterior extension of posterior identities, consistent with studies in other metazoans. Surprisingly, inhibiting Wnt signaling did not produce a reciprocal anteriorization of the embryo with a loss of more posterior identities like in vertebrates and hemichordate. Epidermis patterning was overall unchanged. Only the identity of two discrete regions of the central nervous system, the anteriormost and the posteriormost regions, were under the control of Wnt. Finally, the caudal peripheral nervous system, while being initially Wnt dependent, formed normally. Our results show that the Ciona embryonic ectoderm responds to Wnt activation in a manner that is compatible with the proposed function for this pathway at the base of the deuterostomes. However, possibly because of its fast and divergent mode of development that includes extensive use of maternal determinants, the overall antero-posterior patterning of the Ciona ectoderm is Wnt independent, and Wnt/β-catenin signaling controls the formation of some sub-domains. Our results thus indicate that there has likely been a drift in the developmental systems controlling ectoderm patterning in the lineage leading to ascidians.

Dataset Information

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

Publications

Elastic instability during branchial ectoderm development causes folding of the <i>Chlamydosaurus</i> erectile frill.

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