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.
Highlights
Lizards can exhibit moveable skin folds at various locations of their body, such as the wings of the flying dragon (Draco volans), the oral display frill of the ‘secret toadhead agama’ (Phrynocephalus mystaceus), and the dewlap of many anole lizard species (Anolis spp.)
The emblematic erectile ruff of the frilled dragon is a large and sagitally-symmetric piece of skin attached to the neck and the head
The frill pleats into three convex ridges and two concave folds while the animal can spread this structure by the coordinated movements of hyoid-derived hypertrophied ceratobranchial I bones (CBI) bone and the so-called ‘Grey’s cartilage’ that we identify not to be bona fide cartilage
Summary
Lizards can exhibit moveable skin folds at various locations of their body, such as the wings of the flying dragon (Draco volans), the oral display frill of the ‘secret toadhead agama’ (Phrynocephalus mystaceus), and the dewlap of many anole lizard species (Anolis spp.). Erection of the frill is caused by the coordinated movements of the CBI bones and Grey’s cartilages and requires the opening of the mouth Their primary function in tetrapods is associated with deglutition, the bones of the hyoid apparatus are involved in a variety of specialised morphologies and functions such as improved lung ventilation through gular pumping in monitor lizards (Bels et al, 1995; Owerkowicz et al, 1999), extension of the throat in bearded dragons (Throckmorton et al, 1985) and of the dewlap in Anolis lizards (Bels, 1990; Font and Rome, 1990), tongue projection in chameleons (Herrel et al, 2001), as well as tongue extension and shock absorption in woodpeckers (Yoon and Park, 2011). The hyoid apparatus develops from the pre-cartilage
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