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.2019 May 3;10(1):2050.
doi: 10.1038/s41467-019-10032-3.

The pharynx of the stem-chondrichthyan Ptomacanthus and the early evolution of the gnathostome gill skeleton

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The pharynx of the stem-chondrichthyan Ptomacanthus and the early evolution of the gnathostome gill skeleton

Richard P Dearden et al. Nat Commun..

Abstract

The gill apparatus of gnathostomes (jawed vertebrates) is fundamental to feeding and ventilation and a focal point of classic hypotheses on the origin of jaws and paired appendages. The gill skeletons of chondrichthyans (sharks, batoids, chimaeras) have often been assumed to reflect ancestral states. However, only a handful of early chondrichthyan gill skeletons are known and palaeontological work is increasingly challenging other pre-supposed shark-like aspects of ancestral gnathostomes. Here we use computed tomography scanning to image the three-dimensionally preserved branchial apparatus in Ptomacanthus, a 415 million year old stem-chondrichthyan. Ptomacanthus had an osteichthyan-like compact pharynx with a bony operculum helping constrain the origin of an elongate elasmobranch-like pharynx to the chondrichthyan stem-group, rather than it representing an ancestral condition of the crown-group. A mixture of chondrichthyan-like and plesiomorphic pharyngeal patterning in Ptomacanthus challenges the idea that the ancestral gnathostome pharynx conformed to a morphologically complete ancestral type.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1
Ptomacanthus anglicus, specimen NHM P.24919a.a Photograph.b Virtual rendering of the pharyngeal skeleton and dermal shoulder girdle in ventral view, with the moulded surface of the matrix in the background.c Virtual rendering of the pharyngeal skeleton in ventral view, with the moulded surface of the matrix in the background, and the positions of the braincase (as interpreted by Brazeau) and branchiostegals overlain
Fig. 2
Fig. 2
The pharyngeal skeleton ofPtomacanthus anglicus.a Virtual rendering in dorsal view.b Drawing of dorsal branchial skeleton from the anatomical left hand side.c Drawing of ventral branchial skeleton. Colour scheme: red, basihyal/branchial; purple, ceratohyal (light shade)/branchial (dark shade); yellow, epibranchial; orange, pharyngohyal/branchial; green, mandibular arch
Fig. 3
Fig. 3
Postero-anterior extent of branchial skeleton in early gnathostomes. The phylogenetic tree is congruent with the topology described in the results (Supplementary Figs. 4, 5). Changes in position are reconstructed: P indicates a shift of the posterior extent of the branchial skeleton, A indicates a shift of the anterior extent, O indicates the appearance or loss of a bony operculum. Colour scheme: grey, neurocranium; pale yellow, hyomandibular; bright yellow, epibranchial; orange, pharyngobranchial; blue, dermal shoulder girdle. Reconstructions redrawn from refs.,,,,,. The redrawn illustration from figure 8 of Maisey is used with permission from the American Museum of Natural History
Fig. 4
Fig. 4
The phylogenetic distribution of branchial arch morphologies in gnathostomes. The scheme of relationships is based on the strict consensus tree derived from the parsimony analysis described in the methods. Character changes of selected pharyngeal arch characters from our analysis are plotted using an ACCTRAN optimisation. Taxa shown areaCowralepis,bParaplesiobatis,cRaynerius,dGlyptolepis,eAcanthodes (data from refs.,),fPtomacanthus,gGladbachus,hTriodus,iScyliorhinus,jOzarcus,kCallorhinchus,lDebeerius. Colour scheme: as in Fig. 2, with addition of: light turquoise, hypohyal; dark turquoise, hypobranchial; grey, urohyal; pale orange, pharyngohyal. Silhouettes from refs.,, and Phylopic. Phylopic images ofBothriolepis andCallorhinchus milii were submitted by Ghedoghedo and Tony Ayling (vectorised by Milton Tan) respectively. Both were distributed under a Creative Commons Attribution-ShareAlike 3.0 Unported license (https://creativecommons.org/licenses/by-sa/3.0/). The redrawn illustration from figure 7 of Heidtke et al. is used with permission from the Landesamt für Geologie und Bergbau Rheinland-Pfalz
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