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A Palaeozoic shark with osteichthyan-like branchial arches

Nature volume 509, pages 608–611 (2014)Cite this article

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Abstract

The evolution of serially arranged, jointed endoskeletal supports internal to the gills—the visceral branchial arches—represents one of the key events in early jawed vertebrate (gnathostome) history, because it provided the morphological basis for the subsequent evolution of jaws1,2,3,4,5. However, until now little was known about visceral arches in early gnathostomes6,7,8,9,10,11,12,13,14,15,16,17, and theories about gill arch evolution were driven by information gleaned mostly from both modern cartilaginous (chondrichthyan) and bony (osteichthyan) fishes. New fossil discoveries can profoundly affect our understanding of evolutionary history, by revealing hitherto unseen combinations of primitive and derived characters18,19. Here we describe a 325 million year (Myr)-old Palaeozoic shark-like fossil that represents, to our knowledge, the earliest identified chondrichthyan in which the complete gill skeleton is three-dimensionally preserved in its natural position. Its visceral arch arrangement is remarkably osteichthyan-like, suggesting that this may represent the common ancestral condition for crown gnathostomes. Our findings thus reinterpret the polarity of some arch features of the crown jawed vertebrates and invert the classic hypothesis, in which modern sharks retain the ancestral condition3,20. This study underscores the importance of early chondrichthyans in resolving the evolutionary history of jawed vertebrates.

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Figure 1: Three-dimensional reconstructions of Ozarcus mapesae AMNH FF20544.
Figure 2: Reconstructions of the branchial skeleton of O. mapesae.
Figure 3: Evolution of the branchial skeleton in the crown gnathostomes, mapped onto a tree compiled from the most recent phylogenetic analyses19,23,28.

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Acknowledgements

We thank staff at the ID19 beamline at the ESRF for assistance, and F. Ippolito (AMNH) for photographs of the specimens. The main work was supported by the H. R. & E. Axelrod Research Chair in paleoichthyology at the AMNH.

Author information

Authors and Affiliations

  1. Department of Vertebrate Paleontology, American Museum of Natural History, Central Park West at 79th Street, New York, New York 10024, USA,

    Alan Pradel & John G. Maisey

  2. European Synchrotron Radiation Facility, BP 220, 6 rue Jules Horowitz, 38043 Grenoble Cedex, France,

    Paul Tafforeau

  3. Department of Geological Sciences, Ohio University, Athens, 45701, Ohio, USA

    Royal H. Mapes

  4. School of Biological Sciences, Washington State University, Pullman, 99164-4236, Washington, USA

    Jon Mallatt

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  1. Alan Pradel
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Contributions

J.G.M. and A.P. conceived the project. A.P. performed computerized microtomography restorations. A.P., J.G.M. and J.M. interpreted the results and prepared the manuscript. P.T. performed synchrotron computerized microtomography on the material. R.H.M. did the fieldwork.

Corresponding authors

Correspondence to Alan Pradel or John G. Maisey.

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Competing interests

The authors declare no competing financial interests.

Additional information

Data have been deposited in ZooBank under the following LSIDs: urn:lsid:zoobank.org:pub:D80955F3-7C21-457C-BA68-9C70F466E913 (article); urn:lsid:zoobank.org:act:F7EDD4EB-6700-4583-8569-9BAC89B3A945 (genus); and urn:lsid:zoobank.org:act:6ACCB5D2-E0D7-4BFD-85D6-9C8250515614 (species).

Extended data figures and tables

Extended Data Figure 1 Photographs of O. mapesae AMNH FF 20544 (holotype).

a, Right lateral view. b, Left lateral view. Scale bar, 10 mm.

Extended Data Figure 2 The diagnostic features of O. mapesae.

a, b, Part of right palatoquadrate in Ozarcus (a) and Akmonistion14 (b) showing smaller size of teeth (t) relative to the dental bullae (db) in Ozarcus. Anterior to left. Not to scale. c, One tooth family (top) composed of tiny cladodont, pentacuspid and symmetrical teeth in lingual (left) and labial (right) views. d, e, f, g, The ventral (d) and lateral (e) surfaces of the palatoquadrate (right palatoquadrate shown here) and the dorsal (f) and medial (g) surface of the Meckel’s cartilage (left Meckel’s cartilage shown here) show ten concavities that each housed a tooth family (tfc). The quadrate part of the palatoquadrate (q) lacks a continuous posterior margin. h, The neurocranium (top, right lateral view; bottom, ventral view) possesses a laterally extended antorbital process (ap) that overlies a suborbital process (subp) which displays a series of four ridges and grooves for articulation with the palatoquadrate.

Extended Data Figure 3 Three-dimensional reconstructions of O. mapesae showing the relationship of the hyoid arch with the surrounding cartilages.

a, Braincase, right mandibular and hyoid arches in lateral right view. b, Braincase and right hyoid arch in lateral right view. c, Braincase and right hyoid arch in oblique ventral view. d, Dorsal (epi-, supra- and infra-) branchial cartilages of the right hyoid and branchial arches in oblique dorsal view. Colour coding of the skeletal elements: yellow, epi-; blue, cerato-; green, hypo-; orange, infrapharyngo-; turquoise, suprapharyngo-; peachy pink, braincase. The colours of the mandibular elements are lightened and those of the hyoid are darkened. Asterisk indicates the space between the mandibular and hyoid arches.

Extended Data Figure 4 The aphetohyoidean hypothesis and jaw evolution.

a, c, d, The stage shown in a leads to c and d, both of which have a jaw-supporting hyoid. b, Ozarcus may fit just after a, because of its possible aphetohyoidean aspects. However, it is impossible to know whether Ozarcus had a respiratory gill pore between its mandibular and hyoid arches (indicated by a question mark). Colours are as in Fig. 1, plus: light pink, gill pouches; dark pink, otic capsule of braincase; purple, interhyal. gp, gill pore; gp1, first (mandibulohyoid) gill pore; ma, mandibular arch; mh, mandibulohyoid (first) gill pouch; oc, otic capsule; sp., spiracle; spp., spiracular pouch. Not to scale.

Supplementary information

Supplementary Information

This file contains Supplementary Text 1-6, and additional references. (PDF 174 kb)

Ozarcus mapesae AMNH FF20544 rotating from anterior to posterior and dorsal to ventral views

Three-dimensional virtual reconstruction made from propagation phase-contrast X-ray synchrotron microtomography images by means of MIMICS (Materialise, Inc.). Color coding: grey, concretion; yellow, epi-; blue, cerato-; green, hypo-; orange, infrapharyngo-; turquoise, suprapharyngo-; purple, accessory elements; red, basi-; peachy pink, braincase. The colors of the mandibular elements are lightened and those of the hyoid are darkened. (MP4 10935 kb)

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Pradel, A., Maisey, J., Tafforeau, P. et al. A Palaeozoic shark with osteichthyan-like branchial arches. Nature 509, 608–611 (2014). https://doi.org/10.1038/nature13195

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