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Osteichthyan-like cranial conditions in an Early Devonian stem gnathostome

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Abstract

The phylogeny of Silurian and Devonian (443–358 million years (Myr) ago) fishes remains the foremost problem in the study of the origin of modern gnathostomes (jawed vertebrates). A central question concerns the morphology of the last common ancestor of living jawed vertebrates, with competing hypotheses advancing either a chondrichthyan-1,2,3 or osteichthyan-like4,5 model. Here we present Janusiscus schultzei gen. et sp. nov., an Early Devonian (approximately 415 Myr ago) gnathostome from Siberia previously interpreted as a ray-finned fish6, which provides important new information about cranial anatomy near the last common ancestor of chondrichthyans and osteichthyans. The skull roof of Janusiscus resembles that of early osteichthyans, with large plates bearing vermiform ridges and partially enclosed sensory canals. High-resolution computed tomography (CT) reveals a braincase bearing characters typically associated with either chondrichthyans (large hypophyseal opening accommodating the internal carotid arteries) or osteichthyans (facial nerve exiting through jugular canal, endolymphatic ducts exiting posterior to the skull roof) but lacking a ventral cranial fissure, the presence of which is considered a derived feature of crown gnathostomes7,8. A conjunction of well-developed cranial processes in Janusiscus helps unify the comparative anatomy of early jawed vertebrate neurocrania, clarifying primary homologies in ‘placoderms’, osteichthyans and chondrichthyans. Phylogenetic analysis further supports the chondrichthyan affinities of ‘acanthodians’, and places Janusiscus and the enigmatic Ramirosuarezia9 in a polytomy with crown gnathostomes. The close correspondence between the skull roof of Janusiscus and that of osteichthyans suggests that an extensive dermal skeleton was present in the last common ancestor of jawed vertebrates4, but ambiguities arise from uncertainties in the anatomy of Ramirosuarezia. The unexpected contrast between endoskeletal structure in Janusiscus and its superficially osteichthyan-like dermal skeleton highlights the potential importance of other incompletely known Siluro-Devonian ‘bony fishes’ for reconstructing patterns of trait evolution near the origin of modern gnathostomes.

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Figure 1: The skull of Janusiscus schultzei gen. et sp. nov. based on high-resolution CT of GIT 496-6 (Pi.1384).
Figure 2: Comparative braincase morphology of selected Palaeozoic gnathostomes.
Figure 3: Summary result of phylogenetic analyses.

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Acknowledgements

We thank U. Toom for access to material, E. Mark-Kurik for discussions on stratigraphy and specimen provenance, W. Renema and R. Garwood for assistance with scanning. This work was supported by a Natural Environment Research Council Cohort NE/J500045/1 grant to S.G., the Philip Leverhulme Prize and John Fell Fund, both to M.F., and the European Research Council (ERC) under the European Union’s Seventh Framework Programme (FP/2007-2013)/ERC Grant Agreement number 311092 to M.D.B.

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Authors and Affiliations

  1. Department of Earth Sciences, University of Oxford, South Parks Road, Oxford, OX1 3AN, UK,

    Sam Giles & Matt Friedman

  2. Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA Leiden, the Netherlands,

    Martin D. Brazeau

  3. Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot SL5 7PY, UK,

    Martin D. Brazeau

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  3. Martin D. Brazeau
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Contributions

The project was conceived by M.D.B. and M.F. CT scanning was conducted by M.F. and M.D.B. S.G. generated the CT renderings. Figs 1–3 were produced by M.D.B. and S.G. with input from M.F. All authors participated in the generation of phylogenetic data. M.D.B. conducted the phylogenetic analyses. All authors participated in the interpretation of the specimen data and writing the manuscript, and generating Extended Data Figs 1–9, Supplementary Fig. 1 and Supplementary Notes.

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Correspondence to Martin D. Brazeau.

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The authors declare no competing financial interests.

Additional information

The Life Science Identifiers (LSIDs) urn:lsid:zoobank.org:pub:CFD16449-8A34-4401-9E01-289EA91C2C77 (article), urn:lsid:zoobank.org:act:652A7405-164B-4D58-B5AF-F21EDF552303 (genus), and urn:lsid:zoobank.org:act:3BD31DC4-11E1-4510-A185-B295CC626C07 (species) have been deposited in ZooBank.

Extended data figures and tables

Extended Data Figure 1 Dermal skull roofing bones of Janusiscus and Dialipina salgueiroensis.

a, Photograph of the holotype (GIT 496-6 (Pi.1384)). b, Original interpretation modified with permission from ref. 6. Reinterpretation of bones italicized in brackets (where applicable). c, Photograph of the referred skull roof (GIT 496-7 (Pi.1383)). d, Original interpretation modified with permission from ref. 6. e, New interpretive drawing of the holotype (GIT 496-6 (Pi.1384)). f, New interpretive drawing of the referred skull roof (GIT 496-7 (Pi.1383)). g, Dialipina salgueiroensis, modified with permission from ref. 13.

Extended Data Figure 2 Scales attributed to Dialipina and scanning electron micrograph images of Janusiscus schultzei gen. et sp. nov.

Scales from the localities of the Kureika Formation along the Sida River, Kotui Basin, Siberia, previously referred to D. markae, in: a, external view (GIT 496-8 (Pi.1384a)), previously figured by Schultze6 (plate 1, figure 3); b, internal view (GIT 496-10 (Pi.1385b)); c, external view (GIT 496-16 (Pi.1387)), ventral margin at upper right. d, e, Gross-scale morphology of D. salgueiroensis and referred species of Dialipina. d, Holotype of D. salgueiroensis, from the Emsian of Canada. Reproduced from ref. 10 (Fig. 3h) (with kind permission from Springer Science and Business Media). e, Holotype of D. markae, from the Lochkovian of the New Siberian Islands. Reproduced from ref. 10 (Fig. 3a) (with kind permission from Springer Science and Business Media). f, Scale from the Kureika Formation, Siberia, referred to D. markae and figured previously (reproduced with permission from figure 4 in ref. 6). This scale is the same specimen as in a6. g, New interpretive drawing of scale in a. h, Broken edge of the skull roof in the holotype (GIT 496-6 (Pi.1384)). The histological structure is not preserved. i, The anterior part of the referred skull roof (GIT 496-7). The dermal bone is poorly preserved, with the bone in the centre of each ridge missing. The histological structure is not preserved. j, The holotype (GIT 496-6 (Pi.1384)) in dorsal view, showing the endoskeletal supraoccipital crest and openings of the endolymphatic ducts. Images in a, b, and c are modified slightly with permission from those by the Institute of Geology at Talinn University of Technology and licensed by CC 3.0 (http://geokogud.info/git/specimen_image/496/496-8.jpg; http://geokogud.info/git/specimen_image/496/496-10.jpg; http://geokogud.info/git/specimen_image/496/496-16.jpg).

Extended Data Figure 3 Semi-transparent rendering of the skull of Janusiscus schultzei gen. et sp. nov. showing osteichthyan-like traits not visible externally.

Scale bar, 5 mm.

Extended Data Figure 4 Janusiscus lacks endochondral ossification.

a, The actinopterygian Kentuckia deani MCZ 5226; tomographs showing extensive and well-developed endochondral ossification in both the sphenoid (top) and otic (bottom) regions. Bright white objects are voids within spongy endochodral bone that have been diagenetically infilled with dense (probably iron) minerals. b, Janusiscus schultzei gen. et sp. nov. GIT 496-6 (Pi.1384); tomographs showing lack of obvious endochondral ossification in either the sphenoid (top) or otic (bottom) regions. There is also no visual indication of endochondral bone in a break across the ethmoid region of this same specimen.

Extended Data Figure 5 Subcranial ridges in Janusiscus and early crown gnathostomes.

a, Reconstructed tomographs showing that the thickenings along the lateral margins of the sphenoid region of Janusiscus do not represent artefacts of post-mortem compression. b, The ‘acanthodian’ Ptomacanthus anglicus NHMUK PV P 24919a; a silicone peel of the specimen preserved in negative, dusted with ammonium chloride. Portions of the skull other than the neurocranium are partially masked for clarity. c, The chondrichthyan Doliodus problematicus NBMG 10127/1a; a reconstruction of the neurocranium based on CT data. d, Janusiscus schultzei gen. et sp. nov. GIT 496-6 (Pi.1384); a reconstruction of the neurocranium based on CT data. Red arrows in each panel indicate subcranial ridges.

Extended Data Figure 6 Orbit anatomy of Janusiscus schultzei gen. et sp. nov.

a, Scanning electron micrograph image into left orbit showing endoskeletal bone and surrounding matrix. b, Image based on X-ray computed microtomography scan with matrix digitally removed. c, Lateral view into right orbit, with matrix digitally removed. d, Anterolateral view into right orbit, with matrix digitally removed. e, Interpretive drawing of the orbit, based on a composite of the left and right orbits of the holotype (GIT 496-6 (Pi.1384)). Arrow points to anterior.

Extended Data Figure 7 Comparison of transverse processes in the braincases of early gnathostomes.

a, Macropetalichthys (redrawn from ref. 18). b, Dicksonosteus (redrawn from ref. 19). c, Buchanosteus (redrawn from ref. 29). d, Entelognathus (redrawn from ref. 4). e, Jagorina (redrawn from ref. 19). f, Ramirosuarezia (redrawn from ref. 9). g, Acanthodes (redrawn from ref. 3). h, Doliodus (redrawn from ref. 17). i, Cladodoides (redrawn from ref. 21). j, Orthacanthus (redrawn from ref. 20). k, Janusiscus. l, ‘Ligulalepis’ (redrawn from ref. 14). m, Mimipiscis (redrawn from ref. 16). n, Psarolepis (redrawn from ref. 25). o, Gogonasus (redrawn from ref. 35).

Extended Data Figure 8 Results of phylogenetic analysis.

a, Strict consensus of the 522,936 shortest trees (639 steps) for 78 taxa and 236 equally weighted characters. Digits above nodes indicate Bremer decay indices above 1. Digits below nodes indicate percentage bootstrap support. b, Adams consensus tree of the 522,936 shortest trees for 78 taxa and 236 equally weighted characters.

Extended Data Figure 9 Results of modified phylogenetic analyses.

a, Strict consensus tree of 216 trees with a score of 452.52565 resulting from analysis of characters reweighted according to retention index. b, Strict consensus of the 128,395 shortest trees for 77 taxa and 236 equally weighted characters, with Janusiscus removed from the data set.

Supplementary information

Supplementary Information

This file contains Supplementary Notes, Phylogenetic Analysis and Supplementary References. (PDF 1332 kb)

Supplementary Figure

This file contains Supplementary Figure 1. (PDF 470 kb)

Supplementary Data

This zipped file contains the Nexus matrix file. (ZIP 28 kb)

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Giles, S., Friedman, M. & Brazeau, M. Osteichthyan-like cranial conditions in an Early Devonian stem gnathostome. Nature 520, 82–85 (2015). https://doi.org/10.1038/nature14065

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