Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

A symmoriiform chondrichthyan braincase and the origin of chimaeroid fishes

Nature volume 541, pages 208–211 (2017)Cite this article

Subjects

Abstract

Chimaeroid fishes (Holocephali) are one of the four principal divisions of modern gnathostomes (jawed vertebrates). Despite only 47 described living species1, chimaeroids are the focus of resurgent interest as potential archives of genomic data2 and for the unique perspective they provide on chondrichthyan and gnathostome ancestral conditions. Chimaeroids are also noteworthy for their highly derived body plan1,3,4. However, like other living groups with distinctive anatomies5, fossils have been of limited use in unravelling their evolutionary origin, as the earliest recognized examples already exhibit many of the specializations present in modern forms6,7. Here we report the results of a computed tomography analysis of Dwykaselachus, an enigmatic chondrichthyan braincase from the ~280 million year old Karoo sediments of South Africa8. Externally, the braincase is that of a symmoriid shark9,10,11,12,13 and is by far the most complete uncrushed example yet discovered. Internally, the morphology exhibits otherwise characteristically chimaeroid specializations, including the otic labyrinth arrangement and the brain space configuration relative to exceptionally large orbits. These results have important implications for our view of modern chondrichthyan origins, add robust structure to the phylogeny of early crown group gnathostomes, reveal preconditions that suggest an initial morpho-functional basis for the derived chimaeroid cranium, and shed new light on the chondrichthyan response to the extinction at the end of the Devonian period.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The braincase of D. oosthuizeni Oelofsen 1986 modelled from high-resolution CT of SAM K5840.
Figure 2: Dwykaselachus and Callorhinchus milii endocranial anatomy.
Figure 3: Plot of orbit versus log-otic capsule length, normalized to basicranial length.
Figure 4: Phylogeny of early chondrichthyans scaled to stratigraphy, with comparative morphology of selected chondrichthyan and outgroup crania.

Similar content being viewed by others

References

  1. Didier, D. A., Kemper, J. M. & Ebert, D. A. in Biology of Sharks and Their Relatives (eds Carrier, J. C., Musick, J. A. & Heithaus, M. R. ) 97–122 (CRC, 2012)

  2. Venkatesh, B. et al. Elephant shark genome provides unique insights into gnathostome evolution. Nature 505, 174–179 (2014)

    Article  ADS  CAS  Google Scholar 

  3. Patterson, C. The phylogeny of the chimaeroids. Phil. Trans. R. Soc. Lond. B 249, 101–219 (1965)

    Article  ADS  Google Scholar 

  4. Stahl, B. J. in Handbook of Paleoichthyology Vol. 4 (ed. Schultze, H.-P. ) (Friedrich Pfeil, 1999)

  5. Simmons, N. B., Seymour, K. L., Habersetzer, J. & Gunnell, G. F. Primitive Early Eocene bat from Wyoming and the evolution of flight and echolocation. Nature 451, 818–821 (2008)

    Article  ADS  CAS  Google Scholar 

  6. Grogan, E. D., Lund, R. & Greenfest-Allen, E. in Biology of Sharks and Their Relatives (eds Carrier, J. C., Musick, J. A. & Heithaus, M. R. ) 3–29 (CRC, 2012)

  7. Finarelli, J. A. & Coates, M. I. Chondrenchelys problematica (Traquair, 1888) redescribed: a Lower Carboniferous, eel-like holocephalan from Scotland. Earth Env. Sci. Trans. R. Soc. Edinb. 105, 1–25 (2014)

    Google Scholar 

  8. Oelofsen, B. W. in Indo-Pacific Fish Biology: Proceedings of the SecondInternational Conference on Indo-Pacific Fishes (eds Uyeno, T., Arai, R., Taniuchi, T. & Matsuura, K. ) 107–124 (Ichthyological Society of Japan, 1986)

  9. Maisey, J. G. The braincase in Paleozoic symmoriiform and cladoselachian sharks. Bull. Am. Mus. Nat. Hist. 307, 1–122 (2007)

    Article  Google Scholar 

  10. Coates, M. I. & Sequeira, S. E. K. The braincase of a primitive shark. Trans. R. Soc. Edinb. Earth Sci. 89, 63–85 (1998)

    Article  Google Scholar 

  11. Zangerl, R. & Case, G. R. Cobelodus aculeatus (Cope), an anacanthous shark from the Pennsylvanian black shales of North America. Palaeontographica A 154, 107–157 (1976)

    Google Scholar 

  12. Williams, M. E. The “cladodont level” sharks of the Pennsylvanian black shales of central North America. Palaeontographica A 190, 83–158 (1985)

    Google Scholar 

  13. Pradel, A., Maisey, J. G., Tafforeau, P., Mapes, R. H. & Mallatt, J. A Palaeozoic shark with osteichthyan-like branchial arches. Nature 509, 608–611 (2014)

    Article  ADS  CAS  Google Scholar 

  14. Bangert, B., Stollhofen, H., Lorenz, V. & Armstrong, R. The geochronology and significance of ash-fall tuffs in the glaciogenic Carboniferous-Permian Dwyka Group of Namibia and South Africa. J. Afr. Earth Sci. 29, 33–49 (1999)

    Article  ADS  CAS  Google Scholar 

  15. McKay, M. P. et al. U-PB zircon tuff geochronology from the Karoo Basin, South Africa: implications of zircon recycling on stratigraphic age controls. Int. Geol. Rev. 57, 393–410 (2015)

    Article  Google Scholar 

  16. De Beer, G. R. & Moy-Thomas, J. A. On the skull of Holocephali. Phil. Trans. R. Soc. Lond. B 224, 287–312 (1935)

    Article  ADS  Google Scholar 

  17. Schaeffer, B. The xenacanth shark neurocranium, with comments on elasmobranch monophyly. Bull. Am. Mus. Nat. Hist. 169, 1–66 (1981)

    Google Scholar 

  18. Pradel, A. Skull and brain anatomy of Late Carboniferous Sibyrhynchidae (Chondrichthyes, Iniopterygia) from Kansas and Oklahoma (USA). Geodiversitas 32, 595–661 (2010)

    Article  Google Scholar 

  19. Maisey, J. G., Miller, R. & Turner, S. The braincase of the chondrichthyan Doliodus from the Lower Devonian Campbellton Formation of New Brunswick, Canada. Acta Zoologica 90 (Suppl. 1), 109–122 (2009)

    Article  Google Scholar 

  20. Pradel, A., Didier, D., Casane, D., Tafforeau, P. & Maisey, J. G. Holocephalan embryo provides new information on the evolution of the glossopharyngeal nerve, metotic fissue and parachordal plate in gnathostomes. PLoS One 8, e66988 (2013)

    Article  ADS  CAS  Google Scholar 

  21. Giles, S. & Friedman, M. Virtual reconstruction of endocast anatomy in early ray-finned fishes (Osteichthyes, Actinopterygii). J. Paleontol. 88, 636–651 (2014)

    Article  Google Scholar 

  22. Howard, L. E. et al. Functional nasal morphology of chimaerid fishes. J. Morphol. 274, 987–1009 (2013)

    Article  Google Scholar 

  23. Coates, M. I. & Sequeira, S. E. K. in Major Events in Early Vertebrate Evolution (ed. Ahlberg, P. E. ) 241–262 (Taylor & Francis, 2001)

  24. Janvier, P. Early Vertebrates (Clarendon, 1996)

  25. Giles, S., Friedman, M. & Brazeau, M. D. Osteichthyan-like cranial conditions in an Early Devonian stem gnathostome. Nature 520, 82–85 (2015)

    Article  ADS  CAS  Google Scholar 

  26. Friedman, M. & Sallan, L. C. Five hundred million years of extinction and recovery: a Phanerozoic survey of large-scale diversity patterns in fishes. Palaeontology 55, 707–742 (2012)

    Article  Google Scholar 

  27. Pradel, A., Tafforeau, P., Maisey, J. G. & Janvier, P. A new paleozoic Symmoriiformes (Chondrichthyes) from the late Carboniferous of Kansas (USA) and cladistic analysis of early chondrichthyans. PLoS One 6, e24938 (2011)

    Article  ADS  CAS  Google Scholar 

  28. Cronin, T. W., Johnsen, S., Marshall, N. J. & Warrant, E. J. Visual Ecology (Princeton Univ. Press, 2014)

  29. Schmitz, L. & Wainwright, P. C. Nocturnality constrains morphological and functional diversity in the eyes of reef fishes. BMC Evol. Biol. 11, 338 (2011)

    Article  Google Scholar 

  30. Lisney, T. J. A review of the sensory biology of chimaeroid fishes (Chondrichthyes; Holocephali). Rev. Fish Biol. Fish. 20, 571–990 (2010)

    Article  Google Scholar 

  31. Swofford, D. L. PAUP*: Phylogenetic Analysis Using Parsimony (*And Other Methods) v.4.0a147 (Sinauer Associates, 2003)

  32. Felsenstein, J. Confidence-limits on phylogenies—an approach using the bootstrap. Evolution 39, 783–791 (1985)

    Article  Google Scholar 

  33. Bremer, K. The limits of amino-acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42, 795–803 (1988)

    Article  CAS  Google Scholar 

  34. Eriksson, T. AutoDecay Version 5.0. (2001)

  35. Rannala, B. & Yang, Z. Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference. J. Mol. Evol. 43, 304–311 (1996)

    Article  ADS  CAS  Google Scholar 

  36. Yang, Z. & Rannala, B. Bayesian phylogenetic inference using DNA sequences: a Markov Chain Monte Carlo Method. Mol. Biol. Evol. 14, 717–724 (1997)

    Article  CAS  Google Scholar 

  37. Lewis, P. O. A likelihood approach to estimating phylogeny from discrete morphological character data. Syst. Biol. 50, 913–925 (2001)

    Article  CAS  Google Scholar 

  38. Ronquist, F. & Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574 (2003)

    Article  CAS  Google Scholar 

  39. Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012)

    Article  Google Scholar 

  40. Gradstein, F. M., Ogg, J. G., Schmitz, M. & Ogg, G. The Geologic Time Scale 2012 (Elsevier, 2012)

  41. Brazeau, M. D. & Friedman, M. The origin and early phylogenetic history of jawed vertebrates. Nature 520, 490–497 (2015)

    Article  ADS  Google Scholar 

  42. Young, G. C. Devonian sharks from south-eastern Australia and Antarctica. Palaeontology 25, 817–843 (1982)

    Google Scholar 

  43. Gaudin, T. J. A re-examination of elasmobranch monophyly and chondrichthyan phylogeny. Jb. Geol. Palaont. Abh. 182, 133–160 (1991)

    Article  Google Scholar 

  44. Lund, R. & Grogan, E. D. Relationships of the Chimaeriformes and the basal radiation of the Chondrichthyes. Rev. Fish Biol. Fish. 7, 65–123 (1997)

    Article  Google Scholar 

  45. Ginter, M., Hampe, O. & Duffin, C. in Handbook of Paleoichthyology Vol. 3D (ed. Schultze, H.-P. ) (Friedrich Pfeil, 2010)

  46. Davis, S. P., Finarelli, J. A. & Coates, M. I. Acanthodes and shark-like conditions in the last common ancestor of modern gnathostomes. Nature 486, 247–250 (2012)

    Article  ADS  CAS  Google Scholar 

  47. Zhu, M. et al. A Silurian placoderm with osteichthyan-like marginal jaw bones. Nature 502, 188–193 (2013)

    Article  ADS  CAS  Google Scholar 

  48. Dupret, V., Sanchez, S., Goujet, D., Tafforeau, P. & Ahlberg, P. E. A. A primitive placoderm sheds light on the origin of the jawed vertebrate face. Nature 507, 500–503 (2014)

    Article  ADS  CAS  Google Scholar 

  49. Janvier, P. & Pradel, A. in Physiology of Elasmobranch Fishes: Structure and Interaction with Environment (eds Shadwick, R. E., Farrell, A. P. & Brauner, C. J. ) (Academic, 2016)

  50. Maisey, J. G. Chondrichthyan phylogeny: a look at the evidence. J. Vertebr. Paleontol. 4, 359–371 (1984)

    Article  Google Scholar 

  51. Zangerl, R. in Handbook of Paleoichthyology Vol. 3A (ed. Schultze, H.-P. ) (Gustav Fischer, 1981)

  52. Zangerl, R. in Mazon Creek Fossils (ed. Nitecki, M. H. ) 449–500 (Academic, 1979)

  53. Tapanila, L. et al. Jaws for a spiral-tooth whorl: CT images reveal novel adaptation and phylogeny in fossil Helicoprion. Biol. Lett. 9, 20130057 (2013)

    Article  Google Scholar 

  54. Benton, M. J. et al. Constraints on the timescale of animal evolutionary history. Palaeontologia Electronica 18, 1–116 (2015)

    Google Scholar 

  55. Darras, L., Derycke, C., Blieck, A. & Vachard, D. The oldest holocephalan (Chondrichthyes) from the Middle Devonian of the Boulonnais (Pas-de-Calais, France). C. R. Palevol 7, 297–304 (2008)

    Article  Google Scholar 

  56. Gardiner, B. G. The relationships of the palaeoniscid fishes, a review based on new specimens of Mimia and Moythomasia from the Upper Devonian of Western Australia. Bull. Br. Mus. Nat. Hist. 37, 173–428 (1984)

    Google Scholar 

Download references

Acknowledgements

We thank the Evolutionary Studies Institute micro-CT scanning unit at the University of the Witwatersrand in Johannesburg, South Africa, for provision of scanning facilities and K. Carlson and K. Jakata for technical assistance. We thank R. Smith and the staff of the South African Museum, Cape Town, for access and loan of specimen. We thank A. Gillis for the donation of Callorhinchus milii embryos and hatchlings. This work was supported by grants DEB-0917922 and DEB-1541491 from the National Science Foundation (to M.I.C.), and a research grant from the National Research Foundation/Department of Science and Technology South African Centre of Excellence in Palaeosciences (to R.W.G.).

Author information

Authors and Affiliations

  1. Department of Organismal Biology and Anatomy, University of Chicago, Chicago, 60637-1508, Illinois, USA

    Michael I. Coates, Katharine E. Criswell & Kristen Tietjen

  2. Geology Department and Albany Museum, Rhodes University, Grahamstown, 6139, South Africa

    Robert W. Gess

  3. UCD School of Biology and Environmental Science, UCD Science Education and Research Centre, University College Dublin, Belfield, 4, Dublin, Ireland

    John A. Finarelli

  4. UCD Earth Institute, University College Dublin, Belfield, 4, Dublin, Ireland

    John A. Finarelli

Authors
  1. Michael I. Coates
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert W. Gess
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John A. Finarelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Katharine E. Criswell
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kristen Tietjen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

This project was conceived by M.I.C. and R.W.G. and developed by M.I.C., R.W.G., J.A.F. and K.E.C. CT scanning of Moythomasia durgaringa was conducted by K.T.; renderings and animations of CT scans and graphics were completed by K.T. with input from M.I.C., K.E.C. and J.A.F. C. milii preparation and staining were completed by K.E.C. Phylogenetic data were collected by M.I.C., K.E.C. and J.A.F. Phylogenetic analyses were completed by J.A.F. and M.I.C. Morphometric data were collected by M.I.C. and K.E.C.; analysis was completed by M.I.C., K.E.C. and J.A.F. Manuscript and supplementary text preparation was undertaken by M.I.C., R.W.G. and J.A.F. with input from K.E.C.

Corresponding author

Correspondence to Michael I. Coates.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Reviewer Information Nature thanks M. Friedman, P. Janvier and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Extended data figures and tables

Extended Data Figure 1 D. oosthuizeni Oelofsen 1986 SAM K584, the nodule.

a, Ventral part, showing infilled orbits, ethmoid region floor and floor of otic and occipital regions in dorsal view; anterior to left. b, Nodule in lateral view, showing division between dorsal and ventral sections. c, Dorsal part, showing infilled nasal capsules, supraorbital shelves, and endocranium in ventral view. Anterior to right in b and c. d, Area of tesselate calcified cartilage.

Extended Data Figure 2 Comparison of symmoriiform braincases.

a, FMNH PF 13242, lateral view, drawn from figure 6 in ref. 9. b, FMNH 13242, ventral view, drawn from figure 8 in ref. 9. c, Cobelodus, FMNH PF 7345, drawn from figure 5b in ref. 11. d, Ozarcus, AMNH FF 20544, lateral view, drawn from extended data figure 2h in ref. 13, grey area signifies material missing in a. e, Ozarcus, AMNH FF 20544, ventral view, adapted from extended data figure 2h in ref. 13, Nature Publishing Group. f, Dwykaselachus, lateral view restored. g, Dwykaselachus, ventral view restored. h, Akmonistion, NMS 1981.63.22C, ventral view, drawn from figure 1c in ref. 10.

Extended Data Figure 3 Ethmoid region of Dwykaselachus based on CT rendering of SAM K584.

a, Anterior view with material anterior to blue line in b removed. b, Dorsal view of nasal capsules and anterior portion of interorbital space, modelled as if sectioned horizontally at mid-capsular level; horizontal blue line indicates level of sections shown in a and c. c, Anterior view of endocranial spaces incompletely infilled to show pattern of interconnecting chambers (model sectioned vertically at mid-nasal capsule level, as indicated by blue line in b). The subnasal space may have formed a cartilage-filled antorbital process (see also Extended Data Fig. 5a), but the communication with the nasal capsule via the subnasal fenestra raises the possibility that it housed an accessory nasal duct, resembling those in modern chimaeroids1,22; arrows suggest possible direction of water flow. d, Anterolateral and ventral aspect. e, Posterior view of ethmoid region, model sectioned across anterior of orbit. f, g, Line drawings of d and e, respectively.

Extended Data Figure 4 Endocast morphology of D. oosthuizeni SAM K5840.

a, b, CT rendering of cranial endocast, semicircular canals and ampullae, and path of superficial ophthalmic nerves in dorsal view (a) and in lateral view (b).

Extended Data Figure 5 D. oosthuizeni SAM K5840 braincase.

a, CT rendering in ventrolateral view. b, Rendering of braincase roof, posterior to level of postorbital process, with occipital arch removed to show posterior tectum.

Extended Data Figure 6 D. oosthuizeni SAM K5840 braincase.

a, Anterior view of CT rendering of postorbital wall, as if the braincase is cross-sectioned (clipped) at mid-orbit level. b, Anterolateral view of same. Removal of ethmoid region permits an unobstructed view. c, d, CT rendering of braincase in posterior view (c) and posterolateral view (d).

Extended Data Figure 7 D. oosthuizeni SAM K5840 braincase.

Medial view of sagittal section of CT rendered neurocranium, showing endocranial spaces.

Extended Data Figure 8 Symmoriiform and osteichthyan (actinopterygian) occipital arches.

a, b, Dwykaselachus in lateral and posterior views; model based on mirrored right side CT of SAM K5840. c, d, Moythomasia durgaringa Gardiner & Bartram in lateral and posterior views, model based on CT of MV P222915 (dorsal portion of occipital plate missing). Blue line in a and c indicates profile of braincase posterior extremity of the otic capsule; profile for Moythomasia, drawn from ref. 56. In both examples, the dorsal part of the occipital arch does not project anteriorly between the otic capsules (unlike elasmobranch conditions).

Extended Data Figure 9 Dwykaselachus and Callorhinchus crania rendered semi-transparent in anterolateral view.

a, b, Dwykaselachus, model based on CT of SAM K5840 (a) and Callorhinchus, revealing relation of superficial ophthalmic trunks to forebrain, and forebrain level relative to dorsally prominent mesencephalon (b). c, Callorhinchus CT coronal preorbital slice linked to framed section in b; ellipses (black line) indicate orbit size.

Extended Data Figure 10 Consensus trees from phylogenetic analyses.

a, Maximum parsimony analysis. Strict consensus of 240 most parsimonious trees; node numbers ringed (character state transitions listed in Supplementary Table 2); numbers above branches are Bremer support scores and numbers below are bootstrap values. Character state summaries (grey boxes) list neurocranial changes at basal nodes within the total group Holocephali. b, Bayesian analysis. Majority rule consensus tree; numbers above branches are the posterior probabilities, measured as proportion of sampled trees in which that topology was recovered. Nodes ringed in red are recovered in both the maximum parsimony and Bayesian analyses.

Supplementary information

Supplementary Information

This file contains Supplementary Notes, Morphometric and Phylogenetic Analysis and Supplementary references. (PDF 1445 kb)

Supplementary Data

This zipped file contains the data matrix nexus file. (ZIP 6 kb)

Dwykaselachus braincase rotate and reveal endocast

Dwykaselachus braincase rotate and reveal endocast. (MP4 13894 kb)

Callorhinchus subadult skull rotate and internal morphology reveal

Callorhinchus subadult skull rotate and internal morphology reveal, illustrating palatal fusion to braincase, large orbits positioned mostly dorsal to forebrain, superficial ophthalmic nerve paths and associated ethmoid canal, brain and otic labyrinth configuration. (MP4 17089 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Coates, M., Gess, R., Finarelli, J. et al. A symmoriiform chondrichthyan braincase and the origin of chimaeroid fishes. Nature 541, 208–211 (2017). https://doi.org/10.1038/nature20806

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature20806

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing