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.

  • Article
  • Published:

Acanthodian dental development and the origin of gnathostome dentitions

Nature Ecology & Evolution volume 5, pages 919–926 (2021)Cite this article

Subjects

Abstract

Chondrichthyan dentitions are conventionally interpreted to reflect the ancestral gnathostome condition but interpretations of osteichthyan dental evolution in this light have proved unsuccessful, perhaps because chondrichthyan dentitions are equally specialized, or else evolved independently. Ischnacanthid acanthodians are stem-Chondrichthyes; as phylogenetic intermediates of osteichthyans and crown-chondrichthyans, the nature of their enigmatic dentition may inform homology and the ancestral gnathostome condition. Here we show that ischnacanthid marginal dentitions were statodont, composed of multicuspidate teeth added in distally diverging rows and through proximal superpositional replacement, while their symphyseal tooth whorls are comparable to chondrichthyan and osteichthyan counterparts. Ancestral state estimation indicates the presence of oral tubercles on the jaws of the gnathostome crown-ancestor; tooth whorls or tooth rows evolved independently in placoderms, osteichthyans, ischnacanthids, other acanthodians and crown-chondrichthyans. Crown-chondrichthyan dentitions are derived relative to the gnathostome crown-ancestor, which possessed a simple dentition and lacked a permanent dental lamina, which evolved independently in Chondrichthyes and Osteichthyes.

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

Fig. 1: Jaw bones and marginal dentition of ischnacanthid acanthodians.
Fig. 2: Surface and reconstructed growth of marginal tooth rows on an ischnacanthid acanthodian jawbone.
Fig. 3: Virtual development of teeth on an ischnacanthid acanthodian jawbone.
Fig. 4: Tooth whorl of an ischnacanthid acanthodian.
Fig. 5: The 50% majority rule consensus tree from a tip-dated Bayesian analysis, annotated with ancestral state reconstructions for oral tubercles.
Fig. 6: The 50% majority rule consensus tree from a tip-dated Bayesian analysis, annotated with ancestral state reconstructions for ankylosed tooth rows and tooth whorls.

Similar content being viewed by others

Data availability

The data matrix is available at https://doi.org/10.6084/m9.figshare.14447139. Sources for taxa and age ranges and the phylogenetic character list are available as supplementary information. Tomograms and surface files are archived in the University of Bristol data repository, data.bris, at https://doi.org/10.5523/bris.1557rzkyzst5b2jagjuz9li5er.

Code availability

XML BEAST2 files, MrBayes Nexus files, BEAST1 XML files and R scripts are available at https://doi.org/10.6084/m9.figshare.14447139.

References

  1. Smith, M. M. & Coates, M. I. Evolutionary origins of the vertebrate dentition: phylogenetic patterns and developmental evolution. Eur. J. Oral. Sci. 106, 482–500 (1998).

    Article  PubMed  Google Scholar 

  2. Botella, H., Blom, H., Dorka, M., Ahlberg, P. E. & Janvier, P. Jaws and teeth of the earliest bony fishes. Nature 448, 583–586 (2007).

    Article  CAS  PubMed  Google Scholar 

  3. Debiais-Thibaud, M. et al. Tooth and scale morphogenesis in shark: an alternative process to the mammalian enamel knot system. BMC Evol. Biol. 15, 292 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  4. Rasch, L. J. et al. An ancient dental gene set governs development and continuous regeneration of teeth in sharks. Dev. Biol. 415, 347–370 (2016).

    Article  CAS  PubMed  Google Scholar 

  5. Smith, M. M., Fraser, G. J. & Mitsiadis, T. A. Dental lamina as source of odontogenic stem cells: evolutionary origins and developmental control of tooth generation in gnathostomes. J. Exp. Zool. B 312, 260–280 (2009).

    Article  Google Scholar 

  6. Tucker, A. S. & Fraser, G. J. Evolution and developmental diversity of tooth regeneration. Semin. Cell Dev. Biol. 25, 71–80 (2014).

    Article  PubMed  Google Scholar 

  7. Coates, M. I. et al. An early chondrichthyan and the evolutionary assembly of a shark body plan. Proc. R. Soc. B 285, https://doi.org/10.1098/rspb.2017.2418 (2018).

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

    Article  CAS  PubMed  Google Scholar 

  9. Giles, S., Friedman, M. & Brazeau, M. D. Osteichthyan-like cranial conditions in an Early Devonian stem gnathostome. Nature 520, 82–U175 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Smith, M. M. & Johanson, Z. Separate evolutionary origins of teeth from evidence in fossil jawed vertebrates. Science 299, 1235–1236 (2003).

    Article  CAS  PubMed  Google Scholar 

  11. Denison, R. H. Acanthodii (Gustav Fischer, 1979).

  12. Smith, M. M. Vertebrate dentitions at the origin of jaws: when and how pattern evolved. Evol. Dev. 5, 394–413 (2003).

    Article  PubMed  Google Scholar 

  13. Blais, S. A., MacKenzie, L. A. & Wilson, M. V. H. Tooth-like scales in Early Devonian eugnathostomes and the ‘outside-in’ hypothesis for the origins of teeth in vertebrates. J. Vertebr. Paleontol. 31, 1189–1199 (2011).

    Article  Google Scholar 

  14. Burrow, C. J., Newman, M., den Blaauwen, J., Jones, R. & Davidson, R. The Early Devonian ischnacanthiform acanthodian Ischnacanthus gracilis (Egerton, 1861) from the Midland Valley of Scotland. Acta Geol. Polon. 68, 335–362 (2018).

    Google Scholar 

  15. Burrow, C. J. Acanthodian fishes with dentigerous jaw bones: the Ischnacanthiformes and Acanthodopsis. Foss. Strat. 50, 8–22 (2004).

    Google Scholar 

  16. Lindley, I. D. Acanthodian fish remains from the lower devonian cavan bluff limestone (Murrumbidgee group), Taemas district, New South Wales. Alcheringa 24, 11–35 (2000).

    Article  Google Scholar 

  17. Newman, M. J., Burrow, C. J. & den Blaaauwen, J. L. A new species of ischnacanthiform acanthodian from the Givetian of Mimerdalen, Svalbard. Norw. J. Geol. 99, 1–13 (2019).

  18. Gross, W. Über das Gebiss der Acanthodier und Placodermen. Zool. J. Linn. Soc. 47, 121–130 (1967).

    Article  Google Scholar 

  19. Ørvig, T. Acanthodian dentition and its bearing on the relationships of the group. Palaeontographica A 143, 119–150 (1973).

    Google Scholar 

  20. Smith, M. M. & Coates, M. I. in Major Events Of Early Vertebrate Evolution (ed. Ahlberg. P. E.) 223–240 (Taylor & Francis, 2001).

  21. Donoghue, P. C. J. et al. Synchrotron X-ray tomographic microscopy of fossil embryos. Nature 442, 680–683 (2006).

    Article  CAS  PubMed  Google Scholar 

  22. Friedman, M. & Brazeau, M. D. A reappraisal of the origin and basal radiation of the osteichthyes. J. Vertebr. Paleontol. 30, 36–56 (2010).

    Article  Google Scholar 

  23. Doeland, M., Couzens, A. M. C., Donoghue, P. C. J. & Rücklin, M. Tooth replacement in early sarcopterygians. R. Soc. Open Sci. 6, https://doi.org/10.1098/rsos.191173 (2019).

  24. Jarvik, E. Middle and Upper Devonian porolepiformes from East Greenland with special reference to Glyptolepis groenlandica n. sp. and a discussion on the structure of the head of porolepiformes. Medd. Groenl. 187, 1–295 (1972).

    Google Scholar 

  25. Chen, D., Blom, H., Sanchez, S., Tafforeau, P. & Ahlberg, P. E. The stem osteichthyan Andreolepis and the origin of tooth replacement. Nature 539, 237–241 (2016).

    Article  PubMed  Google Scholar 

  26. Rücklin, M. et al. Development of teeth and jaws in the earliest jawed vertebrates. Nature 491, 748–751 (2012).

    Article  PubMed  Google Scholar 

  27. Clemen, G., Bartsch, P. & Wacker, K. Dentition and dentigerous bones in juveniles and adults of Polypterus senegalus (Cladistia, Actinopterygii). Ann. Anat. 180, 211–221 (1998).

    Article  CAS  PubMed  Google Scholar 

  28. Chen, D. et al. Development of cyclic shedding teeth from semi-shedding teeth: the inner dental arcade of the stem osteichthyan Lophosteus. R. Soc. Open Sci. 4, 161084 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  29. Patterson, C. in Problems Of Phylogenetic Reconstruction (eds Joysey, K. A. & Friday, A. E.) Systematics Association Special Volume 21, 21–74 (Academic Press, 1982).

  30. King, B., Qiao, T., Lee, M. S. Y., Zhu, M. & Long, J. A. Bayesian morphological clock methods resurrect placoderm monophyly and reveal rapid early evolution in jawed vertebrates. Syst. Biol. 66, 499–516 (2017).

    PubMed  Google Scholar 

  31. Andreev, P. et al. The systematics of the Mongolepidida (Chondrichthyes) and the Ordovician origins of the clade. PeerJ 4, e1850 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Rücklin, M., Giles, S., Janvier, P. & Donoghue, P. C. J. Teeth before jaws? Comparative analysis of the structure and development of the external and internal scales in the extinct jawless vertebrate Loganellia scotica. Evol. Dev. 13, 523–532 (2011).

    Article  PubMed  Google Scholar 

  33. White, E. I. The Old Red Sandstone of Brown Lee Hill and the adjacent area. II. Palaeontology. Bull. Br. Mus. (Nat. Hist.) Geol. 5, 245–310 (1961).

    Google Scholar 

  34. Stampanoni, M. et al. TOMCAT: a beamline for tomographic microscopy and coherent radiology experiments. AIP Conf. Proc. 879, 848 (2007).

    Article  CAS  Google Scholar 

  35. Maisey, J. G. et al. in Evolution and Development of FIshes (eds Johanson, Z., Underwood, C. J. & Richter, M.) 87–109 (Cambridge Univ. Press, 2018).

  36. Bouckaert, R. et al. BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 15, e1006650 (2019).

  37. Ayres, D. L. et al. BEAGLE: an application programming interface and high-performance computing library for statistical phylogenetics. Syst. Biol. 61, 170–173 (2012).

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  39. Gavryushkina, A., Welch, D., Stadler, T. & Drummond, A. J. Bayesian inference of sampled ancestor trees for epidemiology and fossil calibration. PLoS Comput. Biol. 10, e1003919 (2014).

  40. Drummond, A. J., Ho, S. Y. W., Phillips, M. J. & Rambaut, A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, 699–710 (2006).

    Article  CAS  Google Scholar 

  41. Rambaut, A., Suchard, M. A., Xie, D. & Drummond, A. J. Tracer v1.6 http://beast.bio.ed.ac.uk/Tracer (2014).

  42. Warren, D. L., Geneva, A. J. & Lanfear, R. RWTY (R We There Yet): an R package for examining convergence of Bayesian phylogenetic analyses. Mol. Biol. Evol. 34, 1016–1020 (2017).

    CAS  PubMed  Google Scholar 

  43. King, B. Which morphological characters are influential in a Bayesian phylogenetic analysis? Examples from the earliest osteichthyans. Biol. Lett. 15, https://doi.org/10.1098/rsbl.2019.0288 (2019).

  44. 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  PubMed  PubMed Central  Google Scholar 

  45. Bapst, D. W. paleotree: an R package for paleontological and phylogenetic analyses of evolution. Methods Ecol. Evol. 3, 803–807 (2012).

    Article  Google Scholar 

  46. Brazeau, M. D. & Friedman, M. The characters of Palaeozoic jawed vertebrates. Zool. J. Linn. Soc. 170, 779–821 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  47. Suchard, M. A. et al. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 4, https://doi.org/10.1093/ve/vey016 (2018).

  48. Lemey, P., Rambaut, A., Drummond, A. J. & Suchard, M. A. Bayesian phylogeography finds its roots. PLoS Comput. Biol. 5, e1000520 (2009).

  49. Minin, V. N. & Suchard, M. A. Counting labeled transitions in continuous-time Markov models of evolution. J. Math. Biol. 56, 391–412 (2008).

    Article  PubMed  Google Scholar 

  50. Xie, W., Lewis, P. O., Fan, Y., Kuo, L. & Chen, M. H. Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Syst. Biol. 60, 150–160 (2011).

    Article  PubMed  Google Scholar 

  51. Kass, E. R. R. & Bayes, A. E. Factors. J. Am. Stat. Assoc. 90, 773–795 (1995).

    Article  Google Scholar 

  52. Jombart, T. et al. OutbreakTools: a new platform for disease outbreak analysis using the R software. Epidemics 7, 28–34 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  53. Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).

    Article  CAS  PubMed  Google Scholar 

  54. Schliep, K. P. phangorn: phylogenetic analysis in R. Bioinformatics 27, 592–593 (2011).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank S. Bengtson and D. Murdock for help at the TOMCAT beamline. We also thank E. Bernard (Natural History Museum) for access to collections and for facilitating the loan of specimens. The study was funded by an EU FP7 Marie-Curie Intra-European Fellowship (to M.R. and P.C.J.D.), Natural Environmental Research Council grant NE/G016623/1 (to P.C.J.D.) and Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO) (VIDI 864.14.009 to M.R.). We acknowledge the Paul Scherrer Institut, Villigen, Switzerland, for provision of synchrotron radiation beamtime at the TOMCAT (X02DA) beamline of the Swiss Light Source (to P.C.J.D. and S. Bengtson).

Author information

Authors and Affiliations

  1. Naturalis Biodiversity Center, Leiden, The Netherlands

    Martin Rücklin & Benedict King

  2. School of Earth Sciences, University of Bristol, Life Sciences Building, Bristol, UK

    Martin Rücklin, John A. Cunningham & Philip C. J. Donoghue

  3. Department of Linguistic and Cultural Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany

    Benedict King

  4. Department of Earth Sciences, Natural History Museum, London, UK

    Zerina Johanson

  5. Swiss Light Source, Paul Scherrer Institut, Villigen, Switzerland

    Federica Marone

Authors
  1. Martin Rücklin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Benedict King
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John A. Cunningham
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zerina Johanson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Federica Marone
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Philip C. J. Donoghue
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M.R. and P.C.J.D. designed the initial research. M.R., J.A.C., P.C.J.D. and F.M. performed scans. M.R. and J.A.C. segmented tomograms. B.K. produced the phylogenetic data matrix, and performed the phylogenetic analysis and ancestral state reconstruction. M.R. and P.C.J.D. drafted the manuscript, to which all authors contributed.

Corresponding authors

Correspondence to Martin Rücklin or Philip C. J. Donoghue.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Ecology & Evolution thanks Gareth Fraser, Min Zhu, Moya Meredith Smith and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Virtual development of teeth on an ischnacanthid acanthodian jawbone.

Tooth rows of NRM-PZ P. 9449 Early Devonian, Canada. Labelled sclerochronology of the lateral row (a), lingual row (b) and overgrowth of the initial teeth at the centre of ossification (c). Colours of the nested boxes reflect the successive stages of tooth development. Scale bar represents 169 µm in a, b, and 72 µm in (c).

Extended Data Fig. 2 50% majority-rule consensus tree from tip-dated analysis of early gnathostome fossils.

‘Psarolepids’ constrained as stem osteichthyans, annotated with ancestral state reconstruction of tooth whorls.

Extended Data Fig. 3 Posterior probabilities from ancestral state reconstructions.

In column 1, ‘chondrichthyans’ refers to conventionally-defined chondrichthyans possessing tooth batteries. This includes Doliodus and crown chondrichthyans. Posterior probabilities are similar for tip-dated trees, and for undated Bayesian trees time-scaled a posteriori.

Supplementary information

Supplementary Information

Scores for taxa and ranges, character list and references.

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rücklin, M., King, B., Cunningham, J.A. et al. Acanthodian dental development and the origin of gnathostome dentitions. Nat Ecol Evol 5, 919–926 (2021). https://doi.org/10.1038/s41559-021-01458-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-021-01458-4

This article is cited by

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