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Acanthodian dental development and the origin of gnathostome dentitions

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.

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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.

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.

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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).

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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.

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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.

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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

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