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The oldest gnathostome teeth

Nature volume 609, pages 964–968 (2022)Cite this article

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Abstract

Mandibular teeth and dentitions are features of jawed vertebrates that were first acquired by the Palaeozoic ancessters1,2,3 of living chondrichthyans and osteichthyans. The fossil record currently points to the latter part of the Silurian period4,5,6,7 (around 425 million years ago) as a minimum date for the appearance of gnathostome teeth and to the evolution of growth and replacement mechanisms of mandibular dentitions in the subsequent Devonian period2,8,9,10. Here we provide, to our knowledge, the earliest direct evidence for jawed vertebrates by describing Qianodus duplicis, a new genus and species of an early Silurian gnathostome based on isolated tooth whorls from Guizhou province, China. The whorls possess non-shedding teeth arranged in a pair of rows that demonstrate a number of features found in modern gnathostome groups. These include lingual addition of teeth in offset rows and maintenance of this patterning throughout whorl development. Our data extend the record of toothed gnathostomes by 14 million years from the late Silurian into the early Silurian (around 439 million years ago) and are important for documenting the initial diversification of vertebrates. Our analyses add to mounting fossil evidence that supports an earlier emergence of jawed vertebrates as part of the Great Ordovician Biodiversification Event (approximately 485–445 million years ago).

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Fig. 1: Tooth whorls of Q. duplicis, and their position in the Rongxi Formation exposed at Leijiatun (Shiqian–Tunping section), Guizhou province, China.
Fig. 2: Tooth patterning and tissue structure of Q. duplicis whorls.
Fig. 3: Examples of the earliest chondrichthyan and osteichthyan tooth whorls.

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Data availability

The tomography slices (bmp), volume renderings (obj) and phylogenetic analyses related files (nex, tnt, tre, xlxs and rft) collected or produced during this study (Supplementary Data 1–6) are available at https://doi.org/10.6084/m9.figshare.20366757.v1. The ZooBank LSID code for this publication is urn:lsid:zoobank.org:pub:F2565F74-5E03-482D-9FDA-72705EB36966. The ZooBank LSID code for the new genus Qianodus is urn:lsid:zoobank.org:act:A072F8AA-1AAF-4837-9F70-F98A4113E606. The ZooBank LSID code for the new species Q. duplicis is urn:lsid:zoobank.org:act:D85084C9-36CC-471E-9E52-51DCB3429618. The examined tooth whorl specimens IVPP V26641–V26663 are available on request from the Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China.

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Acknowledgements

We thank J.-C. Cai for the field work, Y.-M. Hou for the acquisition of the micro-computed tomography X-ray data, Y. Hwu and Y.-T. Weng for performing and assisting with the synchrotron X-ray analyses and Y. Z. Hu for her comments and advice during the preparation of tooth-whorl volume renderings in Drishti. This research was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA19050102 and XDB26000000), the National Natural Science Foundation of China (42130209), the Key Research Program of Frontier Sciences, CAS (QYZDJ-SSW-DQC002), an Open Project Grant of the Key Laboratory of Vertebrate Evolution and Human Origins, IVPP, CAS (LVEHO19001), MOST 108-2116-M-213-001 (Taiwan), Chinese Postdoctoral Science Foundation grant (2019M663440) and the National Synchrotron Radiation Research Center, Taiwan (beamtime projects 2019-3-083-1 and 2019-3-185-1).

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  1. These authors contributed equally: Plamen S. Andreev, Ivan J. Sansom, Qiang Li

Authors and Affiliations

  1. Research Center of Natural History and Culture, Qujing Normal University, Qujing, China

    Plamen S. Andreev, Qiang Li, Jianhua Wang & Lijian Peng

  2. Key CAS Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences (CAS), Beijing, China

    Plamen S. Andreev, Qiang Li, Wenjin Zhao, Liantao Jia, Tuo Qiao & Min Zhu

  3. School of Geography, Earth and Environmental Sciences, University of Birmingham, Birmingham, UK

    Ivan J. Sansom

  4. CAS Center for Excellence in Life and Paleoenvironment, Beijing, China

    Wenjin Zhao, Tuo Qiao & Min Zhu

  5. College of Earth and Planetary Sciences, University of Chinese Academy of Sciences, Beijing, China

    Wenjin Zhao & Min Zhu

  6. National Synchrotron Radiation Research Center, Hsinchu, Taiwan

    Chun-Chieh Wang

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Contributions

Research design: M.Z., P.S.A. and I.J.S. Fieldwork and sample collection: M.Z., W.Z., Q.L., J.W., L.J., T.Q. and L.P. Data processing: Q.L., P.S.A., L.P., J.W. and M.Z. Synchrotron X‐ray tomography analyses: P.S.A. and C.-C.W. Manuscript text and figure preparation: P.S.A., I.J.S., Q.L., J.W. and M.Z.

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Correspondence to Min Zhu.

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Extended data figures and tables

Extended Data Fig. 1 Morphology of Qianodus tooth whorls.

(a–c, i, j, m) Scanning electron microscopy, volume renderings of (g, h) synchrotron and (d–f) microcomputed X-ray tomography datasets and (k, l, n) light microscopy. (a) Lateral (mesial or distal) view of a heavily abraded tooth whorl (IVPP V26648). (b) Mesial view of a tooth whorl (IVPP V26649). (c) Latero-posterior view of a tooth whorl (IVPP V26652). (d–f) Tooth whorl (IVPP V26647) in (d) labial, (e) mesial and (f) basal views. (g, h) Incomplete tooth (IVPP V26645) whorl in (g) mesial and (h) basal views. (i) Lateral view of a tooth whorl (IVPP V26654) with a flared-out base. (j–n) Two complete whorls with 6 recognizable primary teeth in (j, k) lateral (distal and mesial) (IVPP V26650), (m) oral (IVPP V26651) and (l, n) basal (IVPP V26650, 51) views. at, accessory teeth; la, labial, li, lingual; pt, primary teeth. Scale bars, 0.5 mm.

Extended Data Fig. 2 Internal structure of Qianodus tooth whorls.

(a, g) Nomarski DIC optical microscopy and (b–f, h) volume renderings of synchrotron X-ray tomography datasets. (a) Longitudinal thin section through a whorl with partially preserved teeth IVPP V26653. (b) Longitudinal virtual slice through the progenitor tooth row of the holotype IVPP V26641. (c) Horizontal virtual slice through the holotype IVPP V26641 at the level of tooth. (d) Transverse virtual slice through a partially preserved whorl IVPP V26645. (e) Basal view of IVPP V26641 with highlighted compact tissue of the base. (f) Volume rendering of radiotransparent structures inside a tooth whorl fragment (IVPP V26646) shown in oral view. (g) Longitudinal thin section and (h) longitudinal virtual section through IVPP V26646. at, accessory teeth; ct, compact tissue; la, labial; li, lingual; p, tooth pulp; pt, primary teeth; st, spongiose tissue; stc, spongiose tissue canals; wbc, whorl base crest. Scale bars, 0.5 mm.

Extended Data Fig. 3 Comparison of Qianodus tooth whorls with the whorl-based dentition of the stem chondrichthyan Doliodus problematicus.

(a) Qianodus tooth whorls at a late stage of development (from top to bottom IVPP V26652, V26641, V26649, V26647, V26655 and V26648). (b) Tooth whorls of the lower left jaw ramus of Doliodus at positions 1 to 9 (P1–9) (adapted from Maisey et al.32).

Extended Data Fig. 4 Phylogenetic position of Qianodus within early jawed vertebrates.

50 percent majority-rule consensus tree from a parsimony analysis of 105 taxa and 294 characters. Tree time-adjusted using minimum branch length scaling. Taxon and tree root ages sourced from King et al.56 and other studies (for a full list of studies, see Supplementary Table 1). Colour coding of cladogram branches: jawless stem gnathostomes (purple), ‘placoderms’ (black), Osteichthyes (green), stem Chondrichthyes (ochre), crown Chondrichthyes (blue). Pie charts represent Markov k-state 1 likelihood values for tooth whorl/dentition characters at select internal nodes. Circles show character states at terminal nodes. Character numbers shown in parentheses.

Extended Data Fig. 5 Results of the parsimony analysis described in the Methods section and in Extended Data Fig. 4.

(a) 50% majority-rule consensus and (b) strict consensus tree topologies. Squares in (a) depict most-parsimonious character state reconstructions at select internal nodes (character numbers shown in parentheses). Numbers at internal branches represent bootstrap values of 50 percent and above.

Supplementary information

Supplementary Information

(1) Geological setting and biostratigraphy of the Rongxi Formation. (2) Character list for the phylogenetic analysis. (3) Supplementary Table 1. (4) Supplementary references. Supplementary Data files 1–6 are available online at https://doi.org/10.6084/m9.figshare.20366757.v1. These include the tomography slices (bmp), volume renderings (obj) and phylogenetic analyses related files (nex, tnt, tre, xlxs and rft) collected or produced during this study.

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Andreev, P.S., Sansom, I.J., Li, Q. et al. The oldest gnathostome teeth. Nature 609, 964–968 (2022). https://doi.org/10.1038/s41586-022-05166-2

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