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The stem osteichthyan Andreolepis and the origin of tooth replacement

Abstract

The teeth of gnathostomes (jawed vertebrates) show rigidly patterned, unidirectional replacement that may or may not be associated with a shedding mechanism. These mechanisms, which are critical for the maintenance of the dentition, are incongruently distributed among extant gnathostomes. Although a permanent tooth-generating dental lamina is present in all chondrichthyans, many tetrapods and some teleosts, it is absent in the non-teleost actinopterygians. Tooth-shedding by basal hard tissue resorption occurs in most osteichthyans (including tetrapods) but not in chondrichthyans. Here we report a three-dimensional virtual dissection of the dentition of a 424-million-year-old stem osteichthyan, Andreolepis hedei, using propagation phase-contrast synchrotron microtomography, with a reconstruction of its growth history. Andreolepis, close to the common ancestor of all extant osteichthyans, shed its teeth by basal resorption but probably lacked a permanent dental lamina. This is the earliest documented instance of resorptive tooth shedding and may represent the primitive osteichthyan mode of tooth replacement.

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Figure 1: The lower jaw of Andreolepis.
Figure 2: The external odontode skeleton.
Figure 3: The shedding dentition.

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Acknowledgements

We thank P. Janvier for originally bringing LOG87-301DF to our attention and Lund University for the loan of the specimen. Scanning was performed at the ESRF as part of proposal ES 151 and with in-house beamtime provided to S.S. during her time as a postdoctoral fellow at ESRF. D.C., P.E.A. and S.S. thank ERC (Advanced Investigator Grant 233111) for support. D.C. and P.E.A. also thank the Knut and Alice Wallenberg Foundation (Wallenberg Scholarship awarded to P.E.A.).

Author information

Affiliations

Authors

Contributions

The project was conceived by D.C., P.E.A. and H.B. Scanning and reconstruction of datasets was carried out by S.S. and P.T., with minor contributions to the scanning by D.C. and P.E.A. All segmentation (morphological modelling) of datasets was done by D.C., with technical support by S.S. Morphological and developmental interpretation of the models was made by D.C. in collaboration with P.E.A. and H.B. The text was written by P.E.A. with contributions from D.C. and other authors. All figure images and animations were by D.C., except Extended Data Figs 6 and 7, which were by P.E.A. Figures assembled by P.E.A. and D.C. with input from other authors.

Corresponding authors

Correspondence to Donglei Chen or Per E. Ahlberg.

Additional information

The synchrotron data will be made available through the European Synchrotron Radiation Facility (ESRF) palaeontology database (http://paleo.esrf.eu), catalogued by taxon name and publication reference.

Reviewer Information Nature thanks M. Coates, M. M. Smith 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 Vasculature of the jaw bone.

a, A block model from an oblique posteromedial view showing the internal face of the jaw bone (rendered semi-transparent), the vasculature and a single shedding tooth on the lingual margin. Note the abrupt change in vascular organization between the original bone and the part added by appositional growth. Colours as in Fig. 1a. b, overview of LOG87- 301DF showing location of a. Scale bars, 0.1 mm (a) and 1 mm (b).

Extended Data Figure 2 Odontodes and growth increments in section.

a, A virtual section from the second high-resolution dataset (turquoise in Figs 1b, 2c, 3c), showing a transverse section through tooth-bearing region. On the left, 1 indicates a buried first-generation facial odontode with a characteristic smooth-sided pulp cavity and purely tubular dentine. On the right, 2 indicates a shedding tooth with basal resorption cup and partly cellular dentine. b, c, Two tooth files of first-generation odontodes and shedding teeth (see also Fig. 2a); c shows the morphology of the pulp cavities. Note the marked difference in surface texture: facial odontodes have smooth pulp cavities, but in shedding teeth the pulp cavities appear ‘warty’ because of numerous attached cell lacunae. Scale bars, 0.1 mm.

Extended Data Figure 3 Breakage and resorption of odontodes.

a, b, Virtual sections from the first high-resolution scan dataset (mauve in Figs 1b, 2c, 3c), illustrating examples of odontode damage by in vivo breakage (buried by later overgrowth) and resorption. c, A block model of the same region, with bone rendered transparent, terminating at a slice plane corresponding to virtual section in a and b. The ventral aspect is on the left in these images; the lateral surface of the bone is dorsal. Panel a is shown without labelling or highlighted model surfaces, to facilitate reader evaluation of the data quality. In b, modelled surfaces are shown, using the same colour code as Fig. 1a. Resorption can be distinguished from breakage because the characteristically curved resorption bays cut through both the odontode and the surrounding bony tissue that embeds it. Note that the facial odontodes all lack basal resorption cups. Scale bar, 0.1 mm.

Extended Data Figure 4 Odontodes on the ventral part of the facial lamina.

a, An overview of LOG87- 301DF showing location of detail images in b. b, Series of histological models, moving from deeper on the left to more superficial on the right. Shown are the vascular supply of the basal plate, four generations of odontode pulp cavities and the exposed surface of odontocomplexes. Colours of internal structures are as in Fig. 1a. Scale bars, 1mm (a), 0.1 mm (b).

Extended Data Figure 5 Morphology of an empty tooth socket.

a, Area of shedding dentition in dorsal view (see also Fig. 3a). The red box indicates the area shown in b and c, the black box indicates area shown in d and e. b, Empty tooth socket (see also Fig. 3a) and two adjacent teeth in oblique anteromesial view, socket indicated in dark blue. c, The same region, rendered to show only pulp cavities and radial vessels. d, e, Stereo pairs in dorsal (d) and oblique anteromesiodorsal (e) views. Note the distinct raised lip of the empty tooth socket. This socket contains no dentine remnants and is an exposed example of the structures elsewhere described as basal resorption cups (Fig. 3e, f and Extended Data Fig. 2a). Scale bars, 0.1 mm.

Extended Data Figure 6 Growth model.

af, Block models of the dorsal part of the bone in oblique dorsolateral view, lingual margin to the right, showing reconstructed ontogeny of the dentition and dermal ornament. Images are slightly schematized, vascular canals not shown. Scale bar, 0.1 mm. Colours as in Fig. 1a.

Extended Data Figure 7 The evolution of tooth replacement.

Simplified gnathostome phylogeny, based on recent publications1,17,22,26,27,28,29, showing diagrammatic cross-sections of lower jaws. The labial aspect is to the left and the lingual to the right in each diagram. Crosses denote fossil taxa. Sites of tooth development (pink) are known in extant taxa and inferred for fossil taxa. A permanent dental lamina can be either continuous along the length of the jaw, or discontinuous and associated to an individual tooth position. Other sites of tooth development include transient dental laminae and direct development from the oral epithelium2,3,4,5,6,7,8,9,10,11. The placoderm is based on a primitive arthrodire33, the acanthodian on a tooth-whorl-bearing form such as Ptomacanthus38,39. The actinopterygian and tetrapod examples represent common modes of tooth replacement in the respective groups. Both clades also contain different styles of tooth replacement, including intraosseous dental laminae4,5,6,8,9,10,11. Note that acanthodian-like parasymphysial tooth whorls occur in some fossil osteichthyans25,42,43; if these are homologous with those of chondrichthyans (a matter of current debate), then tooth removal by rotation would map to node G. Node O denotes the osteichthyan crown group node, node G the gnathostome crown group node.

Supplementary information

Scroll-through video of part of the first high-resolution scan (purple block in Figure 1b).

This video, which was reconstructed using an edge-detection algorithm and hence displays a rather flat grey tone with sharply delineated dark features such as odontode outlines and dentine tubules, shows non-shedding teeth overgrown by later generations of odontodes. The beginning of the shedding tooth field is on the far right, where well-developed resorption surfaces can be seen. The direction of the scroll-through is longitudinal to the jaw and the individual images are transverse sections. (MOV 29132 kb)

Scroll-through video of part of the second high-resolution scan (turquoise block in Figure 1b).

This video, which was reconstructed using a Paganin algorithm11,40 and displays more subtle gradations of grey values, shows the shedding dentition. The lingual edge of the bone is on the right. Note the very strongly developed, multiple resorption surfaces. Early in the video (9-19 seconds), a first generation odontode can be seen on the left, rising through overgrowth of later bone and odontodes. The direction of the scroll-through is longitudinal to the jaw and the individual images are transverse sections. (MOV 25885 kb)

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Chen, D., Blom, H., Sanchez, S. et al. The stem osteichthyan Andreolepis and the origin of tooth replacement. Nature 539, 237–241 (2016). https://doi.org/10.1038/nature19812

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