Enamel, the hardest vertebrate tissue, covers the teeth of almost all sarcopterygians (lobe-finned bony fishes and tetrapods) as well as the scales and dermal bones of many fossil lobe-fins1,2,3,4,5. Enamel deposition requires an organic matrix containing the unique enamel matrix proteins (EMPs) amelogenin (AMEL), enamelin (ENAM) and ameloblastin (AMBN)6. Chondrichthyans (cartilaginous fishes) lack both enamel and EMP genes7,8. Many fossil and a few living non-teleost actinopterygians (ray-finned bony fishes) such as the gar, Lepisosteus, have scales and dermal bones covered with a proposed enamel homologue called ganoine1,9. However, no gene or transcript data for EMPs have been described from actinopterygians10,11. Here we show that Psarolepis romeri, a bony fish from the the Early Devonian period, combines enamel-covered dermal odontodes on scales and skull bones with teeth of naked dentine, and that Lepisosteus oculatus (the spotted gar) has enam and ambn genes that are expressed in the skin, probably associated with ganoine formation. The genetic evidence strengthens the hypothesis that ganoine is homologous with enamel. The fossil evidence, further supported by the Silurian bony fish Andreolepis, which has enamel-covered scales but teeth and odontodes on its dermal bones made of naked dentine12,13,14,15,16, indicates that this tissue originated on the dermal skeleton, probably on the scales. It subsequently underwent heterotopic expansion across two highly conserved patterning boundaries (scales/head–shoulder and dermal/oral) within the odontode skeleton.
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Sire, J.-Y., Donoghue, P. C. J. & Vickaryous, M. K. Origin and evolution of the integumentary skeleton in non-tetrapod vertebrates. J. Anat. 214, 409–440 (2009)
Chang, M.-M. & Smith, M. M. Is Youngolepis a porolepiform? J. Vertebr. Paleontol. 12, 294–312 (1992)
Smith, M. M. Enamel in the oral teeth of Latimeria chalumnae (Pisces: Actinistia): a scanning electron microscope study. J. Zool. 185, 355–369 (1978)
Satchell, P. G., Shuler, C. F. & Diekwisch, T. G. H. True enamel covering in teeth of the Australian lungfish Neoceratodus forsteri. Cell Tissue Res. 299, 27–37 (2000)
Smith, M. M. in Structure, Function and Evolution of Teeth (eds Smith, P. & Tchernov, E. ) 73–101 (Freund, 1992)
Sire, J.-Y., Davit-Béal, T., Delgado, S. & Gu, X. The origin and evolution of enamel mineralization genes. Cells Tissues Organs 186, 25–48 (2007)
Venkatesh, B. et al. Elephant shark genome provides unique insights into gnathostome evolution. Nature 505, 174–179 (2014)
Grady, J. E. Tooth development in sharks. Arch. Oral Biol. 15, 613–619 (1970)
Sasagawa, I., Ishiyama, M., Yokosuka, H. & Mikami, M. Teeth and ganoid scales in Polypterus and Lepisosteus, the basic actinopterygian fish: an approach to understand the origin of the tooth enamel. J. Oral Biosciences 55, 76–84 (2013)
Kawasaki, K. & Amemiya, C. T. SCPP genes in the coelacanth: tissue mineralization genes shared by sarcopterygians. J. Exp. Zool. B Mol. Dev. Evol. 322, 390–402 (2014)
Kawasaki, K. The SCPP gene family and the complexity of hard tissues in vertebrates. Cells Tissues Organs 194, 108–112 (2011)
Botella, H., Blom, H., Dorka, M., Ahlberg, P. E. & Janvier, P. Jaws and teeth of the earliest bony fishes. Nature 448, 583–586 (2007)
Zhu, M. et al. The oldest articulated osteichthyan reveals mosaic gnathostome characters. Nature 458, 469–474 (2009)
Gross, W. Fragliche Actinopterygier-Schuppen aus dem Silur Gotlands. Lethaia 1, 184–218 (1968)
Qu, Q., Sanchez, S., Blom, H., Tafforeau, P. & Ahlberg, P. E. Scales and tooth whorls of ancient fishes challenge distinction between external and oral ‘teeth’. PLoS One 8, e71890 (2013)
Cunningham, J. A., Rücklin, M., Blom, H., Botella, H. & Donoghue, P. C. J. Testing models of dental development in the earliest bony vertebrates, Andreolepis and Lophosteus. Biol. Lett. 8, 833–837 (2012)
Moffatt, P., Wazen, R. M., Dos Santos Neves, J. & Nanci, A. Characterisation of secretory calcium-binding phosphoprotein-proline-glutamine-rich 1: a novel basal lamina component expressed at cell-tooth interfaces. Cell Tissue Res. 358, 843–855 (2014)
Nakayama, Y., Holcroft, J. & Ganss, B. Enamel hypomineralization and structural defects in amelotin-deficient mice. J. Dent. Res. 94, 697–705 (2015)
Fraser, G. J. & Smith, M. M. Evolution of developmental pattern for vertebrate dentitions: an oro-pharyngeal specific mechanism. J. Exp. Zool. B Mol. Dev. Evol. 316B, 99–112 (2011)
Sire, J.-Y., Géraudie, J., Meunier, F. J. & Zylberberg, L. On the origin of ganoine: histological and ultrastructural data on the experimental regeneration of the scales of Calamoichthys calabaricus (Osteichthyes, Brachyopterygii, Polypteridae). Am. J. Anat. 180, 391–402 (1987)
Thomson, K. S. & McCune, A. Development of the scales in Lepisosteus as a model for scale formation in fossil fishes. Zool. J. Linn. Soc. 82, 73–86 (1984)
Poole, D. F. G. in Structural and Chemical Organization of Teeth Vol. 1 (ed. Miles, A. E. W. ) 111–149 (Academic, 1967)
Braasch, I. et al. A new model army: emerging fish models to study the genomics of vertebrate Evo-Devo. J. Exp. Zool. B Mol. Dev. Evol. 324, 316–341 (2015)
Gross, W. Lophosteus superbus Pander: Zähne, Zahnknochen und besondere Schuppenformen. Lethaia 4, 131–152 (1971)
Richter, M. & Smith, M. M. A microstructural study of the ganoine tissue of selected lower vertebrates. Zool. J. Linn. Soc. 114, 173–212 (1995)
Zhu, M. et al. A primitive fossil fish sheds light on the origin of bony fishes. Nature 397, 607–610 (1999)
Zhu, M. et al. A Silurian placoderm with osteichthyan-like marginal jaw bones. Nature 502, 188–193 (2013)
Qu, Q., Zhu, M. & Wang, W. Scales and dermal skeletal histology of an early bony fish Psarolepis romeri and their bearing on the evolution of rhombic scales and hard tissues. PLoS ONE 8, e61485 (2013)
Pearson, D. M. & Westoll, T. S. The Devonian actinopterygian Cheirolepis Agassiz. Trans. R. Soc. Edinb. 70, 337–399 (1979)
Jarvik, E. Basic Structure and Evolution of Vertebrates Vol. 1 (Academic, 1980)
Flicek, P. et al. Ensembl 2014. Nucleic Acids Res. 42, D749–D755 (2014)
Sievers, F. et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539 (2011)
Kawasaki, K. The SCPP gene repertoire in bony vertebrates and graded differences in mineralized tissues. Dev. Genes Evol. 219, 147–157 (2009)
Kawasaki, K., Suzuki, T. & Weiss, K. M. Phenogenetic drift in evolution: the changing genetic basis of vertebrate teeth. Proc. Natl Acad. Sci. USA 102, 18063–18068 (2005)
Petersen, T. N., Brunak, S., von Heijne, G. & Nielsen, H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods 8, 785–786 (2011)
This project was inspired in part by initial discussions with K. Kawasaki, whom we gratefully acknowledge. We thank the Broad Institute Genomics Platform and Vertebrate Genome Biology group, Spotted Gar Genome Consortium and K. Lindblad-Toh for making the data for L. oculatus available. We thank W. Zhang and S. Zhang for technical help with thin sections and SEM. The work was supported by the Knut and Alice Wallenberg Foundation through a Wallenberg Scholarship awarded to P.E.A., and by Vetenskapsrådet (Swedish Research Council) through a Young Researcher Grant awarded to T.H. M.Z. was funded by the National Basic Research Programme of China (2012CB821902).
The authors declare no competing financial interests.
Extended data figures and tables
Extended Data Figure 1 Exon organization of P/Q-rich SCPP genes in human, anole lizard, coelacanth, spotted gar and zebrafish.
Each box represents a single exon. 5′ and 3′ untranslated regions are marked in white and protein-coding regions are marked in black. Location of the signal peptide (SP) is marked in yellow (EMPs), orange (maturation-stage proteins) and grey (zebrafish SCPP6). P/Q-labelled exons contain at least 25% of Pro and Gln residues. Exons with aromatic residues Phe, Tyr and Trp are marked with Y/F. Conserved amino acid motifs are indicated on the top or inside the exon boxes. Nearly identical exons are marked by asterisk or circle.
Extended Data Figure 2 The skull roof (IVPP V17756) of P. romeri used for making thin sections in this study.
Dorsal view (left) showing the relative positions of the thin sections and anterior view (right) showing the position of premaxilla. ‘a–h’ represent positions of the eight sections in Extended Data Fig. 3. Scale bar, 5 mm.
Scale bar, 300 µm.
a, From Extended Data Fig. 2a (IVPP V17756.1). b, Detail of a under transmission light (top) and polarized light (bottom). c, From Extended Data Fig. 2b (IVPP V17756.4), under transmission light (top) and polarized light (bottom). d, From Extended Data Fig. 2d (IVPP V17756.4). e, Detail of d under transmission light (top) and polarized light (bottom). Scale bar, 100 µm.
Scale bar, 5 mm.
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Qu, Q., Haitina, T., Zhu, M. et al. New genomic and fossil data illuminate the origin of enamel. Nature 526, 108–111 (2015). https://doi.org/10.1038/nature15259
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