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.

Nonindependence of mammalian dental characters

Abstract

Studies of mammalian evolution frequently use data derived from the dentition1,2,3,4. Dental characters are particularly central for inferring phylogenetic relationships of fossil taxa1,2,3,4, of which teeth are often the only recovered part. The use of different aspects of dental morphology as phylogenetic signals implies the independence of dental characters from each other. Here we report, however, that, at least developmentally, most dental characters may be nonindependent. We investigated how three different levels of the cell signalling protein ectodysplasin (Eda)5 changed dental characters in mouse. We found that with increasing expression levels of this one gene, the number of cusps increases, cusp shapes and positions change, longitudinal crests form, and number of teeth increases. The consistent modification of characters related to lateral placement of cusps can be traced to a small difference in the formation of an early signalling centre at the onset of tooth crown formation. Our results suggest that most aspects of tooth shape have the developmental potential for correlated changes during evolution which may, if not taken into account, obscure phylogenetic history.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Mouse molar teeth differ in several characters in mice with no (Tabby), normal (wild type), and above normal (K14-Eda) ectodysplasin activity.
Figure 2: Dynamics of Shh expression in developing first molar (a) and extra tooth (b).

References

  1. Beard, K. C., Tong, Y. S., Dawson, M. R., Wang, J. W. & Huang, X. S. Earliest complete dentition of an anthropoid primate from the late middle Eocene of Shanxi Province, China. Science 272, 82–85 (1996)

    ADS  CAS  Article  Google Scholar 

  2. Flynn, J. J., Parrish, J. M., Rakotosamimanana, B., Simpson, W. F. & Wyss, A. R. A Middle Jurassic mammal from Madagascar. Nature 401, 57–60 (1999)

    ADS  CAS  Article  Google Scholar 

  3. Luo, Z. X., Cifelli, R. L. & Kielan-Jaworowska, Z. Dual origin of tribosphenic mammals. Nature 409, 53–57 (2001)

    ADS  CAS  Article  Google Scholar 

  4. Seiffert, E. R., Simons, E. L. & Attia, Y. Fossil evidence for an ancient divergence of lorises and galagos. Nature 422, 421–424 (2003)

    ADS  CAS  Article  Google Scholar 

  5. Srivastava, A. K. et al. The Tabby phenotype is caused by mutation in a mouse homologue of the EDA gene that reveals novel mouse and human exons and encodes a protein (ectodysplasin-A) with collagenous domains. Proc. Natl Acad. Sci. USA 94, 13069–13074 (1997)

    ADS  CAS  Article  Google Scholar 

  6. Naylor, G. J. P. & Adams, D. C. Are the fossil data really at odds with the molecular data? Morphological evidence for cetartiodactyla phylogeny reexamined. Syst. Biol. 50, 444–453 (2001)

    CAS  PubMed  Google Scholar 

  7. Woodburne, M. O., Rich, T. H. & Springer, M. S. The evolution of tribospheny and the antiquity of mammalian clades. Mol. Phylogenet. Evol. 28, 360–385 (2003)

    CAS  Article  Google Scholar 

  8. Archibald, J. D. Timing and biogeography of the eutherian radiation: fossils and molecules compared. Mol. Phylogenet. Evol. 28, 350–359 (2003)

    Article  Google Scholar 

  9. O'Leary, M. A., Gatesy, J. & Novacek, M. J. Are the dental data really at odds with the molecular data? Morphological evidence for whale phylogeny reexamined. Syst. Biol. 52, 853–864 (2003)

    Article  Google Scholar 

  10. Geisler, J. H. & Uhen, M. D. Morphological support for a close relationship between hippos and whales. J. Vert. Paleontol. 23, 991–996 (2003)

    Article  Google Scholar 

  11. Bateson, W. Materials for the Study of Variation, Treated with Special Regard to Discontinuity in the Origin of Species (Macmillan, London, 1894)

    Google Scholar 

  12. Butler, P. M. The ontogeny of molar pattern. Biol. Rev. 31, 30–70 (1956)

    Article  Google Scholar 

  13. Van Valen, L. An analysis of developmental fields. Dev. Biol. 23, 456–477 (1970)

    CAS  Article  Google Scholar 

  14. Weiss, K. M., Stock, D. W. & Zhao, Z. Dynamic integrations and the evolutionary genetics of dental patterning. Crit. Rev. Oral Biol. Med. 9, 369–398 (1998)

    CAS  Article  Google Scholar 

  15. Hlusko, L. J. Integrating the genotype and phenotype in hominid paleontology. Proc. Natl Acad. Sci. USA 101, 2653–2657 (2004)

    ADS  CAS  Article  Google Scholar 

  16. Mustonen, T. et al. Stimulation of ectodermal organ development by ectodysplasin-A1. Dev. Biol. 259, 123–136 (2003)

    CAS  Article  Google Scholar 

  17. Mikkola, M. & Thesleff, I. Ectodysplasin signaling in development. Cytokine Growth Factor Rev. 14, 211–224 (2003)

    CAS  Article  Google Scholar 

  18. Laurikkala, J. et al. TNF signaling via the ligand-receptor pair ectodysplasin and edar controls the function of epithelial signaling centers and is regulated by Wnt and activin during tooth organogenesis. Dev. Biol. 229, 443–455 (2001)

    CAS  Article  Google Scholar 

  19. Jernvall, J., Keränen, S. V. E. & Thesleff, I. Evolutionary modification of development in mammalian teeth: Quantifying gene expression patterns and topography. Proc. Natl Acad. Sci. USA 97, 14444–14448 (2000)

    ADS  CAS  Article  Google Scholar 

  20. Jernvall, J. & Selänne, L. Laser confocal microscopy and geographic information systems in the study of dental morphology. Paleo. Electronica 2, 1–18 〈http://www-odp.tamu.edu/paleo/1999_1/confocal/issue1_99.htm〉 (1999)

    Google Scholar 

  21. Evans, A. R., Harper, I. S. & Sanson, G. D. Confocal imaging, visualization and 3-D surface measurement of small mammalian teeth. J. Microsc. 204, 108–118 (2001)

    MathSciNet  CAS  Article  Google Scholar 

  22. Flynn, L. J., Jacobs, L. L. & Lindsay, E. H. in Evolutionary Relationships among Rodents. A Multidisciplinary Analysis (eds Luckett, W. P. & Hartenberger, J.-L.) 589–616 (NATO ASI Series, Plenum, New York, 1985)

    Book  Google Scholar 

  23. Nowak, R. M. Walker's Mammals of the World, 5th edn (Johns Hopkins Univ. Press, Baltimore, 1991)

    Google Scholar 

  24. Meng, J., Hu, Y. M. & Li, C. K. The osteology of Rhombomylus (mammalia, glires): Implications for phylogeny and evolution of glires. Bull. Am. Mus. Nat. Hist. 275, 1–247 (2003)

    Article  Google Scholar 

  25. Salazar-Ciudad, I. & Jernvall, J. A gene network model accounting for development and evolution of mammalian teeth. Proc. Natl Acad. Sci. USA 99, 8116–8120 (2002)

    ADS  CAS  Article  Google Scholar 

  26. Dawson, M. R. A. & Tong, Y. New material of Pappocricetodon schaubi, an Eocene rodent (Mammalia: Cricetidae) from the Yuanqu basin, Shanxi province, China. Bull. Carnegie Mus. Nat. Hist. 34, 278–285 (1998)

    Google Scholar 

  27. Viriot, L., Peterkova, R., Peterka, M. & Lesot, H. Evolutionary implications of the occurrence of two vestigial tooth germs during early odontogenesis in the mouse lower jaw. Connect. Tiss. Res. 43, 129–133 (2002)

    Article  Google Scholar 

  28. Goodwin, H. T. Supernumerary teeth in Pleistocene, recent and hybrid individuals of the Spermophilus richardsonii complex (Sciuridae). J. Mamm. 79, 1161–1169 (1998)

    Article  Google Scholar 

  29. Tucker, A. S., Headon, D. J., Courtney, J. M., Overbeek, P. & Sharpe, P. T. The activation level of the TNF family receptor, Edar, determines cusp number and tooth number during tooth development. Dev. Biol. 268, 185–194 (2004)

    CAS  Article  Google Scholar 

  30. Pispa, J. et al. Tooth patterning and enamel formation can be manipulated by misexpression of TNF receptor Edar. Dev. Dyn. 231, 433–441 (2004)

    Article  Google Scholar 

Download references

Acknowledgements

We thank F. Ankel-Simons, M. Fortelius, J. Eronen, K. Kavanagh, S. King, J. Meng, P. Munne, T. Mustonen, J. Pispa, S. Pochron, I. Salazar-Ciudad, E. Seiffert, and P. C. Wright for comments or help on this work, which was supported by the Academy of Finland.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jukka Jernvall.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Methods

Tooth characters and character states (PDF 139 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Kangas, A., Evans, A., Thesleff, I. et al. Nonindependence of mammalian dental characters. Nature 432, 211–214 (2004). https://doi.org/10.1038/nature02927

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature02927

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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