Article | Published:

Replaying evolutionary transitions from the dental fossil record

Nature volume 512, pages 4448 (07 August 2014) | Download Citation

Abstract

The evolutionary relationships of extinct species are ascertained primarily through the analysis of morphological characters. Character inter-dependencies can have a substantial effect on evolutionary interpretations, but the developmental underpinnings of character inter-dependence remain obscure because experiments frequently do not provide detailed resolution of morphological characters. Here we show experimentally and computationally how gradual modification of development differentially affects characters in the mouse dentition. We found that intermediate phenotypes could be produced by gradually adding ectodysplasin A (EDA) protein in culture to tooth explants carrying a null mutation in the tooth-patterning gene Eda. By identifying development-based character inter-dependencies, we show how to predict morphological patterns of teeth among mammalian species. Finally, in vivo inhibition of sonic hedgehog signalling in Eda null teeth enabled us to reproduce characters deep in the rodent ancestry. Taken together, evolutionarily informative transitions can be experimentally reproduced, thereby providing development-based expectations for character-state transitions used in evolutionary studies.

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Acknowledgements

We thank M. Fortelius, J. Eronen, I. Thesleff, P. Munne for discussions; S. Alto, M. Mäkinen, R. Santalahti, R. Savolainen, and M. Christensen for technical assistance; P. Schneider for the Fc-EDA-A1-protein; F. de Sauvage for HhAntag compound; Hou Yemao for tomography; and the Finnish Museum of Natural History (Helsinki, Finland), Museum of Natural History (Stockholm, Sweden), and Museum für Naturkunde (Berlin, Germany) for specimen loans. This work was supported by the Academy of Finland to J.J., M.M., I.S.-C., R01-DE021420 (NIH/NIDCR) and an NIH Director’s New Innovator Award DP2-OD007191 to O.D.K., an Australian Research Council Future Fellowship to A.R.E, and the Major Basic Research Projects (2012CB821904) of MST to Z.-Q.Z. Data are presented in the Supplementary and Extended Data Tables, available in the MorphoBrowser database (http://morphobrowser.biocenter.helsinki.fi/) and from the authors, and models can be accessed at (http://www.biocenter.helsinki.fi/bi/evodevo/toothmaker.html).

Author information

Affiliations

  1. Developmental Biology Program, Institute of Biotechnology, University of Helsinki, P.O. Box 56, FIN-00014 Helsinki, Finland

    • Enni Harjunmaa
    • , Teemu Häkkinen
    • , Elodie Renvoisé
    • , Ian J. Corfe
    • , Marja L. Mikkola
    • , Isaac Salazar-Ciudad
    •  & Jukka Jernvall
  2. Program in Craniofacial and Mesenchymal Biology, University of California, San Francisco, San Francisco, California 94114, USA

    • Kerstin Seidel
    •  & Ophir D. Klein
  3. Department of Orofacial Sciences, University of California, San Francisco, San Francisco, California 94114, USA

    • Kerstin Seidel
    •  & Ophir D. Klein
  4. Division of Materials Physics, Department of Physics, University of Helsinki, P.O. Box 64, FIN-00014 Helsinki, Finland

    • Aki Kallonen
  5. Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China

    • Zhao-Qun Zhang
  6. School of Biological Sciences, Monash University, Victoria 3800, Australia

    • Alistair R. Evans
  7. Geosciences, Museum Victoria, GPO Box 666, Melbourne, Victoria 3001, Australia

    • Alistair R. Evans
  8. Genomics, Bioinformatics and Evolution Group. Department de Genètica i Microbiologia, Universitat Autònoma de Barcelona, Cerdanyola del Vallès 08193, Spain

    • Isaac Salazar-Ciudad
  9. Department of Pediatrics, University of California, San Francisco, San Francisco, California 94114, USA

    • Ophir D. Klein
  10. Institute for Human Genetics, University of California, San Francisco, San Francisco, California 94114, USA

    • Ophir D. Klein

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Contributions

E.H., J.J. and O.D.K. designed the project and wrote the initial manuscript. E.H. and E.R. performed culturing experiments and K.S. mouse experiments. E.H., E.R., A.K. and J.J. performed measurements and prepared images. I.J.C., A.R.E. and J.J. analysed evolutionary data. I.S.-C. constructed the computational model and T.H. the ToothMaker. M.L.M., Z.-Q.Z. provided materials, observations and scientific interpretations. O.D.K. and J.J. coordinated the study. All authors discussed the results and provided input on the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Ophir D. Klein or Jukka Jernvall.

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DOI

https://doi.org/10.1038/nature13613

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