A computational model of teeth and the developmental origins of morphological variation

Abstract

The relationship between the genotype and the phenotype, or the genotype–phenotype map, is generally approached with the tools of multivariate quantitative genetics and morphometrics1,2,3,4. Whereas studies of development5,6,7 and mathematical models of development4,8,9,10,11,12 may offer new insights into the genotype–phenotype map, the challenge is to make them useful at the level of microevolution. Here we report a computational model of mammalian tooth development that combines parameters of genetic and cellular interactions to produce a three-dimensional tooth from a simple tooth primordia. We systematically tinkered with each of the model parameters to generate phenotypic variation and used geometric morphometric analyses to identify, or developmentally ordinate, parameters best explaining population-level variation of real teeth. To model the full range of developmentally possible morphologies, we used a population sample of ringed seals (Phoca hispida ladogensis)13. Seal dentitions show a high degree of variation, typically linked to the lack of exact occlusion13,14,15,16. Our model suggests that despite the complexity of development and teeth, there may be a simple basis for dental variation. Changes in single parameters regulating signalling during cusp development may explain shape variation among individuals, whereas a parameter regulating epithelial growth may explain serial, tooth-to-tooth variation along the jaw. Our study provides a step towards integrating the genotype, development and the phenotype.

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Figure 1: A model integrating gene networks and tissue mechanics.
Figure 2: Shape of variation in real and in silico seal teeth.
Figure 3: Variation in cusp position and number implicate the same patterning kernel parameters.
Figure 4: Serial tooth-to-tooth variation implicates a cellular parameter.

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Acknowledgements

We thank I. Corfe, A. R. Evans, J. Fierst, M. Fortelius, B. Julia, S. Sova, J. Hakanen, E. Harjunmaa, N. Navarro, I. Thesleff, P. C. Wright and S. Zohdy for comments, discussions, and support on this work, A. Kangas for help in data collection, and M. Hildén and I. Hanski (Finnish Museum of Natural History) for access to collections. This study was supported by the Ramón y Cajal Program (RYC-2007-00149) and the Academy of Finland.

Author Contributions I.S.-C. and J.J. conceived the study; I.S.-C. constructed the computational model and performed computer simulations; J.J. obtained the empirical data; I.S.-C. and J.J. performed quantitative analyses and wrote the paper.

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Correspondence to Isaac Salazar-Ciudad or Jukka Jernvall.

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Salazar-Ciudad, I., Jernvall, J. A computational model of teeth and the developmental origins of morphological variation. Nature 464, 583–586 (2010). https://doi.org/10.1038/nature08838

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