High-level similarity of dentitions in carnivorans and rodents

Abstract

The study of mammalian evolution depends greatly on understanding the evolution of teeth and the relationship of tooth shape to diet. Links between gross tooth shape, function and diet have been proposed since antiquity, stretching from Aristotle1 to Cuvier2, Owen3 and Osborn4. So far, however, the possibilities for exhaustive, quantitative comparisons between greatly different tooth shapes have been limited. Cat teeth and mouse teeth, for example, are fundamentally distinct in shape and structure as a result of independent evolutionary change over tens of millions of years5. There is difficulty in establishing homology between their tooth components or in summarizing their tooth shapes, yet both carnivorans and rodents possess a comparable spectrum of dietary specializations from animals to plants. Here we introduce homology-free techniques6,7,8 to measure the phenotypic complexity of the three-dimensional shape of tooth crowns. In our geographic information systems (GIS) analysis of 441 teeth from 81 species of carnivorans and rodents, we show that the surface complexity of tooth crowns directly reflects the foods they consume. Moreover, the absolute values of dental complexity for individual dietary classes correspond between carnivorans and rodents, illustrating a high-level similarity between overall tooth shapes despite a lack of low-level similarity of specific tooth components. These results suggest that scale-independent forces have determined the high-level dental shape in lineages that are widely divergent in size, ecology and life history. This link between diet and phenotype will be useful for inferring the ecology of extinct species and illustrates the potential of fast-throughput, high-level analysis of the phenotype.

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Figure 1: Dental and dietary diversity in carnivorans and rodents.
Figure 2: Dental complexity follows diet similarly in carnivorans and rodents.

References

  1. 1

    Aristotle. Parts of Animals (transl. Peck, A. L.) (Harvard Univ. Press, Cambridge, Massachusetts, 1983)

  2. 2

    Cuvier, G. Discours sur les Révolutions de la Surface du Globe, et sur les Changements qu’elles ont Produits dans le Règne Animal (Dufour et d’Ocagne, Paris, 1825)

    Google Scholar 

  3. 3

    Owen, R. Odontography (Hippolyte Baillière, London, 1840–1845.)

  4. 4

    Osborn, H. F. Evolution of Mammalian Teeth, to and from the Triangular Type (Macmillan, New York, 1907)

    Google Scholar 

  5. 5

    Wible, J. R., Rougier, G. R. & Novacek, M. J. in The Rise of Placental Mammals: Origins and Relationships of the Major Extant Clades (eds Rose, K. D. & Archibald, J. D.) 15–36 (Johns Hopkins Univ. Press, Baltimore, Maryland, 2005)

    Google Scholar 

  6. 6

    Ungar, P. S. & M’Kirera, F. A solution to the worn tooth conundrum in primate functional anatomy. Proc. Natl Acad. Sci. USA 100, 3874–3877 (2003)

    ADS  CAS  Article  Google Scholar 

  7. 7

    Evans, A. R. Connecting morphology, function and tooth wear in microchiropterans. Biol. J. Linn. Soc. 85, 81–96 (2005)

    Article  Google Scholar 

  8. 8

    King, S. J. et al. Dental senescence in a long-lived primate links infant survival to rainfall. Proc. Natl Acad. Sci. USA 102, 16579–16583 (2005)

    ADS  CAS  Article  Google Scholar 

  9. 9

    Fortelius, M. in Teeth Revisited: Proceedings of the VIIth International Symposium on Dental Morphology (eds Russell, D. E., Santoro, J.-P. & Sigogneau-Russell, D.) 459–462 (Mémoires du Muséum national d’Histoire naturelle C, Paris, 1988)

    Google Scholar 

  10. 10

    Lucas, P. W. Dental Functional Morphology (Cambridge Univ. Press, Cambridge, 2004)

    Google Scholar 

  11. 11

    Evans, A. R. & Sanson, G. D. The tooth of perfection: functional and spatial constraints on mammalian tooth shape. Biol. J. Linn. Soc. 78, 173–191 (2003)

    Article  Google Scholar 

  12. 12

    Stevens, C. & Hume, I. Comparative Physiology of the Vertebrate Digestive System (Cambridge Univ. Press, Cambridge, 1995)

    Google Scholar 

  13. 13

    Kay, R. F. The functional adaptations of primate molar teeth. Am. J. Phys. Anthropol. 43, 195–215 (1975)

    ADS  CAS  Article  Google Scholar 

  14. 14

    Strait, S. G. Differences in occlusal morphology and molar size in frugivores and faunivores. J. Hum. Evol. 25, 471–484 (1993)

    Article  Google Scholar 

  15. 15

    Hillson, S. Teeth (Cambridge Univ. Press, Cambridge, 2005)

    Google Scholar 

  16. 16

    Peyer, B. Comparative Odontology (Univ. of Chicago Press, Chicago, Illinois, 1968)

    Google Scholar 

  17. 17

    Polly, P. D. On morphological clocks and paleophylogeography: towards a timescale for Sorex hybrid zones. Genetica 112, 339–357 (2001)

    Article  Google Scholar 

  18. 18

    Polly, P. D., Le Comber, S. C. & Burland, T. M. On the occlusal fit of tribosphenic molars: Are we underestimating species diversity in the Mesozoic? J. Mamm. Evol. 12, 283–299 (2005)

    Article  Google Scholar 

  19. 19

    Birdsey, G. M. et al. A comparative analysis of the evolutionary relationship between diet and enzyme targeting in bats, marsupials and other mammals. Proc. R. Soc. B 272, 833–840 (2005)

    CAS  Article  Google Scholar 

  20. 20

    Phillips, C. J., Weiss, A. & Tandler, B. Plasticity and patterns of evolution in mammalian salivary glands: comparative immunohistochemistry of lysozyme in bats. Eur. J. Morphol. 36, 19–26 (1998)

    Article  Google Scholar 

  21. 21

    Kurtén, B. The evolution of the polar bear, Ursus maritimus Phipps. Acta Zool. Fenn. 108, 1–30 (1964)

    Google Scholar 

  22. 22

    Kurtén, B. Pleistocene Mammals of Europe (Weidenfeld & Nicolson, London, 1968)

    Google Scholar 

  23. 23

    Talbot, S. L. & Shields, G. F. Phylogeography of brown bears (Ursus arctos) of Alaska and paraphyly within the Ursidae. Mol. Phylogenet. Evol. 5, 477–494 (1996)

    CAS  Article  Google Scholar 

  24. 24

    Kangas, A. T., Evans, A. R., Thesleff, I. & Jernvall, J. Nonindependence of mammalian dental characters. Nature 432, 211–214 (2004)

    ADS  CAS  Article  Google Scholar 

  25. 25

    Scott, R. S. et al. Dental microwear texture analysis shows within-species diet variability in fossil hominins. Nature 436, 693–695 (2005)

    ADS  CAS  Article  Google Scholar 

  26. 26

    Nowak, R. Walker’s Mammals of the World (Johns Hopkins Univ. Press, Baltimore, Maryland, 1999)

    Google Scholar 

  27. 27

    Shannon, C. E. A mathematical theory of communication. Bell Syst. Tech. J. 27, 379–423. 623–656 (1948)

    MathSciNet  Article  Google Scholar 

  28. 28

    Eterovick, P. C., Figueira, J. E. C. & Vasconcellos-Neto, J. Cryptic coloration and choice of escape microhabitats by grasshoppers (Orthoptera: Acrididae). Biol. J. Linn. Soc. 61, 485–499 (1997)

    Article  Google Scholar 

  29. 29

    Cover, T. M. & Thomas, J. A. Elements of Information Theory (Wiley, New York, 1991)

    Google Scholar 

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Acknowledgements

We thank G. Evans, K. Kavanagh, I. Salazar Ciudad, P. Wright, C. Strömberg, A. Gionis, G. Sanson, A. Lister, M. Skinner, I. Pljusnin and J. Eronen for comments and discussions on this work; E. Penttilä for scanning some of the rodents; M. Barbeitos for the suggestion to use information theory; and the following museum curators, collection managers and librarians for loans and reference material: O. Grönwall, R. Asher, M. Hildén, I. Hanski, K. Gully and M. Cytrynbaum. This study was supported by the Academy of Finland (J.J., M.F.), Synthesys (A.R.E.), the Centre for International Mobility (CIMO) (A.R.E.), and a National Science Foundation Postdoctoral Fellowship (G.P.W.).

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Correspondence to Alistair R. Evans.

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Data deposition: the three-dimensional scans for this study are deposited in the MorphoBrowser database (http://morphobrowser.biocenter.helsinki.fi/). Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Figures and Legends 1-2 and Supplementary Tables 1-8. Supplementary Figures show orientation patch count (OPC) versus two different measures of relative tooth size. Supplementary Tables list the species used in the study together with dietary information and references; data for some of the dental complexity measures; and the full results of statistical tests mentioned in the paper. (PDF 244 kb)

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Evans, A., Wilson, G., Fortelius, M. et al. High-level similarity of dentitions in carnivorans and rodents. Nature 445, 78–81 (2007). https://doi.org/10.1038/nature05433

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