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The role of miniaturization in the evolution of the mammalian jaw and middle ear

Naturevolume 561pages533537 (2018) | Download Citation

Abstract

The evolution of the mammalian jaw is one of the most important innovations in vertebrate history, and underpins the exceptional radiation and diversification of mammals over the last 220 million years1,2. In particular, the transformation of the mandible into a single tooth-bearing bone and the emergence of a novel jaw joint—while incorporating some of the ancestral jaw bones into the mammalian middle ear—is often cited as a classic example of the repurposing of morphological structures3,4. Although it is remarkably well-documented in the fossil record, the evolution of the mammalian jaw still poses the paradox of how the bones of the ancestral jaw joint could function both as a joint hinge for powerful load-bearing mastication and as a mandibular middle ear that was delicate enough for hearing. Here we use digital reconstructions, computational modelling and biomechanical analyses to demonstrate that the miniaturization of the early mammalian jaw was the primary driver for the transformation of the jaw joint. We show that there is no evidence for a concurrent reduction in jaw-joint stress and increase in bite force in key non-mammaliaform taxa in the cynodont–mammaliaform transition, as previously thought5,6,7,8. Although a shift in the recruitment of the jaw musculature occurred during the evolution of modern mammals, the optimization of mandibular function to increase bite force while reducing joint loads did not occur until after the emergence of the neomorphic mammalian jaw joint. This suggests that miniaturization provided a selective regime for the evolution of the mammalian jaw joint, followed by the integration of the postdentary bones into the mammalian middle ear.

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Data availability

All relevant data (three-dimensional osteological, finite element analysis and multibody dynamics analysis models and computer code) are available via the DataBris repository of the University of Bristol (https://doi.org/10.5523/bris.n5f4ogftag0r2fbffh8u7waok).

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Acknowledgements

We thank P. Brewer, S. Chapman (Natural History Museum, London), O. Rauhut, G. Roessner (Bayerische Staatssammlung für Historische Geologie und Palaeontologie, Munich), K. Angielczyk, W. Simpson (Field Museum of Natural History, Chicago), G. Hantke and A. Kitchener (National Museums of Scotland, Edinburgh) for access to specimens in their care. T. Rowe and J. Maisano (University of Texas, Austin) generously provided digital datasets of specimens. A. Neander (University of Chicago), G. Roessner, D. Sykes (Natural History Museum London), K. Robson Brown (University of Bristol), O. Katsamenis and M. Mavrogordato (University of Southampton) assisted with computed tomography scanning. E. Ghirardello prepared the specimens and performed property testing on hedgehog mandible material. We thank J. Hopson (University of Chicago) for discussion. This work was funded by NERC (Natural Environment Research Council) grants NE/K01496X/1 (to E.J.R.) and NE/K013831/1 (to M.J.F.), and support from the University of Chicago (to Z.-X.L.).

Reviewer information

Nature thanks C. A. Sidor and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author information

Affiliations

  1. School of Earth Sciences, University of Bristol, Bristol, UK

    • Stephan Lautenschlager
    • , Pamela G. Gill
    •  & Emily J. Rayfield
  2. School of Geography, Earth and Environmental Sciences, University of Birmingham, Birmingham, UK

    • Stephan Lautenschlager
  3. Earth Science Department, The Natural History Museum, London, UK

    • Pamela G. Gill
  4. Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA

    • Zhe-Xi Luo
  5. School of Engineering and Computer Science, University of Hull, Hull, UK

    • Michael J. Fagan

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Contributions

S.L., P.G.G., Z.-X.L., M.J.F. and E.J.R. conceived and designed the study. S.L., P.G., Z.-X.L. and E.J.R. arranged logistics of specimens for computed tomography scanning and collected computed tomography data. Z.-X.L. provided access to additional specimens and data. S.L. processed computed tomography data, performed digital restorations and reconstructions, and performed computational analyses. M.J.F. and E.J.R. contributed to finite element and multibody dynamics analyses. S.L., P.G., Z.-X.L., M.J.F. and E.J.R equally contributed to the analysis of results. S.L. prepared main text, figures and supplementary data. S.L., P.G., Z.-X.L., M.J.F. and E.J.R. equally contributed to editing, commenting and revising the manuscript and figures. E.J.R. and M.J.F. acquired funding.

Competing interests

The authors declare no competing interests.

Corresponding authors

Correspondence to Stephan Lautenschlager or Emily J. Rayfield.

Extended data figures and tables

  1. Extended Data Fig. 1 Relative bite forces and biomechanical performance measures of cynodont and mammaliaform taxa.

    a, Relative bite forces for original-sized models. b, Relative bite forces for models scaled to the same size (with T. liorhinus as reference). Relative bite forces calculated as the ratio between muscle forces and resultant bite forces (obtained from reaction forces of finite element models). Range of values represents results for unilateral and bilateral bite simulations. cf, Average per element values for Von Mises stress (c), displacement (d), maximum principal strain (e) and minimum principal strain (f). Range of values represents results for unilateral and bilateral bite simulations (for original-sized models). Sample size for each species, n = 1.

  2. Extended Data Fig. 2 Biomechanical analysis results of cynodont and mammaliaform taxa for simulated unilateral biting at canines and last tooth.

    Results for models scaled to the same size (with T. liorhinus as reference). ag, Multibody dynamics analysis plots showing bite forces and joint forces (working and balancing side) during jaw opening and closing cycles. Range bars denote values obtained from reaction forces of finite element models. Peak values represent maximum bite force obtained from multibody dynamics analysis models. hn, Finite element von-Mises-stress contour plots for bite at canine and last tooth (indicated by red arrows). Scale bars in h, jn, 10 mm; i, 50 mm. Sample size for each species, n = 1.

  3. Extended Data Fig. 3 Tensile and compressive stress contour plots of mandibular joint region.

    Results shown for unilateral bite at the canine (upper rows) and the last tooth position (lower rows), each for the jaw joint of the working side and the balancing side in dorsal view. All contour plot images are scaled to the same size.

  4. Extended Data Fig. 4 Bite-force magnitude versus von Mises stress for different muscle activation patterns.

    Results shown for unilateral bite at the canine tooth position. Relative bite force measured as bite force in relation to von Mises stress occurring in the jaw joint.

  5. Extended Data Fig. 5 Bite-force magnitude versus von Mises stress for different muscle activation patterns.

    Results shown for unilateral bite at the last tooth position. Relative bite force measured as bite force in relation to von Mises stress occurring in the jaw joint.

  6. Extended Data Fig. 6 Bite-force magnitude versus tensile stress for different muscle activation patterns.

    Results shown for unilateral bite at the canine tooth position. Relative bite force measured as bite force in relation to tensile stress occurring in the jaw joint.

  7. Extended Data Fig. 7 Bite-force magnitude versus tensile stress for different muscle activation patterns.

    Results shown for unilateral bite at the last tooth position. Relative bite force measured as bite force in relation to tensile stress occurring in the jaw joint.

  8. Extended Data Fig. 8 Bite-force magnitude versus compressive stress for different muscle activation patterns.

    Results shown for unilateral bite at the canine tooth. Relative bite force measured as bite force in relation to compressive stress occurring in the jaw joint.

  9. Extended Data Fig. 9 Bite-force magnitude versus compressive stress for different muscle activation patterns.

    Results shown for unilateral bite at the last tooth. Relative bite force measured as bite force in relation to compressive stress occurring in the jaw joint.

Supplementary information

  1. Supplementary Information

    This file contains Supplementary Tables 1 and 2, Supplementary Text and References cited in the Supplementary Information.

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DOI

https://doi.org/10.1038/s41586-018-0521-4

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