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.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
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).
Kemp, T. S. The Origin and Evolution of Mammals (Oxford Univ. Press, Oxford, 2005).
Kielan-Jaworowska, Z. et al. Mammals from the Age of Dinosaurs—Origins, Evolution, and Structure (Columbia Univ. Press, New York, 2004).
Crompton, A. W. in Studies in Vertebrate Evolution (eds Joysey, K. A. & Kemp, T. S.) 231–253 (Oliver & Boyd, Edinburgh, 1972).
Luo, Z.-X. Transformation and diversification in early mammal evolution. Nature 450, 1011–1019 (2007).
Crompton, A. W. & Hylander, W. L. in The Ecology and Biology of Mammal-like Reptiles (eds Hotton, N. III et al.) 263–282 (Smithsonian Institution, Washington, 1986).
Bramble, D. M. Origin of the mammalian feeding complex: models and mechanisms. Paleobiology 4, 271–301 (1978).
Barghusen, H. R. in Morphology of the Maxillomandibular Apparatus (ed. Schumacher, G. H.) 26–32 (Georg Thieme, Leipzig, 1972).
DeMar, R. & Barghusen, H. R. Mechanics and the evolution of the synapsid jaw. Evolution 26, 622–637 (1972).
Luo, Z.-X. Developmental patterns in Mesozoic evolution of mammal ears. Annu. Rev. Ecol. Evol. Syst. 42, 355–380 (2011).
Allin, E. F. Evolution of the mammalian middle ear. J. Morphol. 147, 403–437 (1975).
Sidor, C. A. Evolutionary trends and the origin of the mammalian lower jaw. Paleobiology 29, 605–640 (2003).
Manley, G. A. Evolutionary paths to mammalian cochleae. J. Assoc. Res. Otolaryngol. 13, 733–743 (2012).
Luo, Z.-X. et al. New evidence for mammaliaform ear evolution and feeding adaptation in a Jurassic ecosystem. Nature 548, 326–329 (2017).
Reichert, C. in Archiv für Anatomie, Physiologie und wissenschaftliche Medicin (ed. Müller, J.) 120–222 (W. Thome, Berlin, 1837).
Gaupp, E. W. T. Die Reichertsche Theorie (Hammer-, Amboss und Kieferfrage). Archiv für Anatomie und Entwicklungsgeschichte 1912, 1–426 (1913).
Urban, D. J. et al. A new developmental mechanism for the separation of the mammalian middle ear ossicles from the jaw. Proc. R. Soc. Lond. B 284, 20162416 (2017).
Anthwal, N., Urban, D. J., Luo, Z. X., Sears, K. E. & Tucker, A. S. Meckel’s cartilage breakdown offers clues to mammalian middle ear evolution. Nat. Ecol. Evol. 1, 0093 (2017).
Hylander, W. L. The functional significance of primate mandibular form. J. Morphol. 160, 223–239 (1979).
Herring, S. W., Rafferty, K. L., Liu, Z. J. & Marshall, C. D. Jaw muscles and the skull in mammals: the biomechanics of mastication. Comp. Biochem. Physiol. A 131, 207–219 (2001).
Liu, Z. J. & Herring, S. W. Bone surface strains and internal bony pressures at the jaw joint of the miniature pig during masticatory muscle contraction. Arch. Oral Biol. 45, 95–112 (2000).
Crompton, A. W. in Functional Morphology in Vertebrate Paleontology (ed. Thomason, J. J.) 55–75 (Cambridge Univ. Press, Cambridge, 1995).
Lautenschlager, S., Gill, P., Luo, Z. X., Fagan, M. J. & Rayfield, E. J. Morphological evolution of the mammalian jaw adductor complex. Biol. Rev. Camb. Philos. Soc. 92, 1910–1940 (2017).
Reed, D. A., Iriarte-Diaz, J. & Diekwisch, T. G. A three dimensional free body analysis describing variation in the musculoskeletal configuration of the cynodont lower jaw. Evol. Dev. 18, 41–53 (2016).
Rowe, T. in Mammal Phylogeny (eds Szalay, F. S. et al.) 129–145 (Springer, New York, 1993).
Kemp, T. S. The origin of higher taxa: macroevolutionary processes, and the case of the mammals. Acta Zool. 88, 3–22 (2007).
Hanken, J. & Wake, D. B. Miniaturization of body size: organismal consequences and evolutionary significance. Annu. Rev. Ecol. Syst. 24, 501–519 (1993).
Gill, P. G. et al. Dietary specializations and diversity in feeding ecology of the earliest stem mammals. Nature 512, 303–305 (2014).
Close, R. A., Friedman, M., Lloyd, G. T. & Benson, R. B. Evidence for a mid-Jurassic adaptive radiation in mammals. Curr. Biol. 25, 2137–2142 (2015).
Pacheco, C. P., Martinelli, A. G., Pavanatto, A. E., Soares, M. B. & Dias-da-Silva, S. Prozostrodon brasiliensis, a probainognathian cynodont from the Late Triassic of Brazil: second record and improvements on its dental anatomy. Hist. Biol. 30, 475–485 (2017).
Lautenschlager, S. Reconstructing the past: methods and techniques for the digital restoration of fossils. R. Soc. Open Sci. 3, 160342 (2016).
Lautenschlager, S. Cranial myology and bite force performance of Erlikosaurus andrewsi: a novel approach for digital muscle reconstructions. J. Anat. 222, 260–272 (2013).
Lautenschlager, S. Estimating cranial musculoskeletal constraints in theropod dinosaurs. R. Soc. Open Sci. 2, 150495 (2015).
Thomason, J. J. Cranial strength in relation to estimated biting forces in some mammals. Can. J. Zool. 69, 2326–2333 (1991).
Ashman, R. B. & Rho, J. Y. Elastic modulus of trabecular bone material. J. Biomech. 21, 177–181 (1988).
Curtis, N. et al. Predicting muscle activation patterns from motion and anatomy: modelling the skull of Sphenodon (Diapsida: Rhynchocephalia). J. R. Soc. Interface 7, 153–160 (2010).
Dumont, E. R., Grosse, I. R. & Slater, G. J. Requirements for comparing the performance of finite element models of biological structures. J. Theor. Biol. 256, 96–103 (2009).
Bright, J. A. The importance of craniofacial sutures in biomechanical finite element models of the domestic pig. PLoS ONE 7, e31769 (2012).
R Core Team. R: A Language and Environment for Statistical Computing https://www.R-project.org/ (R Foundation for Statistical Computing, Vienna, 2017).
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.).
Nature thanks C. A. Sidor and the other anonymous reviewer(s) for their contribution to the peer review of this work.
The authors declare no competing interests.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data figures and tables
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. c–f, 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.
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). a–g, 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. h–n, Finite element von-Mises-stress contour plots for bite at canine and last tooth (indicated by red arrows). Scale bars in h, j–n, 10 mm; i, 50 mm. Sample size for each species, n = 1.
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.
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.
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.
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.
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.
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.
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.
About this article
Cite this article
Lautenschlager, S., Gill, P.G., Luo, ZX. et al. The role of miniaturization in the evolution of the mammalian jaw and middle ear. Nature 561, 533–537 (2018). https://doi.org/10.1038/s41586-018-0521-4
- Bite Force
- Postdentary Bones
- Reduce Joint Loading
- Modern Mammals
Scientific Reports (2021)
Nature Communications (2020)