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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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).
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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.