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Function of pretribosphenic and tribosphenic mammalian molars inferred from 3D animation

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Abstract

Appearance of the tribosphenic molar in the Late Jurassic (160 Ma) is a crucial innovation for food processing in mammalian evolution. This molar type is characterized by a protocone, a talonid basin and a two-phased chewing cycle, all of which are apomorphic. In this functional study on the teeth of Late Jurassic Dryolestes leiriensis and the living marsupial Monodelphis domestica, we demonstrate that pretribosphenic and tribosphenic molars show fundamental differences of food reduction strategies, representing a shift in dental function during the transition of tribosphenic mammals. By using the Occlusal Fingerprint Analyser (OFA), we simulated the chewing motions of the pretribosphenic Dryolestes that represents an evolutionary precursor condition to such tribosphenic mammals as Monodelphis. Animation of chewing path and detection of collisional contacts between virtual models of teeth suggests that Dryolestes differs from the classical two-phased chewing movement of tribosphenidans, due to the narrowing of the interdental space in cervical (crown–root transition) direction, the inclination angle of the hypoflexid groove, and the unicuspid talonid. The pretribosphenic chewing cycle is equivalent to phase I of the tribosphenic chewing cycle, but the former lacks phase II of the tribosphenic chewing. The new approach can analyze the chewing cycle of the jaw by using polygonal 3D models of tooth surfaces, in a way that is complementary to the electromyography and strain gauge studies of muscle function of living animals. The technique allows alignment and scaling of isolated fossil teeth and utilizes the wear facet orientation and striation of the teeth to reconstruct the chewing path of extinct mammals.

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Acknowledgments

We thank Z.-X. Luo, T. Smith, G W. Rougier and two anonymous reviewers for their critical comments on the manuscript. This study is funded by the Deutsche Forschungsgemeinschaft (DFG) as part of the DFG research unit 771 “Function and performance enhancement in the mammalian dentition” (project D1; MA 1643/16-1) and is publication number 67 of the DFG research unit 771. We thank the members of the DFG research unit 771 for fruitful discussions, especially O. Kullmer (Senckenberg Forschungsinstitut und Naturmuseum Frankfurt, Germany) and colleagues (ZiLoX IT) for support and advice for the OFA software. G. Wilson helped to improve an older version of the manuscript. The dryolestid material was collected during field operations under the supervision of S. Henkel and B. Krebs of the Freie Universität Berlin (Germany). Fieldwork in Portugal was supported by the Serviços Geológicos de Portugal (Lisbon). A. H. Schwermann (Universität Bonn, Germany) shared polygonal models of Monodelphis domestica. We thank R. Schellhorn for discussion and D. Kranz (both from Universität Bonn, Germany) for suggestions that improved the artwork.

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During the repeated chewing movement of Dryolestes leiriensis, the occlusion of the paracone into the interdental space between two lower adjacent teeth is obvious. When the lower teeth are lifted, the paracone slides in to the interdental space and touches the hypoflexid groove lingually then slides down the groove in buccal direction. Interdental shearing is demonstrated by the collisional contacts that are detected between the polygonal surface models during every time step of the animated movement. The detected collisional contacts between the upper and lower teeth are shown in gradient colors (collisions of three time steps overlaid in one time step, green to red) in the first seven chewing cycles. To fully visualize all collisions that occur during the chewing movement, the upper molar is animated to be translucent after one cycle and the scene is changing from anterior view to buccal view and to occlusal view. In chewing cycle 8 (minute 1:32), the collisions are shown in normal coloring without overlay, for the viewer to get an impression of the size and allocation of detected areas between the polygonal models. The orange line is the path of the lower jaw calculated by the OFA. (MPG 9356 kb)

The animated chewing cycle of Dryolestes leiriensis in occlusal view with a translucent upper molar. The upper molar is animated to disappear after three chewing cycles for better view of the detected collisions in the interdental space between the lower molars. The visualization of the collisions starts with gradient colors (collisions of three time steps overlaid in one, green to red), and then changes in the third chewing cycle to normal coloring of the detected areas. The orange line is the path of the lower jaw calculated by the OFA. (MPG 5216 kb)

During the repeated chewing movement of Monodelphis domestica the occlusion of the protocone into the talonid basin positioned between the trigonids of two lower adjacent molars is obvious. When the lower teeth are lifted, the protocone first slides in to the talonid basin lingually then crosses the deepest part of the basin in direction of the hypoconid. The shearing is demonstrated by the collisional contacts that are detected between the polygonal surface models along the nearly vertical aspects of the trigon and the two trigonids during every time step of the animated movement. Crushing occurs when the protocone crossed the horizontal floor of the talonid basin. Leaving the talonid basin in buccal direction, the protocone crosses the lingual side of the hypoconid. Here, the additional collisional contacts are evident, which are nonexistent in Dryolestes leiriensis. The change of direction in the chewing path from downward to upward after crossing the deepest part of the talonid basin depicts the transition from phases I to II. The detected collisional contacts between the upper and lower teeth are shown in gradient colors (collisions of three time steps overlaid in one timestep, green to red) in the first seven chewing cycles. To fully visualize, all collisions that occur during the chewing movement the upper molar is animated to be translucent after one cycle and the scene is changing from anterior view to buccal view and to occlusal view. In chewing cycle 7 (minute 1:43), the collisions are shown in normal coloring without overlay, for the viewer to get an impression of the size and allocation of detected areas between the polygonal models. The orange line is the path of the lower jaw calculated by the OFA. (MPG 14582 kb)

The animated chewing cycle of Monodelphis domestica in occlusal view with a translucent upper molar. The upper molar is animated to disappear after three chewing cycles for better view of the detected collisions in the talonid basin between the lower molars. The visualization of the collisions starts with gradient colors (collisions of three time steps overlaid in one, green to red) and then changes in the third chewing cycle to normal coloring of the detected areas. The orange line is the path of the lower jaw calculated by the OFA. (MPG 8630 kb)

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Schultz, J.A., Martin, T. Function of pretribosphenic and tribosphenic mammalian molars inferred from 3D animation. Naturwissenschaften 101, 771–781 (2014). https://doi.org/10.1007/s00114-014-1214-y

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