Letter | Published:

Rolling of the jaw is essential for mammalian chewing and tribosphenic molar function

Abstract

Over the past two centuries, mammalian chewing and related anatomical features have been among the most discussed of all vertebrate evolutionary innovations1,2,3. Chief among these features are two characters: the dentary-only mandible, and the tribosphenic molar with its triangulated upper cusps and lower talonid basin3,4,5. The flexible mandibular joint and the unfused symphysis of ancestral mammals—in combination with transformations of the adductor musculature and palate—are thought to have permitted greater mobility of each lower jaw, or hemimandible6,7. Following the appearance of precise dental occlusion near the origin of the mammalian crown8,9, therians evolved a tribosphenic molar with a craggy topography that is presumed to have been used to catch, cut and crush food. Here we describe the ancestral tribosphenic therian chewing stroke, as conserved in the short-tailed opossum Monodelphis domestica: it is a simple symmetrical sequence of lower tooth-row eversion and inversion during jaw opening and closing, respectively, enacted by hemimandibular long-axis rotation. This sequence is coupled with an eversion–inversion rotational grinding stroke. We infer that the ancestral therian chewing stroke relied heavily on long-axis rotation, including symmetrical eversion and inversion (inherited from the first mammaliaforms) as well as a mortar-and-pestle rotational grinding stroke that was inherited from stem therians along with the tribosphenic molar. The yaw-dominated masticatory cycle of primates, ungulates and other bunodont therians is derived; it is necessitated by a secondarily fused jaw symphysis, and permitted by the reduction of high, interlocking cusps10,11,12. The development of an efficient masticatory system—culminating in the tribosphenic apparatus—allowed early mammals to begin the process of digestion by shearing and crushing food into small boli instead of swallowing larger pieces in the reptilian manner, which necessitates a long, slow and wholly chemical breakdown. The vast diversity of mammalian teeth has emerged from the basic tribosphenic groundplan13.

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Data availability

The raw X-ray and computed-tomography data from the opossums have been deposited in the XMAPortal (http://xmaportal.org/webportal/, with study identifier HARVARD1). Source Data for Figs. 2, 3 and Extended Data Figs. 69 are provided with the paper. All other data that support the findings of this study are available from the corresponding author on request.

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Acknowledgements

We thank A. Biewener, P. Ramirez and the remaining staff at the Concord Field Station, Harvard University, for their support; S. Gatesy for invaluable advice and assistance with Maya; G. Wagner, J. Maziarz and the rest of the Wagner Laboratory for arranging transfer of the study subjects; K. Zyskowski for assistance in preparing and accessioning specimens; and D. B. Baier for developing the XROMM Maya tools. B.-A.S.B. and J.A.M. were supported by Yale University and the Yale Peabody Museum of Natural History. A.R.M. and E.L.B. were supported by Brown University, by an NSF Graduate Research Fellowship awarded to A.R.M. and by NSF grants 1661129 and 1655756 to E.L.B. E.A.H. was supported by The University of Texas at Austin and by an NSF Graduate Research Fellowship. C.M. and A.W.C. were supported by the Harvard Museum of Comparative Zoology.

Reviewer information

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

Author information

B.-A.S.B. and A.W.C. conceived and directed the study. J.A.M. performed surgeries with assistance from C.M., A.W.C. and B.-A.S.B. C.M., A.W.C., E.L.B., J.A.M. and B.-A.S.B. recorded trials and performed computed-tomography scans. E.A.H. and B.-A.S.B. segmented and interpreted skeletal and muscular computed tomography data. A.R.M., C.M., B.-A.S.B. and E.L.B. processed videos and generated XROMM data. A.R.M. and B.-A.S.B. prepared figures, and B.-A.S.B. performed morphometric analyses. B.-A.S.B., A.R.M. and E.A.H. wrote the paper.

Competing interests

The authors declare no competing interests.

Correspondence to Bhart-Anjan S. Bhullar.

Extended data figures and tables

  1. Extended Data Fig. 1 Geometric morphometric analysis of mammaliaform mandibles, showing the results of principal component analysis of dentary shape.

    Landmarks on Monodelphis dentary, redrawn and modified after ref. 23, are shown in the lower left. The darker red polygon encompasses all stem mammals in the analysis; the lighter red polygon encompasses all Mesozoic mammals and includes all stem therians, stem placentals and stem marsupials. The jaw of M. domestica is notably conservative, and falls near the middle of the restricted stem mammal shape-space and the larger stem therian–early therian shape-space. The M. domestica jaw is immediately surrounded by the jaws three taxa that are generally considered to be close in form to the mammalian ancestor: Morganucodon, Docodon and Hadrocodium. The ‘Mesozoic pan-therians’ includes three late-surviving early Cenozoic stem taxa (Necrolestes, Pucadelphys and Leptictis) with ghost lineages that stretch into the Mesozoic; the vertices of the light pink polygon, however, are all confirmed Mesozoic taxa.

  2. Extended Data Fig. 2 Phylogenetic framework for geometric morphometric analysis of mammaliaform mandibles.

    a, Phylogeny, including reconstructed ancestral nodes, superimposed on results from the principal component analysis shown in Extended Data Fig. 1. b, Topology used in the analysis, with relationships following previous work25,28,33. c, Enlarged depiction of landmark positions from Extended Data Fig. 1 upon the Monodelphis jaw, redrawn and modified after ref. 23.

  3. Extended Data Fig. 3 Condylar regions of mammaliaform dentaries.

    The dentary condyle of Monodelphis is conservative in its orientation, relative size and overall form.

  4. Extended Data Fig. 4 Typical chewing sequence, shown in anterolateral view.

    Muscle fibre colours correspond to those in Fig. 1.

  5. Extended Data Fig. 5 Marker sites and details of occlusal kinematics.

    a, b, Marker implantation sites for individual 1 (a) and individual 2 (b). Crania in ventral view and hemimandibles in lateral view. c, Anatomical coordinate system for the cranium, depicted in ventral and ventrolateral views on the left glenoid fossa of individual 1. d, Anatomical coordinate system for the hemimandibles, depicted in dorsal and posteromedial views on the left mandibular condyle of individual 1. e, Path of the lower first molar relative to a fixed upper molar; colouring conventions match those in Fig. 3. f, Mediolateral distance traversed by the protocone during a power stroke, indicated by red arrows and displayed on the lower first molar of individual 1.

  6. Extended Data Fig. 6 Temporomandibular joint rotations during five additional trials from two opossums.

    a, Individual 1 eating kibble. b, Individual 2 eating kibble. c, Individual 2 eating wax worms. d, Individual 2 eating wax worms. e, Individual 2 eating wax worms. Titles of the plots match trial names at http://xmaportal.org/webportal/. Source data

  7. Extended Data Fig. 7 Left (working side) and right (balancing side) temporomandibular joint rotations and translations for a chewing sequence of individual 1 eating wax worms.

    Representative of six total trials from two opossums. See ‘Description of temporomandibular joint translations’ in the Supplementary Information. Title of the plots matches trial name at http://xmaportal.org/webportal/. Source data

  8. Extended Data Fig. 8 Distance between radiopaque markers in lower canines during six trials from two opossums, demonstrating the mobility of the mandibular symphysis.

    a, Individual 1 eating kibble. b, Individual 1 eating wax worms. c, Individual 2 eating kibble. d, Individual 2 eating wax worms. e, Individual 2 eating wax worms. f, Individual 2 eating wax worms. Titles of plots match trial names at http://xmaportal.org/webportal/. Source data

  9. Extended Data Fig. 9 Left (working side) temporomandibular joint rotations and mean muscle lengths.

    Euclidean distance between muscle attachment sites as determined on the basis of contrast-enhanced computed-tomography scans (means taken for all fibres modelled per muscle), for a sequence of individual 1 eating wax worms. Representative of two trials from one opossum; muscle fibres were not reconstructed for individual 2. Muscle colours correspond to those in Figs. 13. Title of the plots matches trial name at http://xmaportal.org/webportal/. Source data

Supplementary information

  1. Supplementary Information

    Supplementary information (methods, calculations, Supplementary Table 1, and references). Contains detailed information regarding methods, additional data and calculations regarding variation among trials, and extended description of motions at the temporomandibular joint (TMJ).

  2. Reporting Summary

  3. Video 1

    Chewing sequence, lateral view. Slowed 10x. Muscle fiber colours correspond to those in Fig. 1.

  4. Video 2

    Chewing sequence, posteroventral view. Slowed 10x. Muscle fiber colours correspond to those in Fig. 1.

  5. Video 3

    Dorsal view of the cranium throughout a chewing sequence, highlighting the attachments of the superficial masseter (cyan) and medial pterygoid (light green). Slowed 10x. See also Fig. 4.

  6. Video 4

    Medial view of left first molar pair throughout a chewing sequence. Slowed 10x.

  7. Video 5

    Posteromedial view of the left molars throughout a chewing sequence, highlighting the paths of protocones. Slowed 10x. Colouring conventions match those in Fig. 4b-c.

  8. Video 6

    Posterior view of the left first molar pair throughout a chewing sequence, highlighting the path of the lower molar relative to a fixed upper molar. Slowed 10x. Colouring conventions match those in Fig. 4b-d and 5a-b.

Source data

  1. Source Data Fig. 2

  2. Source Data Fig. 3

  3. Source Data Extended Data Fig. 6

  4. Source Data Extended Data Fig. 7

  5. Source Data Extended Data Fig. 8

  6. Source Data Extended Data Fig. 9

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DOI

https://doi.org/10.1038/s41586-019-0940-x

Fig. 1: Conservation of ancestral therian features in the skull of Monodelphis.
Fig. 2: Summary of temporomandibular joint kinematics.
Fig. 3: The rotational grinding stroke and occlusion along the tooth row.
Fig. 4: Evolution of mammalian jaw morphology and kinematics.
Extended Data Fig. 1: Geometric morphometric analysis of mammaliaform mandibles, showing the results of principal component analysis of dentary shape.
Extended Data Fig. 2: Phylogenetic framework for geometric morphometric analysis of mammaliaform mandibles.
Extended Data Fig. 3: Condylar regions of mammaliaform dentaries.
Extended Data Fig. 4: Typical chewing sequence, shown in anterolateral view.
Extended Data Fig. 5: Marker sites and details of occlusal kinematics.
Extended Data Fig. 6: Temporomandibular joint rotations during five additional trials from two opossums.
Extended Data Fig. 7: Left (working side) and right (balancing side) temporomandibular joint rotations and translations for a chewing sequence of individual 1 eating wax worms.
Extended Data Fig. 8: Distance between radiopaque markers in lower canines during six trials from two opossums, demonstrating the mobility of the mandibular symphysis.
Extended Data Fig. 9: Left (working side) temporomandibular joint rotations and mean muscle lengths.

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