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New evidence for mammaliaform ear evolution and feeding adaptation in a Jurassic ecosystem

Abstract

Stem mammaliaforms are forerunners to modern mammals1, and they achieved considerable ecomorphological diversity in their own right2. Recent discoveries suggest that eleutherodontids, a subclade of Haramiyida, were more species-rich during the Jurassic period in Asia than previously recognized3,4,5,6,7,8,9,10,11,12. Here we report a new Jurassic eleutherodontid mammaliaform with an unusual mosaic of highly specialized characteristics1,2,3,4,5,6, and the results of phylogenetic analyses that support the hypothesis that haramiyidans are stem mammaliaforms. The new fossil shows fossilized skin membranes that are interpreted to be for gliding and a mandibular middle ear with a unique character combination previously unknown in mammaliaforms. Incisor replacement is prolonged until well after molars are fully erupted, a timing pattern unique to most other mammaliaforms. In situ molar occlusion and a functional analysis reveal a new mode of dental occlusion: dual mortar–pestle occlusion of opposing upper and lower molars, probably for dual crushing and grinding. This suggests that eleutherodontids are herbivorous, and probably specialized for granivory or feeding on soft plant tissues. The inferred dietary adaptation of eleutherodontid gliders represents a remarkable evolutionary convergence with herbivorous gliders in Theria. These Jurassic fossils represent volant, herbivorous stem mammaliaforms associated with pre-angiosperm plants that appear long before the later, iterative associations between angiosperm plants and volant herbivores in various therian clades.

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Figure 1: Dentition of mammaliaform Vilevolodon diplomylos (Haramiyida, Eleutherodontidae) (BMNH2942 holotype).
Figure 2: Disparate tooth occlusal patterns in haramiyidans.
Figure 3: Transformations of mandibular and middle ear structures among mammaliaforms.

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Acknowledgements

We thank A. Shinya for fossil preparation; S. Bi, S. Gatesy, L. Heaney, H.-J. Li, Z.-J. Gao, T. Martin, B. Patterson, N. Shubin, X.-T. Zheng and C.-F. Zhou for access to comparative specimens. Funding supported Q.-J.M. (Beijing Scientific Commission) and Z.-X.L. (UChicago-BSD). Full acknowledgments are provided in the Supplementary Information.

Author information

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Authors

Contributions

Q.-J.M. and Z.-X.L. conceived the project; Q.-J.M., Y.-G.Z., D.L. and Q.J. acquired fossils and studied stratigraphy; all authors were involved in lab fossil work and interpretation; Z.-X.L. and D.M.G. did phylogenetic analyses; A.I.N. scanned and prepared graphics of fossils; Z.-X.L. composed figures; Z.-X.L., Q.-J.M. and D.M.G. led the writing, with feedback from all authors.

Corresponding authors

Correspondence to Zhe-Xi Luo or Qing-Jin Meng.

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The authors declare no competing financial interests.

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Reviewer Information Nature thanks G. Rougier and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Figure 1 Mammaliaform Vilevolodon diplomylos (Haramiyida, Eleutherodontidae) holotype (Beijing Museum of Natural History PM002942).

a, b, BMNH2942A (main slab). Skeletal feature identification, and the outline of the carbonized patagial skin membranes (indicated by red arrows). c, d, BMNH2942B (counterpart). The outline of the carbonized patagial membranes: propatagium, plagiopatagium and uropatagium (indicated by red arrows), and their anatomical relationship to skeleton. e, Partial cranial roof and facial bones preserved on BMNH2942B, extracted by computed tomography (CT) scans and 3D rendering. e1, M2 from counterpart BMNH2942B, in occlusal view. f, Right pes preserved on counterpart, with ventral view of tarsals and approximately lateral views of digit long bones (metatarsal 1 and digit 1 phalanges are not preserved).

Extended Data Figure 2 Vilevolodon skull on holotype main part (BMNH2942A).

a, Stereo pair photographs of skull structures after preliminary preparation. be, CT scan rendering of BMNH2942A, viewed from the partially exposed top side of the skull. Dark green indicates bones segmented from counterpart BMNH2942B. b, Intact left zygoma. c, Stereo images of the skull with left zygoma removed to show the rostroventral flexion of maxillary and the premolar–molar row. d, Unexposed underside of the skull of BMN2942A visualized by CT segmentation, with right mandible in place. e, Stereo images of the skull with right mandible removed to show rostroventral flexion of right maxillary and its tooth row. ** indicates the irregular depression on the mandible formed by underlying massive tooth roots; but it is not a muscle fossa. Detailed analysis of the ear is provided in Extended Data Fig. 8, and comparative morphology in Extended Data Figs 8 and 9.

Extended Data Figure 3 Vilevolodon mandible and teeth on holotype main part (BMNH2942A).

Skull bones removed to expose the roots of upper teeth. a, CT scan rendering of BMNH2942A, viewed from the partially exposed top side of the skull; the intact occlusion of right upper and lower molars. Left dentary condyle and coronoid were preserved on the counterpart, helping to expose the full middle ear. b, CT rendering of the unexposed underside of the skull. c, Top side of the skull of BMNH2942A. The left mandible composite from the coronoid process and dentary condyle segmented from CT scans of the BMNH2942B counterpart. The left petrosal, the occipital and cervicals rendered invisible to highlight the relationship of middle ear to the mandible.

Extended Data Figure 4 Vilevolodon dentition.

a, Right upper teeth in lingual view. The dashed line shows the en echelon or step-wise pattern occlusal surfaces along the upper tooth row, a plesiomorphy of haramiyidans. b, Right upper teeth in ventral view (stereo pair photographs) with black arrows indicating successive lingual imbrication of M1 and M2. c, Left upper teeth (stereo pair photos). Note that M2 was compressed in fossilization. d, Left upper teeth in labial view (stereo pair photos). The dashed line indicates P3–P4 flexure. e, Exposed left lower teeth: first generation deciduous lower incisor 1 (di-1a), second generation deciduous incisor 1 (i-1b), ultimate premolar P4 and M1 extracted from BMNH2942A. The M2 was extracted from BMNH2942B. f, Left lower teeth (stereo pair photos) in occlusal view. Note the roots of deciduous incisors are entirely medial to roots of premolar or molars. The M2 was extracted from BMNH2942B, and all other teeth are from BMNH2942A. g, Right lower M2 from BMNH2942B. h, Right lower M2 (stereo images, occlusal view). i, Right lower teeth (stereo images) in occlusal view from BMNH2942A. j, Right lower teeth in medial view. Bones removed digitally to expose tooth roots and the unerupted replacing incisors, highlighting the prolonged replacement of incisors relative to the adult premolars and molars.

Extended Data Figure 5 Dual mortar–pestle occlusion of Vilevolodon molars, in contrast to embrasure occlusion of Haramiyavia.

a, Vilevolodon right mandible in oblique posterior view, highlighting the M2/M2 orientation and the attachment of the mandibular middle ear. b, Cusp pattern of upper molars (in translucent outline). Note that M2 is imbricated more lingually to M1. c, Cusp pattern of lower molars. Note that M2 is imbricated more lingually to M1, mirroring the imbrication of upper M2 to M1. d, Superimposition of upper M1–M2 (translucent outline) over lower M1–M2 (grey) for dual mortar–pestle occlusion of the upper and lower molars (see also Fig. 3). e, Oblique posterior view of right M2 and M2 in dual mortar–pestle occlusion: A1 cusp (A1 pestle) entering the M2 basin and the A1 cusp (A1 pestle) entering the M2 basin. f, Dual mortar–pestle occlusion of left M2 and M2 (solid surface models) in occlusal views. g, Dual mortar–pestle occlusion of right M2 and M2 surface models in medial (lingual) view (g1), posterior (distal) view (g2), lateral (labial) view (g3), and anterior (mesial) view (g4). h, Occlusion of right lower M1–M2 to right upper M1–M2 in lingual view, based on the best fit of opposing teeth. Note that the B4–B3 cusps of upper molars are always lingual to the lower lingual cusp row, but the B1 cusp is always labial to lower lingual cusp row and in the lower median furrow. i, Occlusion of right M1–M2 to right M1–M2 in labial view. Note that cusp A4 of the upper molar is always labial (lateral) to cusp A1 of the lower molar. The upper labial row A1–A4 occludes obliquely over lower labial row B1–B4. There is no longitudinal alignment of cusp rows between the opposite upper and lower teeth, as in Thomasia, Haramiyavia and Maiopatagium (Fig. 3). j, Haramiyidan Haramiyavia occlusal trajectory (blue, orthal occlusion; green, palinal movement). k, Haramiyavia: transition of orthal phase (blue) to palinal phase (green) occlusion. Cusp row A1–A4 of the lower molar is lingual to cusp row B1–B5 of the upper molars. l, Haramiyavia: full orthal occlusion of M3 with A1 cusp in embrasure between upper M2–M3, and cusp row A1–A4 lingual to cusps B1–B5.

Extended Data Figure 6 Autapomorphic occlusal features of Vilevolodon, including two inferred cycles of the molar occlusal movement.

The upper tooth row has four teeth and is longer than the lower tooth row of three teeth. The upper P3–P4 flexure forms a prominent angle of the occlusal planes between the two premolars. In cycle 1 when lower M1–M2 is able to make full contact with M1–M2, P4 and P3 have no contact. In cycle 2, P4/P3 can make full contact, and their occlusion occurs only during cycle 2. But during this cycle, when the primary cusp of the P4 makes full occlusal contact with P3, the lower M1 and M2 can only barely contact the upper M1 and M2 and cannot make full contact. Occlusal movement was simulated by animation of STL models (see Supplementary Video 1) and inferred by maximal fit of upper and lower tooth occlusal surfaces. Blue arrows indicate the path of cusp A1 of the lower premolar. The blue band in the central column shows the differences in the position of maximum intercuspation (centric occlusion of the P4 primary cusp) between cycle 1 (above) and cycle 2 (below).

Extended Data Figure 7 Dental and mandibular morphologies of eleutherodontids and extant frugivorous bats Sturnira and Artibeus (Chiroptera, Phyllostomidae), Hypsignathus (Megachiroptera: Pteropodidae), and frugivorous/omnivorous primate Daubentonia.

ac, Vilevolodon left M2 (a) and left P4 (b, c). df, Lower teeth of frugivorous bats: Sturnira lilium lilium (FMNH105870) (d); Artibeus jamaicensis (FMNH30776) (e); and Hypsignathus monstrosus (University of Chicago Biological Sciences Division Teaching Collection) (f). g, Megaconus right mandible in lateral view, highlighting the zigzag tooth row profile9. h, Vilevolodon right mandible in lateral view, highlighting the zigzag tooth row profile. i, Hypsignathus mandible in lateral view. j, Artibeus mandible in lateral view, highlighting the zigzag tooth row profile. k, Primate Daubentonia (FMNH15529) right mandible in lateral view. a, df, Similarities of lower molars of Vilevolodon with the basined lower molar talonids of frugivorous bats Artibeus, Sturnira and Hypsignathus. Eleutherodontids are particularly similar to the highly creased talonid basins of Artibeus, whereas Maiopatagium is more similar to Sturnira and pteropodid bats in molar pattern. b–e, f, Similarities of lower premolar of Vilevolodon to those of Sturnira and Hypsignathus. g, h, Similarity of the zigzag tooth row profile of lower premolars and molars of Megaconus and eleutherodontids to those of frugivorous bats. g, h, k, Similarity in mandibles of eleutherodonts and the primate Daubentonia (FMNH15529), which is frugivorous and insectivorous.

Extended Data Figure 8 Vilevolodon middle ear structure preserved in holotype (BMNH2942) and interpretive reconstruction.

a, BMNH2942A in approximately ventral view. External and exposed aspect of left petrosal (partial) and middle ear bones as preserved. The dentary and cervical vertebrae are digitally removed so that the view of the middle ear features is unobstructed. b, BMNH2942A ‘internal’ view (underside of the fossil in matrix), showing the petrosal (partially segmented) and middle ear bones. c, Interpretative reconstruction of the middle ear bones of Vilevolodon, based on middle ear bones exposed in CT scans and 3D segmentation. d, A composite reconstruction of the middle ear of eutriconodonts. e, Cynodont Kayentatherium (redrawn from ref. 30). f, Pre-mammaliaform cynodont Cynognathus middle ear (redrawn from ref. 31) Note 1 to readers: the gracile ectotympanic (reflected lamina of angular), and this gracile and relatively straight morphology is similar to the reflected lamina of several non-mammalian cynodonts. The angle of attachment to the anterior–posterior limbs of ectotympanic (homologue of the angular) is slightly distorted by fossilization. Notes 2 and 3 to readers: the manubrial portion of the malleus (Note 2) is partly attached to the malleus body (Note 3), but there is a gap between these two structures owing to imperfect preservation. Note 4: the posterior end of Meckel’s cartilage is attached to a large sliver of bone. The latter is tentatively interpreted to be a surangular, which in non-mammalian cynodonts is typically parallel to the gonial part (the prearticular) of the malleus (although separated from the latter). There appears to be a suture between the prearticular part of the malleus, and the putative surangular. We infer that the Meckel’s cartilage and the ectotympanic, as preserved in close association, contact each other loosely. But they became slightly separated from each other during fossilization. We reconstructed these two elements as contiguous, as in cynodonts and other mammaliaforms, as demonstrated in c.

Extended Data Figure 9 Comparative morphology of the mandibles and partial mammalian middle ears of extinct Mesozoic mammaliaforms.

a, Morganucodon and several mammaliaforms possess plesiomorphic mandibular middle ear of cynodonts (MMEC). The ectotympanic (homologue of the angular) is nestled in the angular concavity of the mandible. The surangular and the gonial part (homologue of the prearticular) of the malleus make full contact with a broad postdentary trough that extends posteriorly to near the dentary condyle under the medial ridge. The Meckel’s element (ossified cartilage) starts from the postdentary trough, passes anteriorly below the mandibular foramen, and extends further anteriorly into a long Meckel’s sulcus below the mandibular tooth row. b, Eleutherodontid Vilevolodon shows a mandibular connection of the middle ear, although much more reduced (antero-posteriorly shortened) than those of other mammaliaforms. The anterior limb of the ectotympanic and the gonial part (prearticular) of the malleus are nestled in a reduced postdentary trough on the internal aspect of the inflected mandibular angle. The groove occupies the identical position of the postdentary trough in the angular region of other mammaliaforms. However, it is narrower and much shorter than the postdentary trough of other mammaliaforms. The trough is shorter (an apomorphic trait) and does not extend posteriorly to the dentary condyle, in contrast to the postdentary trough in other mammaliaforms. The short and tapering Meckel’s cartilage ends below the mandibular foramen, but it does not extend further anteriorly to the mandibular body below the tooth row. The Meckel’s element and its corresponding Meckel’s sulcus are much shorter than those of other mammaliaforms, eutriconodonts and spalacotherioids. The gonial portion of the malleus (and the putative surangular) also contacts the ventral margin of the mandible. We infer that, in Vilevolodon, the ectotympanic (retroarticular process) and the manubrial part of the malleus are rotated medially and horizontally, away from the mandible (b3), as in eutriconodonts. c, Eutriconodont Yanoconodon, highlighting the massive ossified Meckel’s cartilage that connects the middle ear to the mandible. Owing to the curvature and mid-length bending of Meckel’s element, the ectotympanic and malleal manubrium rotated medially and away from the mandible32.

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Supplementary information

Supplementary Information

This file contains Supplementary Information parts A-Q.

Reporting Summary

Video 1: Analysis of tooth occlusion of Vilevolodon by animation of STL tooth models from CT scan

Part 1: Comparison of distinctive cycle 1 versus cycle 2 of premolars and molars: cycle 1 has full contacts of molars and incisors, but no contact between P3/p4; cycle 2 has full contact of P3/p4 but minimal or no contacts of molars and incisors. Part 2: Molar cusp and basin identification, and cycle 1 of occlusal movement of M1/m1 and M2/m2 during (see Fig. S6). During occlusal cycle 2, the P3/p4 are the only teeth that can fully occlude; the dual mortar-pestle contacts of upper and lower molars do not occur. Thus, cycle 2 is not shown here in animation analysis Part 2 of the video. For better clarity, the un-erupted deciduous incisors are not shown in the video.

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Luo, ZX., Meng, QJ., Grossnickle, D. et al. New evidence for mammaliaform ear evolution and feeding adaptation in a Jurassic ecosystem. Nature 548, 326–329 (2017). https://doi.org/10.1038/nature23483

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