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A Jurassic gliding euharamiyidan mammal with an ear of five auditory bones

Naturevolume 551, pages451–456 (2017)Cite this article

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Abstract

Gliding is a distinctive locomotion type that has been identified in only three mammal species from the Mesozoic era. Here we describe another Jurassic glider that belongs to the euharamiyidan mammals and shows hair details on its gliding membrane that are highly similar to those of extant gliding mammals. This species possesses a five-boned auditory apparatus consisting of the stapes, incus, malleus, ectotympanic and surangular, representing, to our knowledge, the earliest known definitive mammalian middle ear. The surangular has not been previously identified in any mammalian middle ear, and the morphology of each auditory bone differs from those of known mammals and their kin. We conclude that gliding locomotion was probably common in euharamiyidans, which lends support to idea that there was a major adaptive radiation of mammals in the mid-Jurassic period. The acquisition of the auditory bones in euharamiyidans was related to the formation of the dentary-squamosal jaw joint, which allows a posterior chewing movement, and must have evolved independently from the middle ear structures of monotremes and therian mammals.

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Figure 1: Type specimens ofA. allinhopsoni.
Figure 2: Skull ofA. allinhopsoni (holotype; HG-M017-A).
Figure 3: Close-up views of impressions of fur and gliding membrane inA. allinhopsoni (paratype; HG-M018).
Figure 4: Phylogeny of mammaliaforms with focus on Allotheria.
Figure 5: Comparison of mammaliaform middle ears and jaw joints.

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Acknowledgements

We thank S.-H. Xie for specimen preparation; P.-F. Yin and Y.-M. Hou for computed laminography scanning of the specimens; X.-T. Zheng, X.-L. Wang, H.-J. Li, Z.-J. Gao, X.-H. Ding, and D.-Y. Sun for access to comparative specimens; N. Wong for drawing the auditory bones and animal reconstruction; D. W. Krause and S. Hoffmann for sharing data and insights on incisor identification; D. Sigogneau-Russell and Z.-X. Luo for permissions to use their published figures; and Z.-X. Luo, Z.-H. Zhou, X. Xu, G. Rougier, J. A. Schultz, A. S. Tucker, and M. Takechi for discussions. This work was supported by the National Natural Science Foundation of China (41688103; 41404022) and the Strategic Priority Research Program (B) of the Chinese Academy of Sciences (XDB18000000).

Author information

Authors and Affiliations

  1. Paleontology Center, Bohai University, Jinzhou, 121013, Liaoning Province, China

    Gang Han

  2. Hainan Tropical Ocean University, Sanya, 572022, Hainan Province, China

    Gang Han

  3. Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, PO Box 643, Beijing, 100044, China

    Fangyuan Mao & Yuanqing Wang

  4. Department of Biology, Indiana University of Pennsylvania, Indiana, 15705, Pennsylvania, USA

    Shundong Bi

  5. Division of Paleontology, American Museum of Natural History, New York, 10024, New York, USA

    Jin Meng

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  1. Gang Han

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  2. Fangyuan Mao

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Contributions

G.H. and J.M. conceived the study. G.H. acquired and curated the specimens and did the field investigation. F.M. conducted computed laminography, rendered the data, and did most of the phylogenetic analyses and figures. S.B., Y.W. and F.M. helped to build the character list. J.M. supervised preparation of the specimen and design of the figures and drafted the manuscript; all authors edited and approved the manuscript.

Corresponding authors

Correspondence toFangyuan Mao orJin Meng.

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Extended data figures and tables

Extended Data Figure 1 The type locality and fossil pit where the type specimens ofA. allinhopsoni were collected.

a, Distant view of the fossil locality and Tiaojishan Formation in the area of Nanshimen village, Gangou Town, Qinglong County, Hebei Province, China.b,c, The fossil pits where the type specimens were collected. The blue arrow in c points to the bed that generated the holotype and paratype. All photographs were taken by G.H. SeeSupplementary Information for more discussion on the age constraints of the beds and the fauna.

Extended Data Figure 2 The holotype specimen (HG-M017) ofA. allinhopsoni.

The specimen preserves most of the skull, dentition, vertebral column and impressions of the gliding membrane and fur (dark colour).a, The main part of the holotype (HG-M017-A), in which the skull and vertebral column are exposed in their dorsal views (see alsoFigs 2,3;Extended Data Fig. 4).b, The counterpart of the holotype (HG-M017-B), which preserves most of the limb structures and the molds of the vertebral column preserved in the main part. The limbs are exposed primarily in their ventral views (see alsoExtended Data Fig. 6). Red arrows point to ribs (1–13); white arrows mark the exposed edges of the gliding membrane.

Extended Data Figure 3 The paratype specimen (HG-M018) ofA. allinhopsoni.

a, The main part of the paratype (HG-M018-A), which shows the ventral view of the skeleton (mainly the thoracic and lumbar vertebra) and impressions of the gliding membrane and body fur.b, The counterpart of the paratype (HG-M018-B). Skeletal remains preserved in the counterpart (peeled off from the main part) are mainly in the dorsal view. The skull was broken during excavation and reconstructed afterward; this area is outlined with a white dashed line to caution against potential misunderstanding of the morphology. The shape of the gliding membrane and impressions of hair are well preserved in the paratype and the exposed edge is marked by white arrows (see alsoFig. 3;Extended Data Fig. 6a, b). The red arrows ina point to bony spurs2. The red arrows inb point to the ribs; 12 ribs can be recognized, but we assume there are a total of 13 ribs, as in the holotype specimen.c, Reconstruction of the animal in gliding motion.

Extended Data Figure 4 Dentition ofA. allinhopsoni (holotype, HG-M017).

a, Part of the skull with exposed teeth (HG-M017-A).b, Counterpart of the skull part ina.c, Part of the skull with teeth (HG-M017-A). This was prepared from the back side of the main slab.d, Computed laminography image that roughly corresponds to the area shown inc, revealing teeth within the maxilla and blocked by bones.e, Close-up view showing the occlusal relationship of M1 and m1. As inA. jenkinsi and other euharamiyidans1,2,3,4,56, the ‘double engaged’ occlusal pattern is clear: the distolabial main cusp A1 of M1 bites in the basin of m1, whereas the mesiolingual main cusp a1 of m1 occludes in the basin of M1.f, Computed laminography image showing the incisor germ within each jaw bone, located dorsal to the root of the enlarged incisor. a1l, Cusp a1 on left first lower molar; amf, anterior extremity of the masseteric fossa; b1l–b3l, Cusps b1, b2 and b3 on left first lower molar; dlp4, distal portion of left lower fourth premolar; lA1, A1 cusp of left first upper molar (it bites in the basin of m1); lA2, A2 cusp of left first upper molar (small cusp may exist between A1 and A2); ldI2, left second deciduous upper incisor; ldi, left deciduous lower incisor; ldii, left deciduous lower incisor impression; lig, left lower incisor tooth germ (successive incisor); lm1, left first lower molar; lM1, left first upper molar; lm2, left second lower molar; lM2, left second upper molar; lP3, left third upper premolar; lP4, left fourth upper premolar; mf, masseteric fossa; mlp4, mesial portion of left fourth lower premolar; plP4, partial left fourth upper premolar; rl2g, germ of right second upper incisor; rdI2, right second deciduous upper incisor; rdi, right deciduous lower incisor; rig, right lower incisor (successive) tooth germ; rldI2, root of second left upper deciduous incisor; rlM1, root of left first molar; rlP3, root of left their upper premolar; rm1, right first lower molar; rM1, right first upper molar; rm2, right second lower molar; rM2, right second upper molar; rP3, right third upper premolar; rp4, right fourth lower premolar; rP4, right fourth upper premolar; rrdi, root of right lower deciduous incisor; tldi, tip of left lower deciduous incisor.

Extended Data Figure 5 Auditory apparatus ofA. allinhopsoni (holotype, HG-M017).

a, Close-up view of the ear region (mostly left side) that corresponds to the boxed area inFig. 2.b, Computed laminography image of the ear region.c, Computed laminography image showing the extension of the anterior process of the surangular.d, Computed laminography image showing the extension of the anterior process of the malleus.e, Interpretive drawing of the auditory bones (ventral view) with the stapes and incus moved out and the surangular overlapping with the malleus.f, Interpretative drawing of the auditory bones (dorsal view) with interpreted articulation of the incus and the malleus. Because the malleus, surangular and ectotympanic were slightly displaced from their anatomical positions, the reconstruction may not reflect the precise bone relationship. apm, anterior process of the malleus (prearticular); asa, anterior process of the surangular; br, breakage in the anterior process of the surangular; fv, fenestra vestibuli; gf, glenoid fossa; hy, hyoid element; ic, incus; lp, lenticular process; ma, malleus; mm, manubrium of the malleus; mp, medial process of the malleus; oc, occipital condyle; pf, perilymphatic foramen; pic, stapedial process of the incus; pism, process for insertion of the stapedius muscle of the stapes; pm, promontorium; ppr, paroccipital process; ptp, posttympanic process of the squamosal; rtm, ridge for attachment of the anterior part of the tympanic membrane; sa, surangular; sf, stapedius fossa; spg, groove for the stapedial artery; st, stapes; tm, transverse part of the malleus; ty, ectotympanic; ty-d, lateral ectotympanic part presumably equivalent to the dorsal part of the angular; ty-r, ectotympanic part presumably equivalent to the reflected lamina.

Extended Data Figure 6 Limbs and gliding membrane ofA. allinhopsoni.

a,b, Close-up views showing the relationship of the limbs and the gliding membrane (paratype, HG-M018-A). Note that the forelimbs and hind limbs were flexed so that the gliding membrane is not preserved in its fully extended size.c,d, Close-up views showing the relationship of the limbs and the gliding membrane (holotype specimen, HG-M017). pl, plagiopatagium, the primary gliding membrane that extends between the forelimbs and hind limbs; pr, propatagium, the gliding membrane between the neck and forelimbs; ur, uropatagium, the gliding membrane between the hind legs and the tail.

Extended Data Figure 7 Manual and pedal structure and ternary diagrams showing the intrinsic ray III proportions.

a, The manus in ventral view.d, The pes in ventral view.a andb are from the holotype, HG-M017-B. As in other euharamiyidans1,2,3,4, the metapodials are short, whereas the phalanges are proportionally elongate.c,d, Ternary plots showing the relative lengths of the metapodial, proximal and intermediate phalanges for digit III of the manus and pes. The lengths of those elements are shown on their respective axes as a percentage of the combined length of the three segments. As in other euharamiyidans8,9,A. allinhopsoni has a similar intrinsic manual and pedal ray proportion, which is typical of arboreal species in which the phalanges are long relative to the metapodials. In addition to the extant taxa, fossils involved in the plotting are: Ara,A. allinhopsoni; Arj,A. jenkinsi. Eo,Eomaia scansoria; Je,Jeholodens jenkinsi; Ma,Maotherium sinensis; Sb,Sinobaatar lingyuanensis; Sd,Sinodelphys szalayi; Sh,Shenshou; Xl,X. linglong; Xs,Xianshou songae. The plotting data are derived from previous studies1,2.

Extended Data Figure 8 Results of phylogenetic analyses based on dataset I (Vintana A).

a, Strict consensus tree resulted from parsimony-based analysis using PAUP*: tree length, 2,637; consistency index (CI), 0.3250; homoplasy index (HI), 0.6750; retention index (RI), 0.7895; rescaled consistency index (RC), 0.2566.b, Result of Bayesian analysis (50% majority-rule consensus) obtained from five million MCMC generations with burn-in fraction of 0.25. Node support given as posterior probabilities. See Methods andSupplementary Information for more details. In extant mammals, gliding locomotion has evolved independently in marsupials, rodents, and dermopterans12,14, but they are not all illustratable.

Extended Data Table 1 Measurements (in mm) of the type specimens ofA. allinhopsoni

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Han, G., Mao, F., Bi, S.et al. A Jurassic gliding euharamiyidan mammal with an ear of five auditory bones.Nature551, 451–456 (2017). https://doi.org/10.1038/nature24483

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Editorial Summary

Ancient glider lends an ear bone or two

The haramiyids were a group of mammals living in the age of dinosaurs that seem to have had a penchant for gliding, rather like flying squirrels of today. Two newly described species of gliding haramiyids were presented recently and now Jin Meng and colleagues follow with another. The new species lived in China in the Jurassic period between 164 and 159 million years ago and shows many intriguing features in addition to its adaptations for gliding. Its middle ear, for example, represents an interesting way-station in the evolution of the mammalian middle ear, which today is made up of three ossicles (the stapes, malleus and incus). It appears that the surangular of the jaw and the ectotympanic of the skull joined the trio of bones to form a hitherto unseen five-ossicle system.

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