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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Zheng, X., Bi, S., Wang, X. & Meng, J. A new arboreal haramiyid shows the diversity of crown mammals in the Jurassic period. Nature 500, 199–202 (2013)
Bi, S., Wang, Y., Guan, J., Sheng, X. & Meng, J. Three new Jurassic euharamiyidan species reinforce early divergence of mammals. Nature 514, 579–584 (2014)
Meng, Q. J. et al. New gliding mammaliaforms from the Jurassic. Nature 548, 291–296 (2017)
Luo, Z. X. et al. New evidence for mammaliaform ear evolution and feeding adaptation in a Jurassic ecosystem. Nature 548, 326–329 (2017)
Fox, R. C. & Meng, J. An X-radiographic and SEM study of the osseous inner ear of multituberculates and monotremes (Mammalia): implications for mammalian phylogeny and evolution of hearing. Zool. J. Linn. Soc. 121, 249–291 (1997)
Kielan-Jaworowska, Z ., Cifelli, R. L. & Luo, Z.-X. Mammals from the Age of Dinosaurs: Origins, Evolution, and Structure (Columbia Univ. Press, 2004)
Meng, J., Bi, S., Zheng, X. & Wang, X. Ear ossicle morphology of the Jurassic euharamiyidan Arboroharamiya and evolution of mammalian middle ear. J. Morphol. http://doi.org/10.1002/jmor.20565 (2016)
Wible, J. R. Origin of Mammalia: the craniodental evidence reexamined. J. Vertebr. Paleontol. 11, 1–28 (1991)
Doran, A. H. G. Morphology of the mammalian ossicular auditûs. Trans. Linn. Soc. Lond 1, 371–497 (1878)
Fleischer, G. Studien am Skelett des Gehörorgans der Säugetiere, einschließlich des Menschen. Saugetierkdl. Mitt. 21, 131–239 (1973)
Zeller, U. in Mammal Phylogeny: Mesozoic Differentiation, Multituberculates, Monotremes, Early Therians, and Marsupials (eds Szalay, F. S., Novacek, M. J. & McKenna, M. J. ) 95–107 (Springer, 1993)
Jackson, S . & Schouten, P. Gliding Mammals of the World (CSIRO, 2012)
Johnson-Murray, J. L. The comparative myology of the gliding membranes of Acrobates, Petauroides and Petaurus contrasted with the cutaneous myology of Hemibelideus and Pseudocheirus (Marsupialia: Phalangeridae) and with selected gliding Rodentia (Sciuridae and Anamoluridae). Aust. J. Zool. 35, 101–113 (1987)
Jackson, S. M. & Thorington, R. W. Jr. Gliding mammals: taxonomy of living and extinct species. Smithson. Contrib. Zool. 638, 1–117 (2012)
Luo, Z.-X., Yuan, C.-X., Meng, Q.-J. & Ji, Q. A Jurassic eutherian mammal and divergence of marsupials and placentals. Nature 476, 442–445 (2011)
Meng, J., Wang, Y. & Li, C. Transitional mammalian middle ear from a new Cretaceous Jehol eutriconodont. Nature 472, 181–185 (2011)
Krause, D. W. et al. First cranial remains of a gondwanatherian mammal reveal remarkable mosaicism. Nature 515, 512–517 (2014)
Luo, Z.-X., Gatesy, S. M., Jenkins, F. A. Jr, Amaral, W. W. & Shubin, N. H. Mandibular and dental characteristics of Late Triassic mammaliaform Haramiyavia and their ramifications for basal mammal evolution. Proc. Natl Acad. Sci. USA 112, E7101–E7109 (2015)
Hahn, G. Neue Zähne von Haramiyiden aus der deutschen Ober-Trias und ihre Beziehungen zu den Multituberculaten. Palaeontogr. Abt. A 142, 1–15 (1973)
Jenkins, F. A., Jr, Gatesy, S. M., Shubin, N. H. & Amaral, W. W. Haramiyids and Triassic mammalian evolution. Nature 385, 715–718 (1997)
Allin, E. F. Evolution of the mammalian middle ear. J. Morphol. 147, 403–437 (1975)
Allin, E. F. & Hopson, J. A. in The Evolutionary Biology of Hearing (eds Webster, D. B., Popper, A. N. & Fay, R. R. ) 587–614 (Springer, 1992)
Rich, T. H. et al. The mandible and dentition of the Early Cretaceous monotreme Teinolophos trusleri. Alcheringa 40, 475–501 (2016)
Presley, R. Lizards, mammals and the primitive tetrapod tympanic membrane. Symp. Zool. Soc. Lond. 52, 127–152 (1984)
Meng, J. & Wyss, A. R. Monotreme affinities and low-frequency hearing suggested by multituberculate ear. Nature 377, 141–144 (1995)
Hurum, J. H., Presley, R. & Kielan-Jaworowska, Z. The middle ear in multituberculate mammals. Acta Palaeontol. Pol. 41, 253–275 (1996)
Rougier, G. W., Wible, J. R. & Novacek, M. J. Middle-ear ossicles of the multituberculate Kryptobaatar from the Mongolian Late Cretaceous: implications for mammaliamorph relationships and the evolution of the auditory apparatus. Am. Mus. Novit. 3187, 1–43 (1996)
Kemp, T. S. Acoustic transformer function of the postdentary bones and quadrate of a nonmammalian cynodont. J. Vertebr. Paleontol. 27, 431–441 (2007)
Kermack, K. A., Mussett, F. & Rigney, H. W. The skull of Morganucodon. Zool. J. Linn. Soc. 71, 1–158 (1981)
Mallo, M. Formation of the middle ear: recent progress on the developmental and molecular mechanisms. Dev. Biol. 231, 410–419 (2001)
Anthwal, N., Joshi, L. & Tucker, A. S. Evolution of the mammalian middle ear and jaw: adaptations and novel structures. J. Anat. 222, 147–160 (2013)
Gaupp, E. Die Reichertsche Theorie (Hammer-, Amboss- und Kieferfrage). Archiv. Anatomie. Entwick 1912, 1–426 (1913)
Maier, W. & Ruf, I. Evolution of the mammalian middle ear: a historical review. J. Anat. 228, 270–283 (2016)
Reichert, C. Über die Visceralbogen der Wirbelthiere im Allgemeinen und deren Metamorphosen bei den Vögeln und Säugethieren. Arch. Anat. Phys. Med. 1837, 120–220 (1837)
Kermack, K. A., Mussett, F. & Rigney, H. W. The lower jaw of Morganucodon. Zool. J. Linn. Soc. 53, 87–175 (1973)
Lillegraven, J. A. & Krusat, G. Cranio-mandibular anatomy of Haldanodon exspectatus (Docodonta; Mammalia) from the Late Jurassic of Portugal and its implications to the evolution of mammalian characters. Contrib. Geol 28, 39–138 (1991)
Crompton, A. W. in Studies in Vertebrate Evolution (eds Joysey, K. A . & Kemp, T. S. ) 231–251 (Oliver & Boyd, 1972)
Crompton, A. W. & Jenkins, F. A. Jr in Mesozoic Mammals: The First Two-thirds of Mammalian History (eds Lillegraven, J. A., Kielan-Jaworowska, Z. & Clemen, W. A. ) 59–73 (Univ. California Press, 1979)
Henson, O. W. Jr. in The Handbook of Sensory Physiology: the Auditory System VII (eds Keidel, W. D. & Neff, W. D. ) 39–110 (Springer, 1974)
Tucker, A. S., Watson, R. P., Lettice, L. A., Yamada, G. & Hill, R. E. Bapx1 regulates patterning in the middle ear: altered regulatory role in the transition from the proximal jaw during vertebrate evolution. Development 131, 1235–1245 (2004)
Crompton, A. W. & Hylander, W. L. in The Ecology and Biology of Mammal-like Reptiles (eds Hotton, N. III, MacLean, P. D., Roth J. J. & Rot E. C. ) 263–282 (Smithsonian Inst. Press, 1986)
Dial, R., Bloodworth, B., Lee, A., Boyne, P. & Heys, J. The distribution of free space and its relation to canopy composition at six forest sites. For. Sci. 50, 312–325 (2004)
Heinicke, M. P., Greenbaum, E., Jackman, T. R. & Bauer, A. M. Evolution of gliding in Southeast Asian geckos and other vertebrates is temporally congruent with dipterocarp forest development. Biol. Lett. 8, 994–997 (2012)
Socha, J. J., Jafari, F., Munk, Y. & Byrnes, G. How animals glide: from trajectory to morphology. Can. J. Zool. 93, 901–924 (2015)
Meng, J., Hu, Y., Wang, Y., Wang, X. & Li, C. A Mesozoic gliding mammal from northeastern China. Nature 444, 889–893 (2006)
Hayssen, V. Patterns of body and tail length and body mass in Sciuridae. J. Mamm. 89, 852–873 (2008)
Dudley, R. et al. Gliding and the functional origins of flight: biomechanical novelty or necessity? Annu. Rev. Ecol. Evol. Syst. 38, 179–201 (2007)
Endo, H., Yokokawa, K., Kurohmaru, M. & Hayashi, Y. Functional anatomy of gliding membrane muscles in the sugar glider (Petaurus breviceps). Ann. Anat. 180, 93–96 (1998)
Luo, Z.-X. Transformation and diversification in early mammal evolution. Nature 450, 1011–1019 (2007)
Grossnickle, D. M . & Polly, P. D. Mammal disparity decreases during the Cretaceous angiosperm radiation. Proc. R. Soc. Lond. B 280, 20132110 (2013)
Meng, J. Mesozoic mammals of China: implications for phylogeny and early evolution of mammals. Natl Sci. Rev. 1, 521–542 (2014)
Close, R. A., Friedman, M., Lloyd, G. T. & Benson, R. B. Evidence for a mid-Jurassic adaptive radiation in mammals. Curr. Biol. 25, 2137–2142 (2015)
Meng, J. & Hou, S.-L. Earliest known mammalian stapes from an early cretaceous eutriconodontan mammal and implications for evolution of mammalian middle ear. Palaeontol. Polonica 67, 181–196 (2016)
Zhou, C.-F., Wu, S., Martin, T. & Luo, Z.-X. A Jurassic mammaliaform and the earliest mammalian evolutionary adaptations. Nature 500, 163–167 (2013)
Yuan, C.-X., Ji, Q., Meng, Q.-J., Tabrum, A. R. & Luo, Z.-X. Earliest evolution of multituberculate mammals revealed by a new Jurassic fossil. Science 341, 779–783 (2013)
Meng, J., Bi, S., Wang, Y., Zheng, X. & Wang, X. Dental and mandibular morphologies of Arboroharamiya (Haramiyida, Mammalia): a comparison with other haramiyidans and Megaconus and implications for mammalian evolution. PLoS One 9, e113847 (2014)
Zhou, Z.-H., Jin, F. & Wang, Y. Vertebrate assemblages from the middle-late Jurassic Yanliao Biota in Northeast China. Earth Sci. Front 17, 252–254 (2010)
Xu, X., Zhou, Z.-H., Sullivan, C., Wang, Y. & Ren, D. An updated review of the Middle-Late Jurassic Yanliao biota: chronology, taphonomy, paleontology and paleoecology. Acta Geol. Sin. (English Edition) 90, 2229–2243 (2016)
Gaetano, L. C. & Rougier, G. W. New materials of Argentoconodon fariasorum (Mammaliaformes, Triconodontidae) from the Jurassic of Argentina and its bearing on triconodont phylogeny. J. Vertebr. Paleontol. 31, 829–843 (2011)
Gaetano, L. C. & Rougier, G. W. First amphilestid from South America: a molariform from the Jurassic Cañadón Asfalto Formation, Patagonia, Argentina. J. Mamm. Evol. 19, 235–248 (2012)
Gurovich, Y. & Beck, R. The phylogenetic affinities of the enigmatic mammalian clade Gondwanatheria. J. Mamm. Evol. 16, 25–49 (2009)
Rowe, T. Definition, diagnosis and origin of Mammalia. J. Vertebr. Paleontol. 8, 241–264 (1988)
O’Leary, M. A. et al. The placental mammal ancestor and the post-K-Pg radiation of placentals. Science 339, 662–667 (2013)
Butler, P. M. Review of the early allotherian mammals. Acta Palaeontol. Pol. 45, 317–342 (2000)
Butler, P. M. & Hooker, J. J. New teeth of allotherian mammals from the English Bathonian, including the earliest multituberculates. Acta Palaeontol. Pol. 50, 185–207 (2005)
Hahn, G. & Hahn, R. Evolutionary tendencies and systematic arrangement in the Haramiyida (Mammalia). Geol. Palaeontol 40, 173–193 (2006)
Averianov, A. O. & Lopatin, A. V. Phylogeny of triconodonts and symmetrodonts and the origin of extant mammals. Dokl. Biol. Sci. 436, 32–35 (2011)
Mao, F.-Y., Wang, Y.-Q., Bi, S.-D., Guan, J. & Meng, J. Tooth enamel microstructures of three Jurassic euharamiyidans and implications for tooth enamel evolution in allotherian mammals. J. Vertebr. Paleontol. 37, e1279168 (2017)
Luo, Z.-X., Schultz, J. A. & Ekdale, E. G. in Evolution of the Vertebrate Ear (eds Clack, J. A., Fay, R. R. & Popper, A. N. ) 139–174 (Springer, 2016)
Swofford, D. L. PAUP* - Phylogenetic analysis Using Parsimony (*and other methods). Version 4 (4.0a152) (Sinauer Associates, 2002)
Ronquist, F. & Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574 (2003)
Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012)
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).
The authors declare no competing financial interests.
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 The type locality and fossil pit where the type specimens of A. 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. See Supplementary Information for more discussion on the age constraints of the beds and the fauna.
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 also Figs 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 also Extended Data Fig. 6). Red arrows point to ribs (1–13); white arrows mark the exposed edges of the gliding membrane.
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 also Fig. 3; Extended Data Fig. 6a, b). The red arrows in a point to bony spurs2. The red arrows in b 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.
a, Part of the skull with exposed teeth (HG-M017-A). b, Counterpart of the skull part in a. 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 in c, revealing teeth within the maxilla and blocked by bones. e, Close-up view showing the occlusal relationship of M1 and m1. As in A. 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.
a, Close-up view of the ear region (mostly left side) that corresponds to the boxed area in Fig. 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.
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 and b 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.
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 and Supplementary Information for more details. In extant mammals, gliding locomotion has evolved independently in marsupials, rodents, and dermopterans12,14, but they are not all illustratable.
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Han, G., Mao, F., Bi, S. et al. A Jurassic gliding euharamiyidan mammal with an ear of five auditory bones. Nature 551, 451–456 (2017). https://doi.org/10.1038/nature24483
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