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Transitional mammalian middle ear from a new Cretaceous Jehol eutriconodont



The transference of post-dentary jaw elements to the cranium of mammals as auditory ossicles is one of the central topics in evolutionary biology of vertebrates. Homologies of these bones among jawed vertebrates have long been demonstrated by developmental studies; but fossils illuminating this critical transference are sparse and often ambiguous. Here we report the first unambiguous ectotympanic (angular), malleus (articular and prearticular) and incus (quadrate) of an Early Cretaceous eutriconodont mammal from the Jehol Biota, Liaoning, China. The ectotympanic and malleus have lost their direct contact with the dentary bone but still connect the ossified Meckel’s cartilage (OMC); we hypothesize that the OMC serves as a stabilizing mechanism bridging the dentary and the detached ossicles during mammalian evolution. This transitional mammalian middle ear narrows the morphological gap between the mandibular middle ear in basal mammaliaforms and the definitive mammalian middle ear (DMME) of extant mammals; it reveals complex changes contributing to the detachment of ear ossicles during mammalian evolution.

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Figure 1: The skeleton of the new mammal Liaoconodon hui (dorsal view of the holotype, IVPP V16051, Institute of Vertebrate Paleontology and Paleoanthropology, Beijing).
Figure 2: Skull and ear ossicles of Liaoconodon hui (IVPP V16051).
Figure 3: Morphological transference of mammalian middle ear.
Figure 4: Phylogeny of mammaliaforms (simplified after ref. 18 ) mapping distributions of the post-dentary trough and the Meckelian groove.


  1. Hopson, J. A. The origin of the mammalian middle ear. Am. Zool. 6, 437–450 (1966)

    Article  CAS  Google Scholar 

  2. Allin, E. F. Evolution of the mammalian middle ear. J. Morphol. 147, 403–438 (1975)

    Article  CAS  Google Scholar 

  3. Maier, W. Phylogeny and ontogeny of mammalian middle ear structures. Neth. J. Zool. 40, 55–75 (1990)

    Article  Google Scholar 

  4. Allin, E. F. & Hopson, J. A. in The Evolutionary Biology of Hearing (eds Webster, D. B., Fay, R. R. & Popper, A. N.) 587–614 (Springer, 1992)

    Book  Google Scholar 

  5. Clack, J. A. & Allin, E. F. in Evolution of the Vertebrate Auditory System (eds Manley, G. A., Popper, A. N. & Fay, R. R. ) 128–163 (Springer, 2004)

    Book  Google Scholar 

  6. 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)

    Google Scholar 

  7. Reichert, C. Über die Visceralbogen der Wirbeltiere im Allgemeinen und deren Metamorphosen bei den Vögeln und Säugetieren. Arch. Anat. Physiol. Medizin 1837, 120–222 (1837)

    Google Scholar 

  8. Gaupp, E. Die Reichertsche Theorie (Hammer-, Amboss- und Kieferfrage). Arch. Anat. Entwick. 1912, 1–416 (1913)

    Google Scholar 

  9. Goodrich, E. S. Studies on the Structure and Development of Vertebrates (Macmillan, 1930)

    Book  Google Scholar 

  10. Kermack, K. A., Mussett, F. & Rigney, H. W. The lower jaw of Morganucodon . Zool. J. Linn. Soc. 53, 87–175 (1973)

    Article  Google Scholar 

  11. Kermack, K. A., Mussett, F. & Rigney, H. W. The skull of Morganucodon . Zool. J. Linn. Soc. 71, 1–158 (1981)

    Article  Google Scholar 

  12. Kielan-Jaworowska, Z., Cifelli, R. L. & Luo, Z.-X. Mammals from the Age of Dinosaurs—Origins, Evolution, and Structure (Columbia Univ. Press, 2004)

    Book  Google Scholar 

  13. Zeller, U. Die Entwicklung und Morphologie des Schädels von Ornithorhynchus anatinus (Mammalia: Prototheria: Monotremata). Abhandl. Senckenberg. Natur. Gesell. 545, 1–188 (1989)

    Google Scholar 

  14. Zeller, U. in Mammal Phylogeny Vol. 1 (eds Szalay, F. S., Novacek, M. J. & McKenna, M. C. ) 95–107 (Springer, 1993)

    Book  Google Scholar 

  15. Mallo, M. Formation of the middle ear: recent progress on the developmental and molecular mechanisms. Dev. Biol. 231, 410–419 (2001)

    Article  CAS  Google Scholar 

  16. Wang, Y.-Q., Hu, Y.-M., Meng, J. & Li, C.-K. An ossified Meckel’s cartilage in two Cretaceous mammals and origin of the mammalian middle ear. Science 294, 357–361 (2001)

    Article  ADS  CAS  Google Scholar 

  17. Meng, J. Hu, Y.-M., Wang, Y.-Q. & Li, C.-K. The ossified Meckel’s cartilage and internal groove in Mesozoic mammaliaforms: implications to origin of the definitive mammalian middle ear. Zool. J. Linn. Soc. 138, 431–448 (2003)

    Article  Google Scholar 

  18. Luo, Z.-X., Chen, P.-J., Li, G. & Chen, M. A new eutriconodont mammal and evolutionary development in early mammals. Nature 446, 288–293 (2007)

    Article  ADS  CAS  Google Scholar 

  19. Takechi, M. & Kuratani, S. History of studies on mammalian middle ear evolution: a comparative morphological and developmental biology perspective. J. Exp. Zool. B 314, 1–17 (2010)

    Google Scholar 

  20. Rowe, T. B. Coevolution of the mammalian middle ear and neocortex. Science 273, 651–654 (1996)

    Article  ADS  CAS  Google Scholar 

  21. He, H.-Y. et al. Timing of the Jiufotang Formation (Jehol Group) in Liaoning, northeastern China, and its implications. Geophys. Res. Lett. 31, L12605 (2004)

    ADS  Google Scholar 

  22. Ji, Q., Luo, Z.-X. & Ji, S.-A. A Chinese triconodont mammal and mosaic evolution of the mammalian skeleton. Nature 398, 326–330 (1999)

    Article  CAS  Google Scholar 

  23. Li Li, C.-K., Hu, Y.-M., Wang, Y.-Q. & Meng, J. A new species of Gobiconodon (Triconodonta, Mammalia) and its implication for the age of Jehol Biota. Chin. Sci. Bull. 48, 1129–1134 (2003)

    Google Scholar 

  24. Meng, J., Hu, Y.-M., Wang, Y.-Q. & Li, C.-K. A new gobiconodont species (Mammalia) from the Early Cretaceous Yixian Formation of Liaoning, China. Vert. PalAsiatica 43, 1–10 (2005)

    Google Scholar 

  25. Li, J.-L., Wang, Y., Wang, Y.-Q. & Li, C. K. A new family of primitive mammal from the Mesozoic of western Liaoning, China. Chin. Sci. Bull. 45, 2545–2549 (2000)

    Google Scholar 

  26. Hu, Y.-M., Meng, J., Li, C.-K. & Wang, Y.-Q. Large Mesozoic mammals fed on young dinosaurs. Nature 433, 149–153 (2005)

    Article  ADS  CAS  Google Scholar 

  27. Ji, Q., Luo, Z.-X., Zhang, X., Yuan, C.-X. & Xu, L. Evolutionary development of the middle ear in Mesozoic therian mammals. Science 326, 278–281 (2009)

    Article  ADS  CAS  Google Scholar 

  28. McClain, J. A. The development of the auditory ossicles of the opossum (Didelphys virginiana). J. Morphol. 64, 211–265 (1939)

    Article  Google Scholar 

  29. Filan, S. L. Development of the middle ear region in Monodelphis domestica (Marsupialia, Didelphidae): marsupial solutions to an early birth. J. Zool. 225, 577–588 (1991)

    Article  Google Scholar 

  30. Clark, C. T. & Smith, K. K. Cranial osteogenesis in Monodelphis domestica (Didelphidae) and Macropus eugenii (Macropodidae). J. Morphol. 215, 119–145 (1993)

    Article  CAS  Google Scholar 

  31. Sánchez-Villagra, M. R., Gemballa, S., Nummela, S., Smith, K. K. & Maier, W. Ontogenetic and phylogenetic transformations of the ear ossicles in marsupial mammals. J. Morphol. 251, 219–238 (2002)

    Article  Google Scholar 

  32. Meng, J. & Wyss, A. R. Monotreme affinities and low-frequency hearing suggested by multituberculate ear. Nature 377, 141–144 (1995)

    Article  ADS  CAS  Google Scholar 

  33. Fleischer, G. Studien am Skelett des Gehörorgans der Säugetiere, einschliesslich des Menschen. Säugetierk. Mitt. 21, 131–239 (1973)

    Google Scholar 

  34. Fleischer, G. Evolutionary principles of the mammalian middle ear. Adv. Anat. Embryol. Cell Biol. 55, 1–70 (1978)

    Google Scholar 

  35. Henson, O. W. Comparative anatomy of the middle ear. Handbook of Sensory Physiology: The Auditory System Vol. 5, Pt 1 (eds Keidel, W. D. & Neff, W. D. ) 39–110 (Springer, 1974)

    Google Scholar 

  36. Barghusen, H. R. in The Ecology and Biology of Mammalian-like Reptiles (eds Hotton III N., MacLean, P. D., Roth, J. J. & Roth, E. C. ) 253–262 (Smithsonian Institution Press, 1986)

    Google Scholar 

  37. Crompton, A. W. in Studies in Vertebrate Evolution (eds Joysey, K. A. & Kemp, T. S. ) 231–251 (Oliver & Boyd, 1972)

    Google Scholar 

  38. Bensley, B. A. On the identification of Meckelian and mylohyoid grooves in the jaws of Mesozoic and Recent Mammalia. Univ. Toronto Stud. Biol. Ser. 3, 75–81 (1902)

    Google Scholar 

  39. Krebs, B. Evolution of the mandible and lower dentition in dryolestids (Pantotheria, Mammalia). Zool. J. Linn. Soc. 50, (Suppl. 1)89–102 (1971)

    Google Scholar 

  40. 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)

    Google Scholar 

  41. Allin, E. F. in The Ecology and Biology of Mammal-like Reptiles (eds Hotton, N., MacLean, P. D., Roth, J. J. & Roth, E. C. ) 283–294 (Smithsonian Institution Press, 1986)

    Google Scholar 

  42. Kermack, K. A. & Mussett, F. The ear in mammal-like reptiles and early mammals. Acta Palaeontol. Pol. 28, 147–158 (1983)

    Google Scholar 

  43. Presley, R. Lizards, mammals and the primitive tetrapod tympanic membrane. Symp. Zool. Soc. Lond. 52, 127–152 (1984)

    Google Scholar 

  44. Westoll, T. S. The mammalian middle ear. Nature 155, 114–115 (1945)

    Article  ADS  Google Scholar 

  45. Watson, D. M. S. Evolution of the mammalian ear. Evolution 7, 159–177 (1953)

    Article  Google Scholar 

  46. Shute, C. C. The evolution of the mammalian eardrum and tympanic cavity. J. Anat. 90, 261–281 (1956)

    CAS  PubMed  PubMed Central  Google Scholar 

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We thank X.-L. Wang of the Institute of Vertebrate Paleontology and Paleoanthropology for collecting the specimen; S.-H. Xie for preparing the specimen; J. Zhang, W. Gao, X. Jin, F.-C. Zhang and S.-B. Wang for photographs; W.-D. Zhang for scanning electron microscope and X-ray images; and E. Allin, G. Rougier and M. Takechi for discussion. The study was supported by the Major Basic Research Project of the Ministry of Science and Technology, China (2006CB806400), the National Science Foundation of China (40121202), the Special Fund for Fossil Excavation and Preparation of the Chinese Academy of Sciences, and the National Science Foundation of USA (EF-0629811 to J.M.).

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J.M. designed the study, performed the comparative and analytical work and wrote the paper. Y.W. and C.L. provided most of the photographs and contributed to the writing and discussion.

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Correspondence to Jin Meng.

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The authors declare no competing financial interests.

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This file contains Supplementary Sections A-G comprising Systematic Paleontology, Description, Discussion, Supplementary Figures 1-8 with legends, Phylogenetic analyses, Methods and References (see Table of Contents for full list). (PDF 2741 kb)

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Meng, J., Wang, Y. & Li, C. Transitional mammalian middle ear from a new Cretaceous Jehol eutriconodont. Nature 472, 181–185 (2011).

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