Abstract
Detachment of the three tiny middle ear bones from the reptilian mandible is an important innovation of modern mammals. Here we describe a Mesozoic eutriconodont nested within crown mammals that clearly illustrates this transition: the middle ear bones are connected to the mandible via an ossified Meckel’s cartilage. The connected ear and jaw structure is similar to the embryonic pattern in modern monotremes (egg-laying mammals) and placental mammals, but is a paedomorphic feature retained in the adult, unlike in monotreme and placental adults. This suggests that reversal to (or retention of) this premammalian ancestral condition is correlated with different developmental timing (heterochrony) in eutriconodonts. This new eutriconodont adds to the evidence of homoplasy of vertebral characters in the thoraco-lumbar transition and unfused lumbar ribs among early mammals. This is similar to the effect of homeobox gene patterning of vertebrae in modern mammals, making it plausible to extrapolate the effects of Hox gene patterning to account for homoplastic evolution of vertebral characters in early mammals.
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References
Kielan-Jaworowska, Z. et al. Mammals from the Age of Dinosaurs—Origins, Evolution, and Structure (Columbia Univ. Press, New York, 2004)
Ji, Q. et al. Mesozoic Jehol Biota of Western Liaoning, China (Geol. Publ. House, Beijing, 2004)
Zhou, Z.-H. et al. An exceptionally preserved Lower Cretaceous ecosystem. Nature 421, 807–814 (2003)
Zhang, F. et al. Description of a new enantiornithine bird from the Early Cretaceous of Hebei, northern China. Can. J. Earth Sci. 41, 1097–1107 (2004)
Kermack, K. A. et al. The lower jaw of Morganucodon.. Zool. J. Linn. Soc. (Lond.) 53, 87–175 (1973)
Crompton, A. W. & Luo, Z.-X. in Mammal Phylogeny Vol. 1 (eds Szalay, F. S. et al.) 30–44 (Springer, New York, 1993)
Luo, Z.-X. et al. A new mammaliaform from the Early Jurassic of China and evolution of mammalian characteristics. Science 292, 1535–1540 (2001)
Jenkins, F. A. & Schaff, C. R. The Early Cretaceous mammal Gobiconodon (Mammalia, Triconodonta) from the Cloverly Formation in Montana. J. Vert. Paleontol. 8, 1–24 (1988)
Wang, Y.-Q. et al. An ossified Meckel’s cartilage in two Cretaceous mammals and origin of the mammalian middle ear. Science 294, 357–361 (2001)
Li, C.-K. et al. A new species of Gobiconodon (Triconodonta, Mammalia) and its implication for the age of Jehol Biota. Chin. Sci. Bull. (English edn). 48, 1129–1134 (2003)
Meng, J. et al. The ossified Meckel’s cartilage and internal groove in Mesozoic mammaliaforms: implications to origin of the definitive mammalian middle ear. Zool. J. Linn. Soc. (Lond.) 138, 431–448 (2003)
Hu, Y.-M. et al. Large Mesozoic mammals fed on young dinosaurs. Nature 433, 149–153 (2005)
Ji, Q. et al. A Chinese triconodont mammal and mosaic evolution of the mammalian skeleton. Nature 398, 326–330 (1999)
Luo, Z.-X. et al. Dual origin of tribosphenic mammals. Nature 409, 53–57 (2001)
Luo, Z.-X. et al. In quest for a phylogeny of Mesozoic mammals. Acta Palaeont. Polonica 47, 1–78 (2002)
Luo, Z.-X. & Wible, J. R. A new Late Jurassic digging mammal and early mammalian diversification. Science 308, 103–107 (2005)
Zeller, U. Die Entwicklung und Morphologie des Schädels von Ornithorhynchus anatinus (Mammalia: Prototheria: Monotremata). Abhandl. Senckenberg. Natur. Gesell. 545, 1–188 (1989)
Zeller, U. in Mammal Phylogeny Vol. 1 (eds Szalay, F. S. et al.) 95–107 (Springer, New York, 1993)
Fleischer, G. Studien am Skelett des Gehörorgans der Säugetiere, einschliesslich des Menschen. Säugetierk. Mitteil. 21, 131–239 (1973)
Jenkins, F. A. & Parrington, F. R. The postcranial skeletons of the Triassic mammals Eozostrodon, Megazostrodon and Erythrotherium.. Phil. Trans. R. Soc. Lond. 273, 387–431 (1976)
Martin, T. Postcranial anatomy of Haldanodon exspectatus (Mammalia, Docodonta) from the Late Jurasssic (Kimmeridgian) of Portugal and its bearing for mammalian evolution. Zool. J. Linn. Soc. (Lond.) 145, 219–248 (2005)
Ji, Q. et al. A swimming mammaliaform from the Middle Jurassic and ecomorphological diversification of early mammals. Science 311, 1123–1127 (2006)
Jenkins, F. A. The postcranial skeleton of African cynodonts. Peabody Mus. Nat. Hist. Bull. 36, 1–216 (1971)
Jenkins, F. A. The Chañares (Argentina) Triassic reptile fauna VII. The postcranial skeleton of the traversodontid Massetognathus pascuali (Therapsida, Cynotondia). Breviora 352, 1–28 (1970)
Sues, H.-D. & Jenkins, F. A. in Amniote Paleobiology: Perspectives on the Evolution of Mammals, Birds, and Reptiles (eds Carrano, M. T. et al.) 114–152 (Univ. Chicago Press, Chicago, 2006)
Krebs, B. 1991. Das Skelett von Henkelotherium guimarotae gen. et sp. nov. (Eupantotheria, Mammalia) aus dem Oberen Jura von Portugal. Berliner Geowisch. Abhandl. A133, 1–110 (1991)
Rougier, G. W. Vincelestes neuquenianus Bonaparte (Mammalia, Theria), un Primitivo Mamífero del Cretácico Inferior de la Cuenca Neuquina. PhD dissertation (Univ. Nacional Buenos Aires, 1993)
Szalay, F. S. Evolutionary History of the Marsupials and an Analysis of Osteological Characters (Cambridge Univ. Press, Cambridge, 1994)
Hu, Y.-M. et al. A new symmetrodont mammal from China and its implications for mammalian evolution. Nature 390, 137–142 (1997)
Ji, Q. et al. The earliest-known eutherian mammal. Nature 416, 816–822 (2002)
Luo, Z.-X. et al. An Early Cretaceous tribosphenic mammal and metatherian evolution. Science 302, 1934–1940 (2003)
Luo, Z.-X. & Ji, Q. New study on dental and skeletal features of the Cretaceous mammal Zhangheotherium. J. Mammal. Evol. 12, 337–357 (2005)
Li, G. & Luo, Z.-X. A Cretaceous symmetrodont therian with some monotreme-like postcranial features. Nature 439, 195–200 (2006)
Krause, D. W. & Jenkins, F. A. The postcranial skeleton of North American multituberculates. Bull. Mus. Comp. Zool. 150, 199–246 (1983)
Kielan-Jaworowska, Z. & Gambaryan, P. P. Postcranial anatomy and habits of Asian multituberculate mammals. Fossils Strata 36, 1–92 (1994)
Hu, Y.-M. The postcranium of Repenomamus and its implications for evolution of mammalian skeletal characters. J. Vert. Paleontol. 22 (3-Suppl.). 67A–68A (2002)
Narita, Y. & Kuratani, S. Evolution of vertebral formulae in mammals: a perspective on developmental constraints. J. Exp. Zool. 304B, 91–106 (2005)
Gaupp, E. Die Reichertsche Theorie (Hammer-, Amboss- und Kieferfrage). Archiv Anatomie Entwick.. 1912, 1–426 (1913)
Maier, W. Phylogeny and ontogeny of mammalian middle ear structures. Nether. J. Zool. 40, 55–75 (1990)
Maier, W. in Mammal Phylogeny (Volume 1) (eds Szalay, F. S. et al.) 165–181 (Springer, New York, 1993)
Rowe, T. B. Coevolution of the mammalian middle ear and neocortex. Science 273, 651–654 (1996)
Sánchez-Villagra, M. R. et al. Ontogenetic and phylogenetic transformations of the ear ossicles in marsupial mammals. J. Morphol. 251, 219–238 (2002)
Allin, E. F. Evolution of the mammalian middle ear. J. Morphol. 147, 403–438 (1975)
Allin, E. F. & Hopson, J. A. in The Evolutionary Biology of Hearing (eds Webster, D. B. et al.) 587–614 (Springer, New York, 1992)
Rich, T. H. et al. Independent origins of middle ear bones in monotremes and therians. Science 307, 910–914 (2005)
Martin, T. & Luo, Z.-X. Paleontology: homoplasy in the mammalian ear. Science 307, 861–862 (2005)
Bever, G. et al. Comment on “Independent origins of middle ear bones in monotremes and therians “ (I-II). Science 309, 1492a–1492b (2005)
Wellik, D. M. & Capecchi, M. R. Hox10 and Hox11 genes are required to globally pattern the mammalian skeleton. Science 301, 363–367 (2003)
Burke, A. C. & Nowicki, J. L. Hox genes and axial specification in vertebrates. Am. Zool. 41, 687–697 (2001)
Galis, F. Why do almost all mammals have seven cervical vertebrae? Developmental constraints, Hox genes, and cancer. J. Exp. Zool. 285, 19–26 (1999)
Acknowledgements
We thank A. Tabrum for preparing this fossil; X.-N. Yang, Y.-K. Shi, J.-R. Liu, Q. Yang, J.-G. Sha, H.-C. Zhang for support; Q. Ji and J. Wible for access to comparative collections; R. Cifelli, Z. Kielan-Jaworowska, T. Martin, T. Rowe, J. Wible and G. Wilson for discussions; M. Dawson and J. Wible for improving the manuscript; and M. Klingler for assistance with the figures. This work was supported by the National Natural Science Foundation of China (P.C., G.L. and Z.-X.L.), the National Science Foundation and National Geographic Society (Z.-X.L.), the Ministry of Science and Technology of China (the 973 Project under C.-S. Wang) and the State Key Laboratory of Palaeobiology and Stratigraphy of NIGPAS (G. L.).
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Luo, ZX., Chen, P., Li, G. et al. A new eutriconodont mammal and evolutionary development in early mammals. Nature 446, 288–293 (2007). https://doi.org/10.1038/nature05627
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DOI: https://doi.org/10.1038/nature05627
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