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A new eutriconodont mammal and evolutionary development in early mammals

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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Figure 1: New mammal Yanoconodon allini.
Figure 2: Relationship of Yanoconodon allini.
Figure 3: Comparison of mandible and middle ear of Yanoconodon.
Figure 4: Homoplastic evolution of lumbar ribs among Mesozoic mammals and patterning of vertebral and rib development by Hox10 gene in extant mammals.

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References

  1. Kielan-Jaworowska, Z. et al. Mammals from the Age of Dinosaurs—Origins, Evolution, and Structure (Columbia Univ. Press, New York, 2004)

    Book  Google Scholar 

  2. Ji, Q. et al. Mesozoic Jehol Biota of Western Liaoning, China (Geol. Publ. House, Beijing, 2004)

    Google Scholar 

  3. Zhou, Z.-H. et al. An exceptionally preserved Lower Cretaceous ecosystem. Nature 421, 807–814 (2003)

    Article  ADS  CAS  Google Scholar 

  4. 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)

    Article  ADS  Google Scholar 

  5. Kermack, K. A. et al. The lower jaw of Morganucodon.. Zool. J. Linn. Soc. (Lond.) 53, 87–175 (1973)

    Article  Google Scholar 

  6. Crompton, A. W. & Luo, Z.-X. in Mammal Phylogeny Vol. 1 (eds Szalay, F. S. et al.) 30–44 (Springer, New York, 1993)

    Book  Google Scholar 

  7. Luo, Z.-X. et al. A new mammaliaform from the Early Jurassic of China and evolution of mammalian characteristics. Science 292, 1535–1540 (2001)

    Article  ADS  CAS  Google Scholar 

  8. 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)

    Article  Google Scholar 

  9. 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)

    Article  ADS  CAS  Google Scholar 

  10. 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)

    Google Scholar 

  11. 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)

    Article  Google Scholar 

  12. Hu, Y.-M. et al. Large Mesozoic mammals fed on young dinosaurs. Nature 433, 149–153 (2005)

    Article  ADS  CAS  Google Scholar 

  13. Ji, Q. et al. A Chinese triconodont mammal and mosaic evolution of the mammalian skeleton. Nature 398, 326–330 (1999)

    Article  ADS  CAS  Google Scholar 

  14. Luo, Z.-X. et al. Dual origin of tribosphenic mammals. Nature 409, 53–57 (2001)

    Article  ADS  CAS  Google Scholar 

  15. Luo, Z.-X. et al. In quest for a phylogeny of Mesozoic mammals. Acta Palaeont. Polonica 47, 1–78 (2002)

    Google Scholar 

  16. Luo, Z.-X. & Wible, J. R. A new Late Jurassic digging mammal and early mammalian diversification. Science 308, 103–107 (2005)

    Article  ADS  CAS  Google Scholar 

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

    Google Scholar 

  18. Zeller, U. in Mammal Phylogeny Vol. 1 (eds Szalay, F. S. et al.) 95–107 (Springer, New York, 1993)

    Book  Google Scholar 

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

    Google Scholar 

  20. 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)

    Article  Google Scholar 

  21. 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)

    Article  Google Scholar 

  22. Ji, Q. et al. A swimming mammaliaform from the Middle Jurassic and ecomorphological diversification of early mammals. Science 311, 1123–1127 (2006)

    Article  ADS  CAS  Google Scholar 

  23. Jenkins, F. A. The postcranial skeleton of African cynodonts. Peabody Mus. Nat. Hist. Bull. 36, 1–216 (1971)

    Google Scholar 

  24. 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)

    Google Scholar 

  25. 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)

    Google Scholar 

  26. 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)

    Google Scholar 

  27. 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)

  28. Szalay, F. S. Evolutionary History of the Marsupials and an Analysis of Osteological Characters (Cambridge Univ. Press, Cambridge, 1994)

    Google Scholar 

  29. Hu, Y.-M. et al. A new symmetrodont mammal from China and its implications for mammalian evolution. Nature 390, 137–142 (1997)

    Article  ADS  CAS  Google Scholar 

  30. Ji, Q. et al. The earliest-known eutherian mammal. Nature 416, 816–822 (2002)

    Article  ADS  CAS  Google Scholar 

  31. Luo, Z.-X. et al. An Early Cretaceous tribosphenic mammal and metatherian evolution. Science 302, 1934–1940 (2003)

    Article  ADS  CAS  Google Scholar 

  32. Luo, Z.-X. & Ji, Q. New study on dental and skeletal features of the Cretaceous mammal Zhangheotherium. J. Mammal. Evol. 12, 337–357 (2005)

    Article  Google Scholar 

  33. Li, G. & Luo, Z.-X. A Cretaceous symmetrodont therian with some monotreme-like postcranial features. Nature 439, 195–200 (2006)

    Article  ADS  CAS  Google Scholar 

  34. Krause, D. W. & Jenkins, F. A. The postcranial skeleton of North American multituberculates. Bull. Mus. Comp. Zool. 150, 199–246 (1983)

    Google Scholar 

  35. Kielan-Jaworowska, Z. & Gambaryan, P. P. Postcranial anatomy and habits of Asian multituberculate mammals. Fossils Strata 36, 1–92 (1994)

    Google Scholar 

  36. 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)

    Google Scholar 

  37. Narita, Y. & Kuratani, S. Evolution of vertebral formulae in mammals: a perspective on developmental constraints. J. Exp. Zool. 304B, 91–106 (2005)

    Article  Google Scholar 

  38. Gaupp, E. Die Reichertsche Theorie (Hammer-, Amboss- und Kieferfrage). Archiv Anatomie Entwick.. 1912, 1–426 (1913)

    Google Scholar 

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

    Article  Google Scholar 

  40. Maier, W. in Mammal Phylogeny (Volume 1) (eds Szalay, F. S. et al.) 165–181 (Springer, New York, 1993)

    Book  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  42. Sánchez-Villagra, M. R. et al. Ontogenetic and phylogenetic transformations of the ear ossicles in marsupial mammals. J. Morphol. 251, 219–238 (2002)

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  44. Allin, E. F. & Hopson, J. A. in The Evolutionary Biology of Hearing (eds Webster, D. B. et al.) 587–614 (Springer, New York, 1992)

    Book  Google Scholar 

  45. Rich, T. H. et al. Independent origins of middle ear bones in monotremes and therians. Science 307, 910–914 (2005)

    Article  ADS  CAS  Google Scholar 

  46. Martin, T. & Luo, Z.-X. Paleontology: homoplasy in the mammalian ear. Science 307, 861–862 (2005)

    Article  CAS  Google Scholar 

  47. Bever, G. et al. Comment on “Independent origins of middle ear bones in monotremes and therians “ (I-II). Science 309, 1492a–1492b (2005)

    Article  Google Scholar 

  48. Wellik, D. M. & Capecchi, M. R. Hox10 and Hox11 genes are required to globally pattern the mammalian skeleton. Science 301, 363–367 (2003)

    Article  ADS  CAS  Google Scholar 

  49. Burke, A. C. & Nowicki, J. L. Hox genes and axial specification in vertebrates. Am. Zool. 41, 687–697 (2001)

    CAS  Google Scholar 

  50. Galis, F. Why do almost all mammals have seven cervical vertebrae? Developmental constraints, Hox genes, and cancer. J. Exp. Zool. 285, 19–26 (1999)

    Article  CAS  Google Scholar 

Download references

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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