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Three new Jurassic euharamiyidan species reinforce early divergence of mammals

Nature volume 514, pages 579584 (30 October 2014) | Download Citation

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Abstract

The phylogeny of Allotheria, including Multituberculata and Haramiyida, remains unsolved and has generated contentious views on the origin and earliest evolution of mammals. Here we report three new species of a new clade, Euharamiyida, based on six well-preserved fossils from the Jurassic period of China. These fossils reveal many craniodental and postcranial features of euharamiyidans and clarify several ambiguous structures that are currently the topic of debate. Our phylogenetic analyses recognize Euharamiyida as the sister group of Multituberculata, and place Allotheria within the Mammalia. The phylogeny suggests that allotherian mammals evolved from a Late Triassic (approximately 208 million years ago) Haramiyavia-like ancestor and diversified into euharamiyidans and multituberculates with a cosmopolitan distribution, implying homologous acquisition of many craniodental and postcranial features in the two groups. Our findings also favour a Late Triassic origin of mammals in Laurasia and two independent detachment events of the middle ear bones during mammalian evolution.

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References

  1. 1.

    , , & A new arboreal haramiyid shows the diversity of crown mammals in the Jurassic period. Nature 500, 199–202 (2013)

  2. 2.

    Neue Schädel-Reste von Multituberculaten (Mamm.) aus dem Malm Portugals. Geol. Palaeontol. 11, 161–186 (1977)

  3. 3.

    & in The Evolutionary Biology of Hearing (eds , & ) Ch. 28 587–614 (Springer New York, 1992)

  4. 4.

    , , & A new symmetrodont mammal from China and its implications for mammalian evolution. Nature 390, 137–142 (1997)

  5. 5.

    , & The lower jaw of Morganucodon. Zool. J. Linn. Soc. 53, 87–175 (1973)

  6. 6.

    & 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. Univ. Wyo. 28, 39–138 (1991)

  7. 7.

    , & The First Haramiyid (Mammalia, Allotheria) from the Jurassic of Russia. Dokl. Biol. Sci. 437, 103–106 (2011)

  8. 8.

    , , & New multituberculate-like teeth from the Middle Jurassic of England. Acta Palaeontol. Pol. 43, 581–606 (1998)

  9. 9.

    & New teeth of allotherian mammals from the English Bathonian, including the earliest multituberculates. Acta Palaeontol. Pol. 50, 185–207 (2005)

  10. 10.

    , & Mammals from the Late Jurassic Qigu Formation in the southern Junggar Basin, Xinjiang, Northwest China. Palaeobiodiversity and Palaeoenvironments 90, 295–319 (2010)

  11. 11.

    , , , & Earliest evolution of multituberculate mammals revealed by a new Jurassic fossil. Science 341, 779–783 (2013)

  12. 12.

    Review of the early allotherian mammals. Acta Palaeontol. Pol. 45, 317–342 (2000)

  13. 13.

    , , & Variability and constraint in the mammalian vertebral column. J. Evol. Biol. 24, 1080–1090 (2011)

  14. 14.

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

  15. 15.

    , , & A swimming mammaliaform from the Middle Jurassic and ecomorphological diversification of early mammals. Science 311, 1123–1127 (2006)

  16. 16.

    , & Transitional mammalian middle ear from a new Cretaceous Jehol eutriconodont. Nature 472, 181–185 (2011)

  17. 17.

    , , & A new eutriconodont mammal and evolutionary development in early mammals. Nature 446, 288–293 (2007)

  18. 18.

    & A Cretaceous symmetrodont therian with some monotreme-like postcranial features. Nature 439, 195–200 (2006)

  19. 19.

    Homeotic evolution in the mammalia: diversification of therian axial seriation and the morphogenetic basis of human origins. PLoS ONE 2, e1019 (2007)

  20. 20.

    et al. Fixed cervical count and the origin of the mammalian diaphragm. Evol. Dev. 14, 399–411 (2012)

  21. 21.

    & The postcranial skeletons of the Triassic mammals Eozostrodon, Megazostrodon and Erythrotherium. Phil. Trans. R. Soc. Lond. B 273, 387–431 (1976)

  22. 22.

    Postcranial anatomy of Haldanodon exspectatus (Mammalia, Docodonta) from the Late Jurassic (Kimmeridgian) of Portugal and its bearing for mammalian evolution. Zool. J. Linn. Soc. 145, 219–248 (2005)

  23. 23.

    & Cretaceous multituberculate skeleton and the early evolution of the mammalian shoulder girdle. Nature 377, 144–147 (1995)

  24. 24.

    & Postcranial Anatomy and Habits of Asian Multituberculate Mammals. (Scandinavian Univ. Press, 1994)

  25. 25.

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

  26. 26.

    Functional-adaptive anatomy of the forelimb in the didelphidae, and the paleobiology of the paleocene marsupials Mayulestes ferox and Pucadelphys andinus. J. Morphol. 247, 51–79 (2001)

  27. 27.

    , , & An Early Cretaceous tribosphenic mammal and metatherian evolution. Science 302, 1934–1940 (2003)

  28. 28.

    et al. Epipubic bones in eutherian mammals from the Late Cretaceous of Mongolia. Nature 389, 483–486 (1997)

  29. 29.

    & The Early Cretaceous mammal Gobiconodon (Mammalia, Triconodonta) from the Cloverly Formation in Montana. J. Vertebr. Paleontol. 8, 1–24 (1988)

  30. 30.

    , & A Chinese triconodont mammal and mosaic evolution of the mammalian skeleton. Nature 398, 573–574 (1999)

  31. 31.

    , & A new symmetrodont mammal with fur impressions from the Mesozoic of China. Acta. Geol. Sin. (Engl.) 77, 7–14 (2003)

  32. 32.

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

  33. 33.

    , & Mammals from the Age of Dinosaurs: Origins, Evolution, and Structure. (Columbia Univ. Press, 2004)

  34. 34.

    The Biology of the Monotremes. (Academic Press, New York, 1978)

  35. 35.

    , & Were mammals originally venomous? Acta Palaeontol. Pol. 51, 1–11 (2006)

  36. 36.

    , & New data on Theroteinidae: their relations with Paulchoffatiidae and Haramiyidae. Geol. Palaeontol. 23, 205–215 (1989)

  37. 37.

    Haramiyidae (Mammalia, Allotheria) en provenance du Trias supérieur de Lorraine (France). Palaeontogr. Abt. A 206, 137–198 (1989)

  38. 38.

    , , & Haramiyids and Triassic mammalian evolution. Nature 385, 715–718 (1997)

  39. 39.

    & Evolutionary tendencies and systematic arrangement in the Haramiyida (Mammalia). Geol. Palaeontol. 40, 173–193 (2006)

  40. 40.

    , , & A Jurassic mammaliaform and the earliest mammalian evolutionary adaptations. Nature 500, 163–167 (2013)

  41. 41.

    & A Late Jurassic digging mammal and early mammalian diversification. Science 308, 103–107 (2005)

  42. 42.

    , , , & The oldest platypus and its bearing on divergence timing of the platypus and echidna clades. Proc. Natl Acad. Sci. USA 105, 1238–1242 (2008)

  43. 43.

    & Reassessment of the Late Triassic symmetrodont mammal Woutersia. Acta Palaeontol. Pol. 40, 245–260 (1995)

  44. 44.

    , & The Welsh pantothere Kuehneotherium praecursoris. Zool. J. Linn. Soc. 47, 407–423 (1968)

  45. 45.

    & Review of the British Haramiyidae (? Mammalia, Allotheria), their molar occlusion and relationships. Phil. Trans. R. Soc. Lond. B 345, 433–458 (1994)

  46. 46.

    In Pursuit of Early Mammals. 272 (Indiana Univ. Press, 2013)

  47. 47.

    Rhaeto-Liassic mammals from Switzerland and West Germany. Zitteliana 5, 51–92 (1980)

  48. 48.

    Gondwanatheria and ?Multituberculata (Mammalia) from the Late Cretaceous of Madagascar. Can. J. Earth Sci. Rev. Can. Sci. Terre 50, 324–340 (2013)

  49. 49.

    Functional-adaptive anatomy of the axial skeleton of some extant marsupials and the paleobiology of the paleocene marsupials mayulestes ferox and pucadelphys andinus. J. Morphol. 255, 279–300 (2003)

  50. 50.

    , , & Role of the prehensile tail during ateline locomotion: experimental and osteological evidence. Am. J. Phys. Anthropol. 126, 435–446 (2005)

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Acknowledgements

We thank H.-J. Li and Z.-J. Gao for using the specimens housed at the Jizantang Paleontological Museum; Z.-Y. Sun and D.-Y. Sun for using the specimen housed at the Museum of Wuyishan Mountain; J.-C. Lü for assistance in specimen collecting; S.-H. Xie for specimen preparation; M. A. Klingler and F.-X. Wu for specimen drawing and photography; W.-D. Zhang for SEM imaging; Z.-H. Zhou, X. Xu, F.-C. Zhang and X.-L. Wang for discussion on stratigraphy and faunal compositions; and A. Weil and G. W. Rougier for instructive comments. The study was supported by the National Basic Research Program of China (973 program, 2012CB821906), the Strategic Priority Research Program of Chinese Academy of Sciences (XDB03020501), the National Science Foundation of China (41128002) and the Hundred Talents Programs of the Chinese Academy of Sciences.

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Affiliations

  1. Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China

    • Shundong Bi
    •  & Yuanqing Wang
  2. Department of Biology, Indiana University of Pennsylvania, Indiana, Pennsylvania 15705, USA

    • Shundong Bi
  3. Beijing Natural History Museum, 126 Tianqiao Street, Dongcheng District, Beijing 100050, China

    • Jian Guan
  4. Paleontological Museum of Liaoning, Shenyang Normal University, Shenyang, Liaoning 110034, China

    • Xia Sheng
  5. Division of Paleontology, American Museum of Natural History, Central Park West at 79th Street, New York, New York 10024, USA

    • Jin Meng

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Contributions

S.B., J.M. and Y.W. designed the study, performed the comparative and analytical work and wrote the paper. J.G. and X.S. collected data and contributed to the writing and discussion.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Yuanqing Wang or Jin Meng.

The Life Science Identifiers (LSIDs) for this publication have been deposited at http://zoobank.org/ and include: urn:lsid:zoobank.org:pub:766EBC08-EF77-41E5-AC59-9F69E9F59BAA (for this publication), urn:lsid:zoobank.org:act:32B0742D-2DD3-47F9-A35B-E1FB284E9EA5 (Shenshou), urn:lsid:zoobank.org:act:BA8BF69D-0F21-4DE7-9EA5-BA6082973940 (Shenshou lui), urn:lsid:zoobank.org:act:4C10F9F1-A920-450B-8E5F-C88F3BD0920C (Xianshou), urn:lsid:zoobank.org:act:3DB1D738-70E9-4966-93FE-3FE5269F9C91 (Xianshou linglong), urn:lsid:zoobank.org:act:1F7EEE49-5E88-4941-AE8B-B2C7C31F9788 (Xianshou songae).

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https://doi.org/10.1038/nature13718

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