Article | Published:

A Jurassic ceratosaur from China helps clarify avian digital homologies

Nature volume 459, pages 940944 (18 June 2009) | Download Citation

Abstract

Theropods have traditionally been assumed to have lost manual digits from the lateral side inward, which differs from the bilateral reduction pattern seen in other tetrapod groups. This unusual reduction pattern is clearly present in basal theropods, and has also been inferred in non-avian tetanurans based on identification of their three digits as the medial ones of the hand (I-II-III). This contradicts the many developmental studies indicating II-III-IV identities for the three manual digits of the only extant tetanurans, the birds. Here we report a new basal ceratosaur from the Oxfordian stage of the Jurassic period of China (156–161 million years ago), representing the first known Asian ceratosaur and the only known beaked, herbivorous Jurassic theropod. Most significantly, this taxon possesses a strongly reduced manual digit I, documenting a complex pattern of digital reduction within the Theropoda. Comparisons among theropod hands show that the three manual digits of basal tetanurans are similar in many metacarpal features to digits II-III-IV, but in phalangeal features to digits I-II-III, of more basal theropods. Given II-III-IV identities in avians, the simplest interpretation is that these identities were shared by all tetanurans. The transition to tetanurans involved complex changes in the hand including a shift in digit identities, with ceratosaurs displaying an intermediate condition.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    The Interrelationships and Evolution of Basal Theropod Dinosaurs (Palaeontological Association, 2003)

  2. 2.

    , & The osteology of Masiakasaurus knopfleri, a small abelisauroid (Dinosauria: Theropoda) from the Late Cretaceous of Madagascar. J. Vertebr. Paleontol. 22, 510–534 (2002)

  3. 3.

    & in The Dinosauria 2nd edn (eds Weishampel, D. B., Dodson, P. & Osmolska, H.) 47–70 (Univ. California Press, 2004)

  4. 4.

    et al. An abelisauroid (Dinosauria: Theropoda) from the Early Jurassic of the High Atlas mountains, Morocco, and the radiation of ceratosaurs. J. Vertebr. Paleontol. 27, 610–624 (2007)

  5. 5.

    , & The large theropod fauna of the Lourinhã Formation (Portugal) and its similarity to that of the Morrison Formation, with a description of a new species of Allosaurus.. New Mexico Mus. Nat. Hist. Sci. Bull. 36, 123–129 (2006)

  6. 6.

    & The phylogeny of Ceratosauria (Dinosauria: Theropoda). J. Sys. Palaeontol. 6, 183–236 (2008)

  7. 7.

    et al. Sequence stratigraphy, paleoclimate patterns and vertebrate fossil preservation in Jurassic–Cretaceous strata of the Junggar Basin, Xinjiang Autonomous Region, People’s Republic China. Can. J. Earth Sci. 38, 1627–1644 (2001)

  8. 8.

    , , & Anatomy and systematics of the Confuciusornithidae (Theropoda: Aves) from the late Mesozoic of northeastern China. Bull. Am. Mus. 242, 1–89 (1999)

  9. 9.

    , & in The Dinosauria 2nd edn (eds Weishampel, D. B., Dodson, P. & Osmolska, H.) 71–110 (Univ. California Press, 2004)

  10. 10.

    & Limb proportions and avian terrestrial locomotion. J. Ornithol. 143, 356–371 (2002)

  11. 11.

    The Gondwanian theropod families Abelisauridae and Noasauridae. Hist. Biol. 5, 1–25 (1991)

  12. 12.

    et al. Predatory dinosaurs from the Sahara and Late Cretaceous faunal differentiation. Science 272, 986–991 (1996)

  13. 13.

    et al. A basal tyrannosauroid dinosaur from the Late Jurassic of China. Nature 439, 715–718 (2006)

  14. 14.

    The role of Central Asia in dinosaurian biogeography. Can. J. Earth Sci. 30, 2002–2012 (1993)

  15. 15.

    , & in The Dinosauria 2nd edn (eds Weishampel, D. B., Dodson, P. & Osmolska, H.) 137–150 (Univ. California Press, 2004)

  16. 16.

    The anatomy of Effigia okeeffeae (Archosauria, Suchia), theropod-like convergence, and the distribution of related taxa. Bull. Am. Mus. Nat. Hist. 302, 1–84 (2007)

  17. 17.

    et al. Herbivorous diet in an ornithomimid dinosaur. Nature 402, 480–481 (1999)

  18. 18.

    Elaphrosaurus, an ornithomimid dinosaur from the Upper Jurassic of North America and Africa. Palaeontologische Zeitschrift 56, 265–276 (1982)

  19. 19.

    , , , & An unusual oviraptorosaurian dinosaur from China. Nature 419, 291–293 (2002)

  20. 20.

    in The Origin of Birds and the Evolution of Flight (ed. Padian, K.) 1–55 (California Academy of Sciences, 1986)

  21. 21.

    & 1,2,3 = 2,3,4: a solution to the problem of the homology of the digits in the avian hand. Proc. Natl Acad. Sci. USA 96, 5111–5116 (1999)

  22. 22.

    in Homology: The Hierarchical Basis of Comparative Biology (ed. Hall, B. K.) 249–271 (Academic, 1994)

  23. 23.

    & Developmental patterns and the identification of homologies in the avian hand. Science 278, 666–668 (1997)

  24. 24.

    & Abelisaurid forelimb evolution: new evidence from Majungasaurus crenatissimus (Abelisauridae: Theropoda). J. Vertebr. Paleontol. 28 (supplement to 3) 58A (2008)

  25. 25.

    , & A new close relative of Carnotaurus sastrei Bonaparte 1985 (Theropoda: Abelisauridae) from the Late Cretaceous of Patagonia. J. Vertebr. Paleontol. 22, 460–465 (2002)

  26. 26.

    & The reptilian relationships of Archaeopteryx. Aust. J. Zool. 30, 611–634 (1982)

  27. 27.

    Die Ordnung des Lebendigen. Systembedingungen der Evolution (Parey, 1975)

  28. 28.

    , , & Hox genes and the evolution of vertebrate axial morphology. Development 121, 333–346 (1995)

  29. 29.

    & Interdigital regulation of digit identity and homeotic transformation by modulated BMP signaling. Science 289, 438–441 (2000)

  30. 30.

    & Pentadactyl ground state of the avian wing. J. Exp. Zool. B 294, 146–151 (2002)

  31. 31.

    & The hand of birds revealed by early ostrich embryos. Naturwissenschaften 89, 391–393 (2002)

  32. 32.

    , , & Gene expression and digit homology in the chicken embryo wing. Evol. Dev. 7, 18–28 (2005)

  33. 33.

    , , & Pentadactyl pattern of the avian wing autopodium and pyramid reduction hypothesis. J. Exp. Zool. B 294, 152–159 (2002)

  34. 34.

    & Birds have dinosaur wings: the molecular evidence. J. Exp. Zool. B 304, 86–90 (2005)

  35. 35.

    , , , & The evolution of HoxD-11 expression in the bird wing: insights from Alligator mississippiensis. PLoS ONE 3, e3325 (2008)

  36. 36.

    Counting the fingers of birds and dinosaurs. Science 280, 355 (1998)

  37. 37.

    in New Perspectives on the Origin and Early Evolution of Birds (eds Gauthier, J. A. & Gall, L. F.) 122–130 (Yale Univ. Press, 2001)

  38. 38.

    Dilophosaurus wetherilli (Dinosauria, Theropoda), osteology and comparisons. Palaeontgr. Abt. A 185, 85–180 (1984)

  39. 39.

    Manus movements of the coelurosaurian dinosaur Syntarsus and opposability of the theropod hallux. Arnoldia (Rhodesia) 5, 1–8 (1971)

  40. 40.

    The pectoral girdle and forelimb of the basal theropod Herrerasaurus ischigualastensis. J. Vertebr. Paleontol. 13, 425–450 (1993)

  41. 41.

    & in The Dinosauria (eds Weishampel, D. B., Dodson, P. & Osmolska, H.) 478–493 (Univ. California Press, 2004)

  42. 42.

    et al. A model for anteroposterior patterning of the vertebrate limb based on sequential long- and short-range Shh signalling and Bmp signalling. Development 127, 1337–1348 (2000)

  43. 43.

    , & Cross-talk between Wnt signaling parthways in human mesenchymal stem cells leads to functional antagonism during osteogenic differentiation. J. Cell. Biochem. 101, 1109–1124 (2007)

  44. 44.

    Developmental morphology of limb reduction in Hemiergis (Squamata: Scincidae): chondrogenesis, osteogenesis, and heterochrony. J. Morphol. 254, 211–231 (2002)

Download references

Acknowledgements

The authors thank H.-J. Wang for organizing the fieldwork, R. S. Li for illustrations, L.-S. Xiang and X.-Q. Ding for preparing the specimens, X.-Q. Ding for editing the illustrations, M. Kundrát and J. Gauthier for critical comments, O. Rauhut, P. Makovicky and D. Chure for some theropod images, R.-S. Tykoski for references, and members of the Sino-American expedition team for collecting the fossil. The field work was supported by the National Natural Science Foundation of China, the National Science Foundation Division of Earth Sciences of the USA, the Chinese Academy of Sciences, the National Geographic Society, the Jurassic Foundation, the Hilmar Sallee bequest and George Washington University. Study of the specimens was supported by the Chinese Academy of Sciences, the National Science Foundation Division of Earth Sciences of the USA and the National Natural Science Foundation of China.

Author Contributions X.X. and J.M.C. designed the project. X.X., J.M.C., J.C., G.M.E., S. N. and J.-Y.M. performed the research. X.X., J.M.C., G.M.E., J.C., C.S. and D.W.E.H. wrote the manuscript. X.X., J.M.C., J.-Y.M., J.C., C.A.F., D.A.E., Q.Z., R. H., C.-K. J., F.-L.H. and Y.G. excavated the specimens.

Author information

Affiliations

  1. Institute of Vertebrate Paleontology and Paleoanthropology, Beijing 100044, China

    • Xing Xu
    • , David W. E. Hone
    • , Corwin Sullivan
    • , Qi Zhao
    • , Feng-lu Han
    •  & Yu Guo
  2. Department of Biological Sciences, George Washington University, Washington DC 20052, USA

    • James M. Clark
    • , Jonah Choiniere
    •  & Catherine A. Forster
  3. Natural History Museum of Guangxi, Nanning, Guangxi 530012, China

    • Jinyou Mo
  4. Faculty of Earth Sciences, China University of Geosciences, Wuhan, Hubei 430074, China

    • Jinyou Mo
  5. Department of Biological Science, Florida State University, Tallahassee, Florida 32306, USA

    • Gregory M. Erickson
  6. Royal Tyrrell Museum, Drumheller, Alberta T0J 0Y0, Canada

    • David A. Eberth
  7. American Museum of Natural History, Central Park West at 79th Street, New York, New York 10024, USA

    • Sterling Nesbitt
  8. Instituto de Geologia, Universidad Nacional Autónoma de México, Ciudad Universitaria, Del. Coyocan, México DF 04510, Mexico

    • Rene Hernandez
  9. Research Institute of Exploration and Development, Xinjiang Oilfield Company, Karamay, Xinjiang 834000, China

    • Cheng-kai Jia
  10. Graduate School of Chinese Academy of Sciences, Beijing 100039, China

    • Feng-lu Han
    •  & Yu Guo

Authors

  1. Search for Xing Xu in:

  2. Search for James M. Clark in:

  3. Search for Jinyou Mo in:

  4. Search for Jonah Choiniere in:

  5. Search for Catherine A. Forster in:

  6. Search for Gregory M. Erickson in:

  7. Search for David W. E. Hone in:

  8. Search for Corwin Sullivan in:

  9. Search for David A. Eberth in:

  10. Search for Sterling Nesbitt in:

  11. Search for Qi Zhao in:

  12. Search for Rene Hernandez in:

  13. Search for Cheng-kai Jia in:

  14. Search for Feng-lu Han in:

  15. Search for Yu Guo in:

Corresponding author

Correspondence to Xing Xu.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains supplementary discussion and data, Supplementary Figures S1-S8 and References.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature08124

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.