A Jurassic ceratosaur from China helps clarify avian digital homologies

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.

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Figure 1: Limusaurus inextricabilis (IVPP V 15923).
Figure 2: Theropod manual morphologies as represented by several non-avian theropods.
Figure 3: Manual digital evolution in theropod dinosaurs.

References

  1. 1

    Rauhut, O. W. M. The Interrelationships and Evolution of Basal Theropod Dinosaurs (Palaeontological Association, 2003)

    Google Scholar 

  2. 2

    Carrano, M. T., Sampson, S. D. & Forster, C. A. The osteology of Masiakasaurus knopfleri, a small abelisauroid (Dinosauria: Theropoda) from the Late Cretaceous of Madagascar. J. Vertebr. Paleontol. 22, 510–534 (2002)

    Google Scholar 

  3. 3

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

    Google Scholar 

  4. 4

    Allain, R. 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)

    Google Scholar 

  5. 5

    Mateus, O., Walen, A. & Antunes, M. T. 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)

    Google Scholar 

  6. 6

    Carrano, M. T. & Sampson, S. D. The phylogeny of Ceratosauria (Dinosauria: Theropoda). J. Sys. Palaeontol. 6, 183–236 (2008)

    Google Scholar 

  7. 7

    Eberth, D. A. 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)

    ADS  Google Scholar 

  8. 8

    Chiappe, L. M., Ji, S.-A., Ji, Q. & Norell, M. A. Anatomy and systematics of the Confuciusornithidae (Theropoda: Aves) from the late Mesozoic of northeastern China. Bull. Am. Mus. 242, 1–89 (1999)

    Google Scholar 

  9. 9

    Holtz, T. R. J., Molnar, R. E. & Currie, P. J. in The Dinosauria 2nd edn (eds Weishampel, D. B., Dodson, P. & Osmolska, H.) 71–110 (Univ. California Press, 2004)

    Google Scholar 

  10. 10

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

    Google Scholar 

  11. 11

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

    Google Scholar 

  12. 12

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

    ADS  CAS  PubMed  Google Scholar 

  13. 13

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

    ADS  CAS  PubMed  Google Scholar 

  14. 14

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

    ADS  Google Scholar 

  15. 15

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

    Google Scholar 

  16. 16

    Nesbitt, S. 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)

    Google Scholar 

  17. 17

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

    ADS  CAS  Google Scholar 

  18. 18

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

    Google Scholar 

  19. 19

    Xu, X., Cheng, Y. N., Wang, X. L., Chang, C. H. & Chang, H. An unusual oviraptorosaurian dinosaur from China. Nature 419, 291–293 (2002)

    ADS  CAS  PubMed  Google Scholar 

  20. 20

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

    Google Scholar 

  21. 21

    Wagner, G. P. & Gauthier, J. A. 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)

    ADS  CAS  PubMed  Google Scholar 

  22. 22

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

    Google Scholar 

  23. 23

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

    ADS  CAS  Google Scholar 

  24. 24

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

    Google Scholar 

  25. 25

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

    Google Scholar 

  26. 26

    Thulborn, R. A. & Hamley, T. L. The reptilian relationships of Archaeopteryx . Aust. J. Zool. 30, 611–634 (1982)

    Google Scholar 

  27. 27

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

    Google Scholar 

  28. 28

    Burke, A. C., Nelson, C. E., Morgan, B. A. & Tabin, C. Hox genes and the evolution of vertebrate axial morphology. Development 121, 333–346 (1995)

    CAS  PubMed  Google Scholar 

  29. 29

    Dahn, R. D. & Fallon, J. F. Interdigital regulation of digit identity and homeotic transformation by modulated BMP signaling. Science 289, 438–441 (2000)

    ADS  CAS  PubMed  Google Scholar 

  30. 30

    Larsson, H. C. E. & Wagner, G. P. Pentadactyl ground state of the avian wing. J. Exp. Zool. B 294, 146–151 (2002)

    Google Scholar 

  31. 31

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

    ADS  CAS  PubMed  Google Scholar 

  32. 32

    Welten, M. C., Verbeek, F. J., Meijer, A. H. & Richardson, M. K. Gene expression and digit homology in the chicken embryo wing. Evol. Dev. 7, 18–28 (2005)

    CAS  PubMed  Google Scholar 

  33. 33

    Kundrát, M., Seichert, V., Russell, A. P. & Smetana, K. Pentadactyl pattern of the avian wing autopodium and pyramid reduction hypothesis. J. Exp. Zool. B 294, 152–159 (2002)

    Google Scholar 

  34. 34

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

    Google Scholar 

  35. 35

    Vargas, A. O., Kohlsdorf, T., Fallon, J. F., Brooks, J. V. & Wagner, G. P. The evolution of HoxD-11 expression in the bird wing: insights from Alligator mississippiensis . PLoS ONE 3, e3325 (2008)

    ADS  PubMed  PubMed Central  Google Scholar 

  36. 36

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

    ADS  Google Scholar 

  37. 37

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

    Google Scholar 

  38. 38

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

    Google Scholar 

  39. 39

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

    Google Scholar 

  40. 40

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

    Google Scholar 

  41. 41

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

    Google Scholar 

  42. 42

    Drossopoulou, G. 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)

    CAS  PubMed  Google Scholar 

  43. 43

    Baksh, D., Boland, G. M. & Tuan, R. S. 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)

    CAS  PubMed  Google Scholar 

  44. 44

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

    PubMed  Google Scholar 

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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.

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Correspondence to Xing Xu.

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Xu, X., Clark, J., Mo, J. et al. A Jurassic ceratosaur from China helps clarify avian digital homologies. Nature 459, 940–944 (2009). https://doi.org/10.1038/nature08124

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