The theropod ancestry of birds: New evidence from the Late Cretaceous of Madagascar

Science

Volumn 279, Issue 5358, 1998, Pages 1915-1919

  Forster, Catherine A ^a   Sampson, Scott D ^b   Chiappe, Luis M ^c   Krause, David W ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b NEW YORK INSTITUTE OF TECHNOLOGY   (United States)

^c DIVISION OF INVERTEBRATE ZOOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEOPTERYA; BIRD; CRETACEOUS; RAHONA; THEROPOD ANCESTRY;

ANIMAL TISSUE; ARTICLE; BIRD; NONHUMAN; PALEOANTHROPOLOGY; PHYLOGENY; PRIORITY JOURNAL; SKELETON;

MADAGASCAR;

EID: 0032549747     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.279.5358.1915     Document Type: Article

References (39)

1. E. D. Cope, Proc. Acad. Nat. Sci. Phila. 1867, 234 (1867); T. H. Huxley, Geol. Mag. 5, 357 (1868); S. W. Williston, Kans. City Rev. Sci. 3, 457 (1879); L. Witmer, in Origin of the Higher Groups of Tetrapods, H.-P. Schultze and L. Trueb, Eds. (Comstock, Ithaca, NY, 1991), pp. 427-466; P. C. Sereno and C. Rao, Science 255, 845 (1992); L. M. Chiappe, Nature 378, 349 (1995). To increase readability and conserve space, we use the shorthand terms "theropod" and "maniraptoran" in place of "nonavian theropod" and "nonavian maniraptoran," respectively.
2. E. D. Cope, Proc. Acad. Nat. Sci. Phila. 1867, 234 (1867); T. H. Huxley, Geol. Mag. 5, 357 (1868); S. W. Williston, Kans. City Rev. Sci. 3, 457 (1879); L. Witmer, in Origin of the Higher Groups of Tetrapods, H.-P. Schultze and L. Trueb, Eds. (Comstock, Ithaca, NY, 1991), pp. 427-466; P. C. Sereno and C. Rao, Science 255, 845 (1992); L. M. Chiappe, Nature 378, 349 (1995). To increase readability and conserve space, we use the shorthand terms "theropod" and "maniraptoran" in place of "nonavian theropod" and "nonavian maniraptoran," respectively.
3. E. D. Cope, Proc. Acad. Nat. Sci. Phila. 1867, 234 (1867); T. H. Huxley, Geol. Mag. 5, 357 (1868); S. W. Williston, Kans. City Rev. Sci. 3, 457 (1879); L. Witmer, in Origin of the Higher Groups of Tetrapods, H.-P. Schultze and L. Trueb, Eds. (Comstock, Ithaca, NY, 1991), pp. 427-466; P. C. Sereno and C. Rao, Science 255, 845 (1992); L. M. Chiappe, Nature 378, 349 (1995). To increase readability and conserve space, we use the shorthand terms "theropod" and "maniraptoran" in place of "nonavian theropod" and "nonavian maniraptoran," respectively.
4. E. D. Cope, Proc. Acad. Nat. Sci. Phila. 1867, 234 (1867); T. H. Huxley, Geol. Mag. 5, 357 (1868); S. W. Williston, Kans. City Rev. Sci. 3, 457 (1879); L. Witmer, in Origin of the Higher Groups of Tetrapods, H.-P. Schultze and L. Trueb, Eds. (Comstock, Ithaca, NY, 1991), pp. 427-466; P. C. Sereno and C. Rao, Science 255, 845 (1992); L. M. Chiappe, Nature 378, 349 (1995). To increase readability and conserve space, we use the shorthand terms "theropod" and "maniraptoran" in place of "nonavian theropod" and "nonavian maniraptoran," respectively.
5. E. D. Cope, Proc. Acad. Nat. Sci. Phila. 1867, 234 (1867); T. H. Huxley, Geol. Mag. 5, 357 (1868); S. W. Williston, Kans. City Rev. Sci. 3, 457 (1879); L. Witmer, in Origin of the Higher Groups of Tetrapods, H.-P. Schultze and L. Trueb, Eds. (Comstock, Ithaca, NY, 1991), pp. 427-466; P. C. Sereno and C. Rao, Science 255, 845 (1992); L. M. Chiappe, Nature 378, 349 (1995). To increase readability and conserve space, we use the shorthand terms "theropod" and "maniraptoran" in place of "nonavian theropod" and "nonavian maniraptoran," respectively.
6. E. D. Cope, Proc. Acad. Nat. Sci. Phila. 1867, 234 (1867); T. H. Huxley, Geol. Mag. 5, 357 (1868); S. W. Williston, Kans. City Rev. Sci. 3, 457 (1879); L. Witmer, in Origin of the Higher Groups of Tetrapods, H.-P. Schultze and L. Trueb, Eds. (Comstock, Ithaca, NY, 1991), pp. 427-466; P. C. Sereno and C. Rao, Science 255, 845 (1992); L. M. Chiappe, Nature 378, 349 (1995). To increase readability and conserve space, we use the shorthand terms "theropod" and "maniraptoran" in place of "nonavian theropod" and "nonavian maniraptoran," respectively.
7. J. H. Ostrom, Biol. J. Linn. Soc. 8, 91 (1976).
8. J. A. Gauthier, Mem. Calif. Acad. Sci. 8, 1 (1986).
9. T. R. Holtz Jr., J. Paleontol. 68, 1100 (1994).
10. F. E. Novas, Mem. Queensl. Mus. 39, 675 (1996).
11. L. M. Chiappe, ibid., p. 533.
12. G. Heilman, The Origin of Birds (Appleton, New York, 1927); A. S. Romer, Vertebrate Paleontology (Univ. of Chicago Press, Chicago, IL, 1966); P. Brodkorb, in Avian Biology, D. S. Farner, J. R. King, K. C. Parkes, Eds. (Academic Press, New York, 1971), pp. 19-55.
13. G. Heilman, The Origin of Birds (Appleton, New York, 1927); A. S. Romer, Vertebrate Paleontology (Univ. of Chicago Press, Chicago, IL, 1966); P. Brodkorb, in Avian Biology, D. S. Farner, J. R. King, K. C. Parkes, Eds. (Academic Press, New York, 1971), pp. 19-55.
14. G. Heilman, The Origin of Birds (Appleton, New York, 1927); A. S. Romer, Vertebrate Paleontology (Univ. of Chicago Press, Chicago, IL, 1966); P. Brodkorb, in Avian Biology, D. S. Farner, J. R. King, K. C. Parkes, Eds. (Academic Press, New York, 1971), pp. 19-55.
15. S. Tarsitano, in Origin of the Higher Groups of Tetrapods, H.-P. Schultze and L. Trueb, Eds. (Comstock, Ithaca, NY, 1991), pp. 541-576.
16. A. Feduccia and R. Wild, Naturwissenshaften 80, 564 (1993); A. C. Burke and A. Feduccia, Science 278, 666 (1997).
17. A. Feduccia and R. Wild, Naturwissenshaften 80, 564 (1993); A. C. Burke and A. Feduccia, Science 278, 666 (1997).
18. A. Feduccia and L. Martin, Mus. North Ariz. Bull. 60, 185 (1996).
19. J. A. Ruben et al. Science 278, 1267 (1997).
20. L. D. Martin, in Origin of the Higher Groups of Tetrapods, H.-P. Schultze and L. Trueb, Eds. (Comstock, Ithaca, NY, 1991), pp. 485-540.
21. The holotype specimen of Rahona ostromi is cataloged as Université d'Antananarivo (UA) 8656. Locality: MAD93-18, Upper Cretaceous (?Campanian) Maevarano Formation, Mahajanga Basin, northwestern Madagascar; collected by a joint expedition of the State University of New York at Stony Brook and the Université d'Antananarivo in 1995. Etymology: Rahona (RAH-hoo-nah; Malagasy): meaning menace/threat or cloud; intended interpretation: "menace from the clouds"; ostromi: in honor of Dr. John H. Ostrom. Diagnosis: Rahona ostromi is distinguished from all other avians by retention of a robust, hyperextendible, pedal digit II; from all other avians except Patagonykus by hyposphenehypantra articulations on dorsal vertebrae; from Archaeopteryx by six fused sacral vertebrae and a greatly reduced fibula lacking contact with the calcaneum; from nonavian theropods, Archaeopteryx, and alvarezsaurids by its relatively elongate ulna with ulnar papillae and mobile scapulocoracoid articulation; from all other avians except Archaeopteryx and alvarezsaurids by retention of a long tail lacking a pygostyle; and from nonavian theropods by neural canals at least 40% of the height of the dorsal vertebral centra, proximal tibia of equal width and length, lack of a medial fossa on the fibula, and a reversed pedal digit I.
22. C. A. Forster et al., Nature 382, 532 (1996).
23. The placement of Patagonykus and other alvarezsaurids (Mononykus and Alvarezsaurus) within Aves, although supported by cladistic analyses [for example, see (5, 6) and this analysis], is questioned by other researchers (10). Elimination of Alvarezsauridae from the phylogenetic analyses presented in this report does not alter the placement of Rahona within Aves.
24. B. Stephan, Urvögel Archaeopterygiformes (Ziemsen, Wittenberg, Germany, 1974); S. Rietschel, in The Beginnings of Birds, M. K. Hecht, J. H. Ostrom, G. Viohl, P. Wellnhofer, Eds. (Brönner and Daentler, Eichstätt, Germany, 1984), pp. 251-260.
25. B. Stephan, Urvögel Archaeopterygiformes (Ziemsen, Wittenberg, Germany, 1974); S. Rietschel, in The Beginnings of Birds, M. K. Hecht, J. H. Ostrom, G. Viohl, P. Wellnhofer, Eds. (Brönner and Daentler, Eichstätt, Germany, 1984), pp. 251-260.
26. F. A. Jenkins, Am. J. Sci. 293-A, 253 (1993); S. A. Poore, A. Sánchez-Haiman, G. E. Goslow Jr., Nature 387, 799 (1997).
27. F. A. Jenkins, Am. J. Sci. 293-A, 253 (1993); S. A. Poore, A. Sánchez-Haiman, G. E. Goslow Jr., Nature 387, 799 (1997).
28. F. E. Novas and P. F. Puerta, Nature 387, 390 (1997).
29. J. H. Ostrom, Peabody Mus. Bull. 30, 1 (1969).
30. P. J. Currie, J. Vertebr. Paleontol. 7, 72 (1987); P. J. Currie and X. Zhao, Can. J. Earth Sci. 30, 2231 (1993).
31. P. J. Currie, J. Vertebr. Paleontol. 7, 72 (1987); P. J. Currie and X. Zhao, Can. J. Earth Sci. 30, 2231 (1993).
32. Morphological information from Rahona was combined with that of six bird and eight maniraptoran taxa into a 113-character matrix and analyzed with the PAUP and MacClade programs. Characters were unordered and unweighted, and trees were optimized with the use of delayed transformations. Tree statistics are as follows: The most parsimonious tree shown in Fig. 5A is 228 steps; consistency index (Cl) = 0.579, homoplasy index (Hl) = 0.421, retention index (Rl) = 0.712. The tree shown in Fig. 5B is 229 steps; Cl = 0.576, Hl = 0.424, Rl = 0.709. The character matrix and character list for this phylogenetic analysis are available at www.sciencemag.org/ feature/data/972697.shl.
33. The three forelimb elements of Rahona were found either next to or touching the hind portion of the skeleton (Fig. 1B). Because they were not in direct articulation with the rear of the animal, we recognize the possibility, albeit remote in our opinion, that they do not belong to the same individual or taxon. Although material of more derived avians was found elsewhere in the quarry, with the exception of one articulated partial tibiotarsus-tarsometatarsus (14) all avian material occurred as widely scattered, isolated elements. The only articulated skeleton found anywhere in the quarry is that of Rahona. Because of the taphonomic distribution of bone in the quarry and the juxtaposition of these forelimb elements with the rear portion of the skeleton, we believe they belong to the same specimen and are confident in assigning them to Rahona. Nevertheless, to test the effect of an erroneous association, the phylogenetic analysis was run with two data sets, one including and one excluding forelimb elements for Rahona. Each data set resulted in two most parsimonious trees; the ambiguity in these trees was due to the switching of the positions of the theropod taxa Oviraptoridae and Ornithomimidae. The topology of taxa within Aves was consistent across all four most parsimonious trees, with Rahona firmly nested within this clade.
34. J. H. Ostrom, The Beginnings of Birds, M. K. Hecht, J. H. Ostrom, G. Viohl, P. Wellnhofer, Eds. (Brönner and Daentler, Eichstätt, Germany, 1984), pp. 161-176; L. Hou, L. D. Martin, Z. Zhou, A. Feduccia, Science 274, 1164 (1996); N. Bonde, in The Continental Jurassic, M. Morales, Ed. (Museum of Northem Arizona, Flagstaff, AZ, 1996), pp. 193-199.
35. J. H. Ostrom, The Beginnings of Birds, M. K. Hecht, J. H. Ostrom, G. Viohl, P. Wellnhofer, Eds. (Brönner and Daentler, Eichstätt, Germany, 1984), pp. 161-176; L. Hou, L. D. Martin, Z. Zhou, A. Feduccia, Science 274, 1164 (1996); N. Bonde, in The Continental Jurassic, M. Morales, Ed. (Museum of Northem Arizona, Flagstaff, AZ, 1996), pp. 193-199.
36. J. H. Ostrom, The Beginnings of Birds, M. K. Hecht, J. H. Ostrom, G. Viohl, P. Wellnhofer, Eds. (Brönner and Daentler, Eichstätt, Germany, 1984), pp. 161-176; L. Hou, L. D. Martin, Z. Zhou, A. Feduccia, Science 274, 1164 (1996); N. Bonde, in The Continental Jurassic, M. Morales, Ed. (Museum of Northem Arizona, Flagstaff, AZ, 1996), pp. 193-199.
37. It cannot be ascertained whether Archaeopteryx possesses hyposphene-hypantra articulations. Among more derived birds, only the alvarezsaurid Patagonykus retains this character.
38. The foot of Unenlagia is not known. However, it has been suggested that Archaeopteryx retains vestiges of an enlarged, hyperextendible, second pedal digit and claw. This observation was first advanced by J. Gauthier (3) and more recently revived by G. Paul [Programs and Abstracts, Society of Avian Paleontology and Evolution (Washington, DC, 1996), p. 15].
39. We thank B. Rakotosamimanana, P. Wright, B. Andriamihaja, the staff of the Institute for the Conservation of Tropical Environments, the people of Berivotra, and all expedition members for their help; and L. Witmer, J. Clark, and an anonymous reviewer for discussions and critiques. D. Varricchio, J. Clark, M. Norell, H. Osmólska, and P. Wellnhofer provided valuable information on theropods and Archaeopteryx. Rahona was prepared by V. Heisey and photographed by M. Stewart and F. E. Grine (with a scanning electron microscope), and figures were drawn by L. Betti-Nash and C.A.F. This work was supported by grants from NSF and The Dinosaur Society (to C.A.F., S.D.S., and D.W.K.) and the J. S. Guggenheim Foundation and F. Chapman Memorial Fund (to L.M.C.).