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Patristic evolutionary rates suggest a punctuated pattern in forelimb evolution before and after the origin of birds

Published online by Cambridge University Press:  08 April 2016

T. Alex Dececchi  and
Hans C. E. Larsson
T. Alex Dececchi
Affiliation:
Redpath Museum, McGill University, Montreal, Quebec H3A 2K6, Canada. E-mail: thomas.dececchi@mail.mcgill.ca
Hans C. E. Larsson
Affiliation:
Redpath Museum, McGill University, Montreal, Quebec H3A 2K6, Canada. E-mail: hans.ce.larsson@mcgill.ca
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Abstract

The evolution of powered flight has traditionally been associated with the origin of birds, the most successful clade of modern tetrapods, as exemplified by the nearly 10,000 species alive today. Flight requires a suite of morphological changes to skeletal anatomy to create a light yet resistant framework for an airfoil and advanced nervous motor control. Given the level of morphological integration necessary to create a suitable aerofoil, the origin of flight may be intuitively assumed to be coupled with high evolutionary rates of wing-related morphologies. Here we show that the origin of birds is associated with little or no evolutionary change to the skeletal anatomy of the forelimb, and thus Archaeopteryx is unlikely to be the “Rosetta Stone” for the origin of flight it was once believed to be. Using comparative statistics and time-series analyses on a data set constructed from all known forelimb skeletal anatomy of non-avian theropod dinosaurs and a diverse assemblage of early birds, we demonstrate three focused peaks of rapid forelimb evolution at Tetanurae, Eumaniraptora, and Ornithothoraces. The peaks are not associated with missing data and remain stable under multiple perturbations to the phylogenetic arrangements. Different regions of the forelimbs are demonstrated to have undergone asynchronous periods of evolutionary peaks and stasis. Our results evince a more complicated stepwise mode of forelimb evolution before and after the origin of Aves than previously supposed.

Type
Articles
Information
Paleobiology , Volume 35 , Issue 1 , Winter 2009 , pp. 1 - 12
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Alonzo, P. D., Milner, A. C., Ketcham, R. A., Cookson, M. J., and Rowe, T. 2004. The avian nature of the brain and inner ear of Archaeopteryx . Nature 430:666–669.CrossRefGoogle Scholar
Baier, D. B., Gatesy, S. M., and Jenkins, F. A. 2007. A critical ligamentous mechanism in the evolution of avian flight. Nature 445:307–310.CrossRefGoogle ScholarPubMed
Bininda-Emonds, O. R. P. 2004. The evolution of supertrees. Trends in Ecology and Evolution 19:315–322.CrossRefGoogle ScholarPubMed
Carroll, R. L. 1997. Patterns and processes in vertebrate evolution. Cambridge University Press, Cambridge.Google Scholar
Chatterjee, S., and Templin, R. J. 2007. Biplane wing planform and flight performance of the feathered dinosaur Microraptor gui . Proceedings of the National Academy of Sciences USA 104:1576–1580.CrossRefGoogle ScholarPubMed
Chiappe, L. M. 1995. The first 85 million years of avian evolution. Nature 378:349–355.CrossRefGoogle Scholar
Chiappe, L. M. 2002. Basal bird phylogeny: problems and solutions. Pp. 448–472 in Chiappe, L. M. and Witmer, L. M., eds. Mesozoic birds: above the heads of dinosaurs. University of California Press, Berkeley.Google Scholar
Chiappe, L. M., and Dyke, G. J. 2006. The early evolutionary history of birds. Journal of the Paleontological Society of Korea 22:133–151.Google Scholar
Chiappe, L. M., and Walker, C. A. 2002. Skeletal morphology and systematics of the Cretaceous Euenantiornithes (Ornithothoraces: Enantiornithes). Pp. 240–267 in Chiappe, L. M. and Witmer, L. M., eds. Mesozoic birds: above the head of dinosaurs. University of California Press, Berkeley.Google Scholar
Clarke, J. A., Zhou, Z., and Zhang, F. 2006. Insight into the evolution of avian flight from a new clade of Early Cretaceous ornithurines from China and the morphology of Yixianornis grabaui . Journal of Anatomy 208:287–308.CrossRefGoogle ScholarPubMed
Crawley, M. J. 2005. Statistics: an introduction using R. Wiley, Chichester, West Sussex. CrossRefGoogle Scholar
Davis, J. C. 2002. Statistics and data analysis in geology. Wiley, New York.Google Scholar
Gauthier, J., and de Queiroz, K. 2001. Feathered dinosaurs, flying dinosaurs, crown dinosaurs and the name “Aves.” Pp. 7–41 in Gauthier, J. and Gall, L. F., eds. New perspectives on the origin and early evolution of birds: proceedings of the international symposium in honor of John H. Ostrom. Peabody Museum of Natural History, New Haven, Conn. Google Scholar
Gauthier, J., and Padian, K., eds. 1985. Phylogenetic, functional, and aerodynamic analyses of the origins of birds and their flight. Pp. 185–197 in Hecht, M. K., Ostrom, J. H., Viohl, G., and Wellnhofer, P., eds. The beginnings of birds. Proceedings of the international Archaeopteryx conference; 1984, Eichstätt, Germany. Freunde des Jura-Museums, Eichstätt.Google Scholar
Hammer, Ø., Harper, D. A. T., and Ryan, P. D. 2001. PAST: palaeontological statistics software package for education and data analysis. Palaeontologia Electronica 4:1–9.Google Scholar
Holtz, T. R. 2004. Saurischia. Pp. 21–24 in Weishampel, D. B., Dodson, P., and Osmolska, H., eds. The Dinosauria. University of California Press, Berkeley.Google Scholar
Ji, Q., Currie, P. J., Norell, M., and Ji, S. A. 1998. Two feathered dinosaurs from northeastern China. Nature 393:753–761.Google Scholar
Larsson, H. C. E. 2001. Endocranial anatomy of Charcharodontosaurus saharicus (Theropoda: Allosauroidea) and its implications for theropod brain evolution. Pp. 19–33 in Tanke, D. H. and Carpenter, A. K., eds. Mesozoic vertebrate life: new research inspired by the paleontology of Philip J. Currie. Indiana University Press, Bloomington.Google Scholar
Longrich, N. 2006. Structure and function of hindlimb feathers in Archaeopteryx lithographica . Paleobiology 32:417–431.CrossRefGoogle Scholar
Makovicky, P., Apesteguía, S., and Agnolín, F. 2005. The earliest dromaeosaurid theropod from South America. Nature 437:1007–1011.CrossRefGoogle ScholarPubMed
Maryanska, T., Osmolska, H., and Wolsan, M. 2002. Avialan status for Oviraptorosauria. Acta Palaeontologica Polonica 47:97–116.Google Scholar
Mayr, G., Pohl, B., Hartman, S., and Peters, D. S. 2007. The tenth skeletal specimen of Archaeopteryx . Zoological Journal of the Linnean Society 149:97–116.CrossRefGoogle Scholar
Nanayakkara, N. 1992. On the robustness and Johnson's modification of the one sample t-statistic. Communications in Statistics—Theory and Methods 21(11):3079–3096.CrossRefGoogle Scholar
Nixon, K. C. 2002. Winclada 1. 00.08 ed. The author, Ithaca, N.Y. Google Scholar
Ostrom, J. H. 1995. Wing biomechanics and the origin of bird flight. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 195:253–266.CrossRefGoogle Scholar
Padian, K. 2001. Stages in the origin of bird flight: beyond the arboreal-cursorial dichotomy. Pp. 255–272 in Gauthier, J. and Gall, L. F., eds. New perspectives on the origin and early evolution of birds: proceedings of the international symposium in honor of John H. Ostrom. Peabody Museum of Natural History, New Haven, Conn. Google Scholar
Padian, K., de Ricqlès, A. J., and Horner, J. R. 2001. Dinosaurian growth rates and bird origins. Nature 412:405–408.CrossRefGoogle ScholarPubMed
Poore, S. O., Sanchez-Haiman, A., and Goslow, G. E. Jr. 1997. Wing upstroke and the evolution of flapping flight. Nature 387:799–802.CrossRefGoogle Scholar
Prum, R. O., and Brush, A. H. 2002. The evolutionary origin and diversification of feathers. Quarterly Review of Biology 77:261–295.CrossRefGoogle ScholarPubMed
Sereno, P. C. 1999. The evolution of dinosaurs. Science 284:2137–2147.CrossRefGoogle ScholarPubMed
Sidor, C. A., and Hopson, J. A. 1998. Ghost lineages and “mammalness”: assessing the temporal pattern of character acquisition in the Synapsida. Paleobiology 24:254–273.CrossRefGoogle Scholar
Xu, X., Zhou, Z. H., Wang, X. L., Kuang, X. W., Zhang, F. C., and Du, X. K. 2003. Four-winged dinosaurs from China. Nature 421:335–340.CrossRefGoogle ScholarPubMed
Zar, J. H. 1999. Biostatistical analysis. Prentice-Hall, Upper Saddle River, N.J. Google Scholar
Zhang, F., and Zhou, Z. 2000. A primitive enantiornithine bird and the origin of feathers. Science 290:1955–1959.CrossRefGoogle ScholarPubMed
Zhou, Z. 2002. A new and primitive enantiornithine bird from the Early Cretaceous of China. Journal of Vertebrate Paleontology 22:49–57.CrossRefGoogle Scholar
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