Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-23T19:09:08.890Z Has data issue: false hasContentIssue false

Adductors, abductors, and the evolution of archosaur locomotion

Published online by Cambridge University Press:  08 February 2016

John R. Hutchinson
Affiliation:
Department of Integrative Biology and Museum of Paleontology, University of California, Berkeley, California 94720-3140. E-mail: [email protected]
Stephen M. Gatesy
Affiliation:
Department of Ecology and Evolutionary Biology, Brown University, Providence, Rhode Island 02912

Abstract

Living crocodilians (Crocodylia) and birds (Neornithes) differ in many aspects of hindlimb anatomy and locomotor function. How did this disparity evolve? We integrate information from fossils with functional descriptions of locomotion in living crocodilians and birds, using a phylogenetic perspective. We then outline the major changes in three-dimensional control of the hip joint along the line from the ancestral archosaur to birds. Our analysis reveals that most aspects of hip morphology and function in Alligator are ancestral for Archosauria. Femoral protractors and retractors are located cranial and caudal to the hip, respectively. Similarly, femoral adductors and abductors are located ventral and dorsal to the hip. Transformations of this ancestral pattern on the line to birds involved modifications in osteology, myology, and neural control. In some cases, homologous muscles changed function by acquiring new activity patterns. In others, activity was conserved, but origins and/or insertions were altered. Fossil theropods document the stepwise evolution of a novel mechanism of limb adduction/abduction involving long-axis rotation of the femur. This mechanism accounts for the conspicuous absence of significant musculature ventral and dorsal to the hip joint in extant birds.

Type
Articles
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Blob, R. W. 1998. Mechanics of non-parasagittal locomotion in Alligator and Iguana: functional implications for the evolution of non-sprawling posture in the Therapsida. . University of Chicago, Chicago.Google Scholar
Brinkman, D. 1980. The hind limb step cycle of Caiman sclerops and the mechanics of the crocodile tarsus and metatarsus. Canadian Journal of Zoology 58:21872200.CrossRefGoogle Scholar
Bryant, H. N., and Russell, A. P. 1992. The role of phylogenetic analysis in the inference of unpreserved attributes of extinct taxa. Philosophical Transactions of the Royal Society of London B 337:405418.Google Scholar
Carrano, M. T. 1998. Locomotion in non-avian dinosaurs: integrating data from hindlimb kinematics, in vivo strains, and bone morphology. Paleobiology 24:450469.CrossRefGoogle Scholar
Carrano, M. T. 2000. Homoplasy and the evolution of dinosaur locomotion. Paleobiology 26:489512.2.0.CO;2>CrossRefGoogle Scholar
Carrano, M. T., and Biewener, A. A. 1999. Experimental alteration of limb posture in the chicken (Gallus gallus) and its bearing on the use of birds as analogs for dinosaur locomotion. Journal of Morphology 240:237249.3.0.CO;2-N>CrossRefGoogle ScholarPubMed
Charig, A. 1972. The evolution of the archosaur pelvis and hindlimb: an explanation in functional terms. Pp. 121155in Joysey, K. A. and Kemp, T. S., eds. Studies in vertebrate evolution. Oliver & Boyd, Edinburgh.Google Scholar
Chatterjee, S. 1997. The rise of birds: 225 million years of evolution. Johns Hopkins University Press, Baltimore.Google Scholar
Chiappe, L. M. 1996. Late Cretaceous birds of southern South America: anatomy and systematics of Patagopteryx and Enantiornithes. In Arratia, G., ed. Contributions of southern South America to vertebrate paleontology. Münchner Geowissenschaftliche, Abhandlungen A 30:203244.Google Scholar
Clark, J., and Alexander, R. McN. 1975. Mechanics of running by quail (Coturnix). Journal of Zoology 176:87113.CrossRefGoogle Scholar
Colbert, E. H. 1964. Relationships of the saurischian dinosaurs. American Museum Novitates 2181:124.Google Scholar
Forster, C. A., Sampson, S. D., Chiappe, L. M., and Krause, D. W. 1998. The theropod ancestry of birds: new evidence from the Late Cretaceous of Madagascar. Science 279:19151919.CrossRefGoogle ScholarPubMed
Galton, P. M. 1969. The pelvic musculature of the dinosaur Hypsilophodon (Reptilia: Ornithischia). Postilla 131:164.Google Scholar
Gatesy, S. M. 1990. Caudofemoral musculature and the evolution of theropod locomotion. Paleobiology 16:170186.CrossRefGoogle Scholar
Gatesy, S. M. 1991. Hind limb movements of the American alligator (Alligator mississippiensis) and postural grades. Journal of Zoology 224:577588.CrossRefGoogle Scholar
Gatesy, S. M. 1994. Neuromuscular diversity in archosaur deep dorsal thigh muscles. Brain Behavior and Evolution 43:114.CrossRefGoogle ScholarPubMed
Gatesy, S. M. 1995. Functional evolution of the hind limb and tail from basal theropods to birds. Pp. 219234in Thomason, 1995.Google Scholar
Gatesy, S. M. 1997. An electromyographic analysis of hindlimb function in Alligator during terrestrial locomotion. Journal of Morphology 234:197212.3.0.CO;2-9>CrossRefGoogle ScholarPubMed
Gatesy, S. M. 1999a. Guineafowl hind limb function. I. Cineradiographic analysis and speed effects. Journal of Morphology 240:115125.3.0.CO;2-Y>CrossRefGoogle ScholarPubMed
Gatesy, S. M. 1999b. Guineafowl hind limb function. II. Electromyographic analysis and motor pattern evolution. Journal of Morphology 240:127142.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Gatesy, S. M.In press. Locomotor evolution on the line to modern birds. In Witmer, L. M. and Chiappe, L. M., eds. Mesozoic birds: above the heads of the dinosaurs. Academic Press, New York.Google Scholar
Gatesey, S. M., and Middleton, K. M. 1997. Bipedalism, flight, and the evolution of theropod locomotor diversity. Journal of Vertebrate Paleontology 17:308329.CrossRefGoogle Scholar
Gauthier, J. A. 1986. Saurischian monophyly and the origin of birds. In Padian, K., ed. The origin of birds and the evolution of flight. Memoirs of the California Academy of Sciences 8:155.Google Scholar
Gauthier, J. A., Kluge, A. G., and Rowe, T. 1988. Amniote phylogeny and the importance of fossils. Cladistics 4:105209.CrossRefGoogle ScholarPubMed
George, J. C., and Berger, A. J. 1966. Avian myology. Academic Press, New York.Google Scholar
Grenard, S. 1991. Handbook of alligators and crocodiles. Krieger, Malabar, Fla.Google Scholar
Holtz, T. R. Jr.In press. A new phylogeny of the carnivorous dinosaurs. Gaia.Google Scholar
Hutchinson, J. R.In press a. The evolution of pelvic osteology and soft tissues on the line to extant birds (Neornithes). Zoological Journal of the Linnean Society.Google Scholar
Hutchinson, J. R.In press b. The evolution of femoral osteology and soft tissues on the line to extant birds (Neornithes). Zoological Journal of the Linnean Society.Google Scholar
Jacobson, R. D., and Hollyday, M. 1982. A behavioral and electromyographic study of walking in the chick. Journal of Neurophysiology 48:238256.CrossRefGoogle ScholarPubMed
Lovejoy, C. O. 1973. The gait of australopithecines. Yearbook of Physical Anthropology 17:147161.Google Scholar
Maddison, W. P., Donoghue, M. J., and Maddison, D. R. 1984. Outgroup analysis and parsimony. Systematic Zoology 33:83103.CrossRefGoogle Scholar
Makovicky, P. J., and Sues, H.-D. 1998. Anatomy and phylogenetic relationships of the theropod dinosaur Microvenator celer from the Lower Cretaceous of Montana. American Museum Novitates 3240:127.Google Scholar
McKitrick, M. C. 1991. Phylogenetic analysis of avian hindlimb musculature. Miscellaneous Publications of the Museum of Zoology, University of Michigan 179:185.Google Scholar
McLeish, R. D., and Charnley, J. 1970. Abduction forces in the one-legged stance. Journal of Biomechanics 3:191209.CrossRefGoogle ScholarPubMed
Molnar, R. E., Kurzanov, S. M., and Dong, Z. 1990. Carnosauria. Pp. 169209in Weishampel, D. B., Dodson, P., Osmólska, H., eds. The Dinosauria. University of California Press, Berkeley.Google Scholar
Norell, M. A., and Makovicky, P. J. 1999. Important features of the dromaeosaur skeleton. II. information from newly collected specimens of Velociraptor mongoliensis. American Museum Novitates 3282:145.Google Scholar
Novas, F. E. 1996. Dinosaur monophyly. Journal of Vertebrate Paleontology 16:723741.CrossRefGoogle Scholar
Ostrom, J. H. 1976. Archaeopteryx and the origin of birds. Biological Journal of the Linnean Society 8:91182.CrossRefGoogle Scholar
Padian, K., and Olsen, P. E. 1984. Footprints of the Komodo Monitor and the trackways of fossil reptiles. Copeia 1984:662671.CrossRefGoogle Scholar
Padian, K., and Olsen, P. E. 1989. Ratite footprints and the stance and gait of Mesozoic theropods. Pp. 231241in Gillette, D. D. and Lockley, M. G., eds. Dinosaur tracks and traces. Cambridge University Press, Cambridge.Google Scholar
Padian, K., Hutchinson, J. R., and Holtz, T. R. Jr. 1999. Phylogenetic definitions and nomenclature of the major taxonomic categories of the carnivorous Dinosauria (Theropoda). Journal of Vertebrate Paleontology 19:6980.CrossRefGoogle Scholar
Parrish, J. M. 1986. Locomotor adaptations in the hindlimb and pelvis of the Thecodontia. Hunteria 1:135.Google Scholar
Perle, A. 1985. Comparative myology of the pelvic-femoral region in the bipedal dinosaurs. Paleontological Journal 19:105109.Google Scholar
Proctor, N. S., and Lynch, P. J. 1993. Manual of ornithology: avian structure and function. Yale University Press, New Haven, Conn.Google Scholar
Raikow, R. J. 1975. The evolutionary reappearance of ancestral muscles as developmental anomalies in two species of birds. Condor 77:514517.CrossRefGoogle Scholar
Rasskin-Gutmann, D., and Buscalioni, A. D.In press. Theoretical morphology of the archosaur (Reptilia: Diapsida) pelvic girdle. Paleobiology 27.2.0.CO;2>CrossRefGoogle Scholar
Reilly, S. M., and Elias, J. A. 1998. Locomotion in Alligator mississippiensis: kinematic effects of speed and posture and their relevance to the sprawling-to-erect paradigm. Journal of Experimental Biology 201:25592574.CrossRefGoogle Scholar
Romer, A. S. 1923a. Crocodilian pelvic muscles and their avian and reptilian homologues. Bulletin of the American Museum of Natural History 48:533552.Google Scholar
Romer, A. S. 1923b. The pelvic musculature of saurischian dinosaurs. Bulletin of the American Museum of Natural History 48:605617.Google Scholar
Romer, A. S. 1927a. The pelvic musculature of ornithischian dinosaurs. Acta Zoologica 8:225275.CrossRefGoogle Scholar
Romer, A. S. 1927b. The development of the thigh musculature of the chick. Journal of Morphology 43:347385.CrossRefGoogle Scholar
Romer, A. S. 1942. The development of tetrapod limb musculature—the thigh of Lacerta. Journal of Morphology 71:251298.CrossRefGoogle Scholar
Rowe, T. 1986. Homology and evolution of the deep dorsal thigh musculature in birds and other Reptilia. Journal of Morphology 189:327346.CrossRefGoogle ScholarPubMed
Ruben, J. A., Jones, T. D., Geist, N. R., and Hillenius, W. J. 1997. Lung structure and ventilation in theropod dinosaurs and early birds. Science 278:12671270.CrossRefGoogle Scholar
Sennikov, A. G. 1989. Basic evolutionary laws of development of the locomotor apparatus in the archosaurs. Paleontological Journal 4:6068.Google Scholar
Sereno, P. C. 1991. Basal archosaurs: phylogenetic relationships and functional implications. Journal of Vertebrate Paleontology 11(Suppl. to No. 4):153.CrossRefGoogle Scholar
Sereno, P. C. 1999. The evolution of dinosaurs. Science 284:21372147.CrossRefGoogle ScholarPubMed
Sereno, P. C., and Arcucci, A. B. 1994. Dinosaurian precursors from the Middle Triassic of Argentina: Marasuchus lilloensis, gen. nov. Journal of Vertebrate Paleontology 14:5373.CrossRefGoogle Scholar
Stern, J. T., and Susman, R. L. 1981. Electromyography of the gluteal muscles in Hylobates, Pongo, and Pan: implications for the evolution of hominid bipedality. American Journal of Physical Anthropology 55:153166.CrossRefGoogle Scholar
Tarsitano, S. 1983. Stance and gait in theropod dinosaurs. Acta Palaeontologica Polonica 28:251264.Google Scholar
Thomason, J. J., ed. 1995. Functional morphology in vertebrate paleontology. Cambridge University Press, CambridgeGoogle Scholar
Vanden Berge, J. C., and Zweers, G. A. 1993. Myologia. In Baumel, J. J., King, A. S., Breazile, J. E., Evans, H. E., and Vanden Berge, J. C., eds. Handbook of avian anatomy: nomina anatomica avium, 2d ed.Publications of the Nuttall Ornithological Club 23:189250.Google Scholar
Wade, M. 1989. The stance of dinosaurs and the cossack dancer syndrome. Pp. 7382in Gillette, D. D. and Lockley, M. G., eds. Dinosaur tracks and traces. Cambridge University Press, Cambridge.Google Scholar
Walker, A. D. 1961. Triassic reptiles from the Elgin area: Stagonolepis, Dasygnathus and their allies. Philosophical Transactions of the Royal Society of London B 244:103204.Google Scholar
Walker, A. D. 1977. Evolution of the pelvis in birds and dinosaurs. In Andrews, S. M., Miles, R. S., and Walker, A. D., eds. Problems in vertebrate evolution. Linnean Society Symposium Series 4:319358.Google Scholar
Welles, S. P. 1986. Thoughts on the origin of the Theropoda. Pp. 3134in Padian, K., ed. The beginning of the age of dinosaurs. Academic Press, New York.Google Scholar
Witmer, L. M. 1995. The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. Pp. 1933in Thomason, 1995.Google Scholar