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Evolution of hindlimb posture in nonmammalian therapsids: biomechanical tests of paleontological hypotheses

Published online by Cambridge University Press:  08 February 2016

Richard W. Blob*
Affiliation:
Department of Zoology, Division of Fishes, Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, Illinois 60605. E-mail: [email protected]

Abstract

Analyses of limb joint morphology in nonmammalian therapsid “mammal-like reptiles” have suggested that among many lineages, individual animals were capable of shifting between sprawling and upright hindlimb postures, much like modern crocodilians. The ability to use multiple limb postures thus might have been ancestral to the generally more upright posture that evolved during the transition from “mammal-like reptiles” to mammals. Here I derive a biomechanical model to test this hypothesis through calculations of expected posture-related changes in femoral stress for therapsid taxa using different limb postures. The model incorporates morphological data from fossil specimens and experimental data from force platform experiments on iguanas and alligators.

Experimental data suggest that the evolutionary transition from sprawling to nonsprawling posture was accompanied by a change in the predominant loading regime of the limb bones, from torsion to bending. Changes in the cross-sectional morphology of the hindlimb bones between sphenacodontid “pelycosaurs” and gorgonopsid therapsids are consistent with the hypothesis that bending loads increased in importance early in therapsid evolution; thus, bending stresses are an appropriate model for the maximal loads experienced by the limb bones of theriodont therapsids. Results from the model used to estimate stresses in these taxa do not refute the use of both sprawling and more upright stance among basal theriodont therapsids. Thus, the hypothesis that the use of multiple postures was ancestral to the more upright posture typical of most mammals is biomechanically plausible. Model calculations also indicate that the axial rotation of the femur typical in sprawling locomotion can reduce peak bending stresses. Therefore, as experimental data from alligators and iguanas suggest, the evolution of nonsprawling limb posture and kinematics in therapsids might have been accompanied by increased limb bone bending stress.

Type
Articles
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Alexander, R. McN. 1974. The mechanics of a dog jumping, Canis familiaris. Journal of Zoology (London) 173:549573.CrossRefGoogle Scholar
Alexander, R. McN. 1981. Factors of safety in the structure of animals. Science Progress (Oxford) 67:109130.Google ScholarPubMed
Alexander, R. McN. 1983. On the massive legs of a Moa (Pachyornis elephantopus, Dinornithes). Journal of Zoology 201:363376.CrossRefGoogle Scholar
Alexander, R. McN., Maloiy, G. M. O., Hunter, B., Jayes, A. S., and Nturibi, J. 1979. Mechanical stresses in fast locomotion of buffalo (Syncerus caffer) and elephant (Loxodonta africana). Journal of Zoology 189:135144.CrossRefGoogle Scholar
Bakker, R. T. 1971. Dinosaur physiology and the origin of mammals. Evolution 25:636658.CrossRefGoogle Scholar
Beer, F. P., and Johnston, E. R. Jr. 1997. Vector mechanics for engineers: statics and dynamics, 6th ed.McGraw-Hill, Boston.Google Scholar
Biewener, A. A. 1983a. Locomotory stresses in the limb bones of two small mammals: the ground squirrel and chipmunk. Journal of Experimental Biology 103:131154.CrossRefGoogle ScholarPubMed
Biewener, A. A. 1983b. Allometry of quadrupedal locomotion: the scaling of duty factor, bone curvature and limb orientation to body size. Journal of Experimental Biology 105:147171.CrossRefGoogle ScholarPubMed
Biewener, A. A. 1989. Scaling body support in mammals: limb posture and muscle mechanics. Science 245:4548.CrossRefGoogle ScholarPubMed
Biewener, A. A. 1990. Biomechanics of mammalian terrestrial locomotion. Science 250:10971103.CrossRefGoogle ScholarPubMed
Biewener, A. A. 1993. Safety factors in bone strength. Calcified Tissue International 53(Suppl. 1):S68S74.CrossRefGoogle ScholarPubMed
Biewener, A. A., and Full, R. J. 1992. Force platform and kinematic analysis. Pp. 4573in Biewener, A. A., ed. Biomechanics—structures and systems: a practical approach. Oxford University Press, New York.CrossRefGoogle Scholar
Biewener, A. A., Thomason, J., Goodship, A., and Lanyon, L. E. 1983. Bone stress in the horse forelimb during locomotion at different gaits: a comparison of two experimental methods. Journal of Biomechanics 16:565576.CrossRefGoogle ScholarPubMed
Biewener, A. A., Thomason, J., and Lanyon, L. E. 1988. Mechanics of locomotion and jumping in the horse (Equus): in vivo stress in the tibia and metatarsus. Journal of Zoology 214:547565.CrossRefGoogle Scholar
Blob, R. W. 1997. Vertebral markers for vent position in lizards: applications in functional studies. American Zoologist 37:55A.Google Scholar
Blob, R. W. 1998. Mechanics of nonparasagittal locomotion in Alligator and Iguana: functional implications for the evolution of nonsprawling posture in the Therapsida. Ph.D. dissertation. University of Chicago, Chicago.Google Scholar
Blob, R. W. 2000. Interspecific scaling of the hind limb skeleton in lizards, crocodilians, felids and canids: does limb bone shape correlate with limb posture? Journal of Zoology 250:507531.CrossRefGoogle Scholar
Blob, R. W., and Biewener, A. A. 1998. Locomotor mechanics of Alligator and Iguana: in vivo bone strain and force platform analyses. American Zoologist 38:148A.Google Scholar
Blob, R. W., and Biewener, A. A. 1999. In vivo locomotor strain in the hindlimb bones of Alligator mississippiensis and Iguana iguana: implications for the evolution of limb bone safety factor and nonsprawling limb posture. Journal of Experimental Biology 202:10231046.CrossRefGoogle ScholarPubMed
Blob, R. W., and Biewener, A. A.In press. Mechanics of limb bone loading during terrestrial locomotion in the green iguana (Iguana iguana) and American alligator (Alligator mississippiensis). Journal of Experimental Biology.Google Scholar
Boonstra, L. D. 1967. An early stage in the evolution of the mammalian quadrupedal walking gait. Annals of the South African Museum 50:2742.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
Brinkman, D. 1981. The hind limb step cycle of Iguana and primitive reptiles. Journal of Zoology 181:91103.CrossRefGoogle Scholar
Bryant, H. N., and Seymour, K. L. 1990. Observations and comments on the reliability of muscle reconstruction in fossil vertebrates. Journal of Morphology 206:109117.CrossRefGoogle ScholarPubMed
Bustard, H. R. 1967. Gekkonid lizards adapt fat storage to desert environments. Science 158:11971198.CrossRefGoogle ScholarPubMed
Carrano, M. T. 1998. The evolution of dinosaur locomotion: functional morphology, biomechanics, and modern analogs. Ph.D. dissertation. University of Chicago, Chicago.Google Scholar
Cavagna, G. A., Heglund, N. C., and Taylor, C. R. 1977. Mechanical work in terrestrial locomotion: two basic mechanisms for minimizing energy expenditure. American Journal of Physiology 233:R243R261.Google ScholarPubMed
Charig, A. J. 1972. The evolution of the archosaur pelvis and hind-limb: an explanation in functional terms. Pp. 121155in Joysey, K. A. and Kemp, T. S., eds. Studies in vertebrate evolution. Oliver and Boyd, Edinburgh.Google Scholar
Colbert, E. H. 1948. The mammal-like reptile Lycaenops. Bulletin of the American Museum of Natural History 89:357404.Google Scholar
Currey, J. D. 1984. The mechanical properties of bone. Princeton University Press, Princeton, N.J.CrossRefGoogle ScholarPubMed
Currey, J. D. 1987. Evolution of the mechanical properties of amniote bone. Journal of Biomechanics 20:10351044.CrossRefGoogle ScholarPubMed
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. 1997. An electromyographic analysis of hindlimb function in Alligator during terrestrial locomotion. Journal of Morphology 234:197212.3.0.CO;2-9>CrossRefGoogle ScholarPubMed
Gould, S. J., and Lewontin, R. C. 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proceedings of the Royal Society of London B 205:581598.Google Scholar
Hildebrand, M. 1985. Walking and running. Pp. 3857in Hildebrand, M., Bramble, D. M., Liem, K. F., and Wake, D. B., eds. Functional vertebrate morphology. Harvard University Press, Cambridge.CrossRefGoogle Scholar
Hopson, J. A. 1991. Systematics of the nonmammalian Synapsida and implications for patterns of evolution in synapsids. Pp. 635693in Schultze, H.-P. and Trueb, L., eds. Origins of the higher groups of tetrapods: controversy and consensus. Comstock, Ithaca, N.Y.Google Scholar
Hopson, J. A. 1994. Synapsid evolution and the radiation of non-eutherian mammals. In Prothero, D. R. and Schoch, R. M., eds. Major features of vertebrate evolution. Short Courses in Paleontology 7:190217. Paleontological Society, Knoxville, Tenn.Google Scholar
Jayes, A. S., and Alexander, R. McN. 1980. The gaits of chelonians: walking techniques for very low speeds. Journal of Zoology 191:353378.CrossRefGoogle Scholar
Jenkins, F. A. Jr. 1971a. Limb posture and locomotion in the Virginia opossum (Didelphis marsupialis) and in other non-cursorial mammals. Journal of Zoology 165:303315.CrossRefGoogle Scholar
Jenkins, F. A. Jr. 1971b. The postcranial skeleton of African cynodonts. Bulletin of the Peabody Museum of Natural History 36:1216.Google Scholar
Kemp, T. S. 1978. Stance and gait in the hindlimb of a therocephalian mammal-like reptile. Journal of Zoology 186:143161.CrossRefGoogle Scholar
Kemp, T. S. 1980a. The primitive cynodont Procynosuchus: structure, function, and evolution of the postcranial skeleton. Philosophical Transactions of the Royal Society of London B 288:217258.Google Scholar
Kemp, T. S. 1980b. Aspects of the structure and functional anatomy of the Middle Triassic cynodont Luangwa. Journal of Zoology 191:193239.CrossRefGoogle Scholar
Kemp, T. S. 1982. Mammal-like reptiles and the origin of mammals. Academic Press, London.Google Scholar
Kemp, T. S. 1985. A functional interpretation of the transition from primitive tetrapod to mammalian locomotion. Pp. 181191in Reiß, J. and Frey, E., eds. Principles of construction in fossil and recent reptiles. Universität Stuttgart/Universität Tübingen, Stuttgart.Google Scholar
Kemp, T. S. 1986. The skeleton of a bauroid therocephalian therapsid from the Lower Triassic (Lystrosaurus Zone) of South Africa. Journal of Vertebrate Paleontology 6:215232.CrossRefGoogle Scholar
Kielan-Jawaroska, Z., and Gambaryan, P. P. 1994. Postcranial anatomy and habits of Asian multituberculate mammals. Fossils and Strata 36:192.CrossRefGoogle Scholar
King, G. M. 1981. The functional anatomy of a Permian dicynodont. Philosophical Transactions of the Royal Society of London B 291:243321.Google Scholar
Lande, R., and Arnold, S. J. 1983. The measurement of selection on correlated characters. Evolution 37:12101226.CrossRefGoogle ScholarPubMed
Martin, R. F. 1978. Clutch weight/ total body weight ratios of lizards (Reptilia, Lacertilia, Iguanidae): preservative induced variation. Journal of Herpetology 12:248251.CrossRefGoogle Scholar
Parrington, F. R. 1961. The evolution of the mammalian femur. Proceedings of the Zoological Society of London 137:285298.CrossRefGoogle Scholar
Peterson, J. A., and Zernicke, R. F. 1987. The geometric and mechanical properties of limb bones in the lizard, Dipsosaurus dorsalis. Journal of Biomechanics 20:902.CrossRefGoogle Scholar
Reilly, S. M. 1994/95. Quantitative electromyography and muscle function of the hind limb during quadrupedal running in the lizard Sceloporus clarkii. Zoology Analysis of Complex Systems 98:263277.Google Scholar
Reilly, S. M. 1998. Sprawling locomotion in the lizard Sceloporus clarkii: speed modulation of motor patterns in a walking trot. Brain, Behavior and Evolution 52:126138.CrossRefGoogle Scholar
Reilly, S. M., and DeLancey, M. J. 1997a. Sprawling locomotion in the lizard Sceloporus clarkii: quantitative kinematics of a walking trot. Journal of Experimental Biology 200:753765.CrossRefGoogle ScholarPubMed
Reilly, S. M., and DeLancey, M. J. 1997b. Sprawling locomotion in the lizard Sceloporus clarkii: the effects of speed on gait, hindlimb kinematics, and axial bending during walking. Journal of Zoology 243:417433.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. 1922. The locomotor apparatus of certain primitive and mammal-like reptiles. Bulletin of the American Museum of Natural History 46:517606.Google Scholar
Romer, A. S., and Price, L. I. 1940. Review of the Pelycosauria. Geological Society of America Special Paper 28:1538.CrossRefGoogle Scholar
Schaeffer, B. 1941a. The pes of Bauria cynops Broom. American Museum Novitates 1103:17.Google Scholar
Schaeffer, B. 1941b. The morphological and functional evolution of the tarsus in amphibians and reptiles. Bulletin of the American Museum of Natural History 78:395472.Google Scholar
Sidor, C. A. 1996. Early synapsid evolution, with special reference to the Caseasauria. Journal of Vertebrate Paleontology 16:65A66A.Google Scholar
Sidor, C. A., and Hopson, J. A. 1998. Ghost lineages and “mammalness”: assessing the temporal pattern of character acquisition in the Synapsida. Paleobiology 24:254273.CrossRefGoogle Scholar
Sigogneau-Russell, D. 1989. Theriodontia B/I. Pp. 1127in Wellnhofer, P., ed. Encyclopedia of paleoherpetology, Part 17B. Gustav Fischer, Stuttgart.Google Scholar
Sokal, R. R., and Rohlf, F. J. 1995. Biometry, 3d ed.W. H. Freeman, New York.Google Scholar
Snyder, R. C. 1962. Adaptations for bipedal locomotion of lizards. American Zoologist 2:191203.CrossRefGoogle Scholar
Sues, H.-D. 1986. Locomotion and body form in early Therapsida (Dinocephalia, Gorgonopsia, and Therocephalia). Pp. 6170in Hotton, N. III, MacLean, P. D., Roth, J. J., and Roth, E. C., eds. The ecology and biology of mammal-like reptiles. Smithsonian Institution Press, Washington, D.C.Google Scholar
Swartz, S. M., Bennett, M. B., and Carrier, D. R. 1992. Wing bone stresses in free flying bats and the evolution of skeletal design for flight. Nature 359:726729.CrossRefGoogle ScholarPubMed
Thomason, J. J. 1985. Estimation of locomotory forces and stresses in the limb bones of Recent and extinct equids. Paleobiology 11:209220.CrossRefGoogle Scholar
Tsutakawa, R. K., and Hewett, J. E. 1977. Quick test for comparing two populations with bivariate data. Biometrics 33:215219.Google Scholar
Wainwright, S. A., Biggs, W. D., Currey, J. D., and Gosline, J. M. 1976. Mechanical design in organisms. Princeton University Press, Princeton, N.J.Google Scholar
Walker, R. 1985. A guide to the post-cranial bones of east African animals. Hylochoerus, Norwich, England.Google Scholar
Wilson, J. A., and Carrano, M. T. 1999. Titanosaurs and the origin of “wide-gauge” trackways: a biomechanical and systematic perspective on sauropod locomotion. Paleobiology 25:252267.CrossRefGoogle Scholar