Evolution of limb design across divergent locomotor modes: loading, posture, and safety factors

Terrestrial vertebrates use limbs for diverse styles of locomotion, from the slow steps of turtles to the explosive jumps of frogs, and from the sprawling posture of amphibians and reptiles (with legs held out to the side of the body) to the fully upright posture of some mammals (with legs held beneath the body). Work from our lab has shown that differences in posture between lineages can lead to dramatic differences in the loads that their limb bones must withstand. In contrast to the predominant anteroposterior (AP) bending experienced in limb bones of upright, cursorial mammals, our in vivo bone strain experiments and synchronized high-speed video and force platform recordings show that the hindlimb bones of species using sprawling posture, including salamanders, turtles, lizards, and crocodilians, experience major torsion (twisting). Even so, limb bones in these sprawling taxa have much greater safety factors (margin of safety against failure) than mammalian limb bones (Blob and Biewener, 1999, 2001; Reilly et al., 2005; Butcher and Blob, 2008; Butcher et al., 2008; Sheffield and Blob, 2011; Sheffield et al., 2011; Blob et al., 2014; Copploe et al., 2015).

To better evaluate when these contrasting loading patterns evolved, we measured forces and strains from the femur of opossums, mammals that are an outgroup to previously studied ungulates and carnivorans, and which use a crouched posture with near parasagittal limb movements (similar to other mammals), but a more horizontal femur. We found high levels of femoral torsion and high safety factors, similar to those in amphibians and reptiles (Butcher et al., 2011; Gosnell et al., 2011). The persistence of these features from amphibians into marsupial mammals indicates that they are ancestral characteristics of tetrapod locomotion, and that aspects of skeletal loading in cursorial mammals that were long regarded as typical across terrestrial lineages are, in fact, restricted derived features (Blob et al., 2014). Crouched posture also led to mediolateral (ML) bending in the opossum femur, in contrast to cursorial mammals. This loading regime could help to explain the curious anteroposteriorly flattened cross-sections of the femur in therapsid ancestors of mammals, as such shapes are suited to resist ML bending.

Current directions

• Comparisons of in vivo bone strains from the forelimbs and hindlimbs of amphibians and reptiles to test Alexander’s "Mixed Chain Hypothesis,” which predicts that structures within the body should have similar safety factors unless loads are highly variable (Blob et al., 2014).

• PhD student Sandy Kawano is comparing skeletal loading between salamander forelimbs and mudskipper pectoral fins, forming a basis for a computational model of changes in bone stress that affected skeletal design through the fish-to-tetrapod transition in the fossil record (Kawano and Blob, 2013).

This material is based upon work supported by the National Science Foundation under Grant No. 0517340. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author and do not necessarily reflect the views of the National Science Foundation.

Related Publications

Blob, R. W. and A. A. Biewener. 1999. In vivo locomotor strain in the hind limb bones of Alligator mississipiensis and Iguana iguana: implications for the evolution of limb bone safety factor and non-sprawling limb posture. Journal of Experimental Biology 202: 1023-1046. Available HERE

Blob, R. W. 2001. Evolution of hindlimb posture in non-mammalian therapsids: biomechanical tests of paleontological hypotheses. Paleobiology 27: 14-38. Available HERE

Blob, R. W. and A. A. Biewener. 2001. Mechanics of limb bone loading during terrestrial locomotion in the green iguana (Iguana iguana) and American alligator (Alligator mississippiensis). Journal of Experimental Biology 204: 1099-1122. Available HERE

Blob, R. W., N. R. Espinoza, M. T. Butcher, A. H. Lee, A. R. D’Amico, F. Baig, K. M. Sheffield. 2014. Diversity of limb bone safety factors for locomotion in terrestrial vertebrates: evolution and mixed chains. Integrative and Comparative Biology 54:1058-1071. Available HERE

Blob, R. W., T. E. Higham. 2014. Terrestrial locomotion—where do we stand, where are we going? An introduction to the symposium. Integrative and Comparative Biology 54:1051-1057. Available HERE

Butcher, M. T. and Blob, R. W. 2008. Mechanics of limb bone loading during terrestrial locomotion in river cooter turtles (Pseudemys concinna). Journal of Experimental Biology 211: 1187-1202. Available HERE (corregendium)

Butcher, M. T., Espinoza, N. R., Cirilo, S. R., Blob, R. W. 2008. In vivo strains in the femur of river cooter turtles (Pseudemys concinna) during terrestrial locomotion: tests of force-platform models of loading mechanics. Journal of Experimental Biology 211: 2397-2407. Available HERE

Butcher, M. T., B. J. White, N. B. Hudzik, W. C. Gosnell, J. H. A. Parrish, R. W. Blob. 2011. In vivo strains in the femur of the Virginia opossum (Didelphis virginiana) during terrestrial locomotion: testing hypotheses of evolutionary shifts in mammalian bone loading and design. Journal of Experimental Biology 214: 2631-2640. Available HERE

Copploe, J. V. II., R. W. Blob, J. H. A. Parrish, M. T. Butcher. 2015. In vivo strains in the femur of the nine-banded armadillo (Dasypus novemcinctus). Journal of Morphology 276:889-899. Available HERE

Gosnell, W. C., M. T. Butcher, T. Maie, R. W. Blob. 2011. Femoral loading mechanics in the Virginia opossum (Didelphis virginiana): torsion and mediolateral bending in mammalian locomotion. Journal of Experimental Biology 214: 3455-3466. Available HERE

Kawano, S. M., R. W. Blob. 2013. Propulsive forces of mudskipper fins and salamander limbs during terrestrial locomotion: implications for the invasion of land. Integrative and Comparative Biology 53:283-294. Available HERE

Reilly, S. M. and R. W. Blob. 2003. Motor control of locomotor hindlimb posture in the American alligator (Alligator mississippiensis). Journal of Experimental Biology 206: 4327-4340. Available HERE

Reilly, S. M., J. S. Willey , A. R. Biknevicius, and R. W. Blob. 2005. Locomotor dynamics in a semi-erect posture: integrating movements, motor patterns, ground reaction forces and bone strains of hindlimb locomotion in the alligator. Journal of Experimental Biology 208: 993-1009. Available HERE

Schoenfuss, H. L., J. D. Roos, A. R. V. Rivera, R. W. Blob. 2010. Motor patterns of distal hind limb muscles in walking turtles: implications for models of limb bone loading. Journal of Morphology 271: 1527-1536. Available HERE

Sheffield, K. M., R. W. Blob. 2011. Loading mechanics of the femur in tiger salamanders (Ambystoma tigrinum) during terrestrial locomotion. Journal of Experimental Biology 214: 2603-2615. Available HERE

Sheffield, K. M., M. T. Butcher, S. K. Shugart, J. C. Gander, R. W. Blob. 2011. Locomotor loading mechanics in the hindlimbs of tegu lizards (Tupinambis merianae): comparative and evolutionary implications. Journal of Experimental Biology 214: 2616-2630. Available HERE

Wilson, M. P., N. R. Espinoza, S. R. Shah, R. W. Blob. 2009. Mechanical properties of the hindlimb bones of bullfrogs and cane toads in bending and torsion. The Anatomical Record 292: 935-944. Available HERE