Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-26T13:15:21.722Z Has data issue: false hasContentIssue false
  • English
  • Français

Phylogenetic variation in hind-limb bone scaling of flightless theropods

Published online by Cambridge University Press:  24 November 2016

Nicholas R. Chan
Nicholas R. Chan*
Affiliation:
Department of Biological Sciences, Macquarie University, Sydney, New South Wales 2109, Australia. E-mail: nicholas.chan2@students.mq.edu.au
Get access Rights & Permissions [Opens in a new window]

Abstract

The robusticity of the weight-bearing limbs of large terrestrial animals is expected to increase at a more rapid rate than in their smaller relatives. This scaling has been hypothesized to allow large species to maintain stresses in the limb bones that are similar to those seen in smaller ones. Curvilinear scaling has previously been found in mammals and nonavian theropods but has not been demonstrated in birds. In this study, polynomial regressions of leg-bone length and circumference in terrestrial flightless birds were carried out to test for a relationship similar to that seen in nonavian theropods. Flightless birds exhibit curvilinear scaling, with the femora of large taxa becoming thicker relative to length at a greater rate than in smaller taxa. Evidence was found for nonlinear scaling in the leg bones of nonavian theropods. However, unlike in avians, there is also phylogenetic variation between taxonomic groups, with tyrannosaur leg bones in particular scaling differently than other groups. Phylogenetically corrected quadratic regressions and separate analyses of taxonomic groupings found little phylogenetic variation in flightless birds. It is suggested here that the nonlinear scaling seen in avian femora is due to the need to maintain the position of the knee under a more anterior center of mass, thereby restricting femoral length. The femur of nonavian theropods is not so constrained, with greater variability of the linear scaling relationships between clades. Phylogenetic variation in limb-bone scaling may broaden the errors for mass-predictive scaling equations based on limb-bone measurements of nonavian theropods.

Type
Articles
Information
Paleobiology , Volume 43 , Issue 1 , February 2017 , pp. 129 - 143
Copyright
Copyright © 2016 The Paleontological Society. All rights reserved 

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

Akaike, H. 1973. Information theory and an extension of the maximum likelihood principle. Pp. 267–281. In B. N. Petrov, and F. Csáki, eds. Second International Symposium on Information Theory, Budapest. Akadémiai Kiadó, Budapest.Google Scholar
Alexander, R. McN. 1977. Allometry of the limbs of antelopes (Bovidae). Journal of Zoology 183:125–146.CrossRefGoogle Scholar
Allen, V., Bates, K. T., Li, Z., and Hutchinson, J. R.. 2013. Linking the evolution of body shape and locomotor biomechanics in bird-line archosaurs. Nature 497:104–107.Google Scholar
Anderson, J. F., Hall-Martin, A., and Russell, D. A.. 1985. Long-bone circumference and weight in mammals, birds and dinosaurs. Journal of Zoology 207:53–61.Google Scholar
Amadon, D. 1947. An estimated weight of the largest known bird. Condor 49:159–164.CrossRefGoogle Scholar
Bapst, D. W. 2012. Paleotree: paleontological and phylogenetic analyses of evolution. Methods in Ecology and Evolution 3:803–807.CrossRefGoogle Scholar
Baum, B. R. 1992. Combining trees as a way of combining data sets for phylogenetic inference, and the desirability of combining gene trees. Taxon 41:3–10.CrossRefGoogle Scholar
Baumel, J. J., and Witmer, L. M.. 1993. Osteologia. Pp. 45–132. In J. J. Baumel, A. S. King, J. E. Breazile, H. E. Evans, and J. C. Vanden Berge, eds. Handbook of avian anatomy: nomina anatomica avium. Publications of the Nuttall Ornithological Club 23, Cambridge, Mass.Google Scholar
Benjamini, Y., and Hochberg, Y.. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (Methodological) 57:289–300.Google Scholar
Benson, R. B. J. 2010. A description of Megalosaurus bucklandii (Dinosauria: Theropoda) from the Bathonian of the UK and the relationships of Middle Jurassic theropods. Zoological Journal of the Linnean Society 158:882–935.Google Scholar
Benson, R. B. J., and Choiniere, J. N.. 2013. Rates of dinosaur limb evolution provide evidence for exceptional radiation in Mesozoic birds. Proceedings of the Royal Society B 280:20131780.Google Scholar
Benson, R. B. J., Rich, T. H., Vickers-Rich, P., and Hall, M.. 2012. Theropod fauna from South Australia indicates high polar diversity and climate-driven dinosaur provinciality. PLoS ONE 7:e37122. doi:10.1371/journal.pone.0037122.CrossRefGoogle ScholarPubMed
Benson, R. B. J., Campione, N. E., Carrano, M. T., Mannion, P. D., Sullivan, C., Upchurch, P., and Evans, D. C.. 2014. Rates of dinosaur body mass evolution indicate 170 million years of sustained ecological innovation on the avian stem lineage. PLoS Biology 12:e1001853. doi:10.1371/journal.pbio.1001853.CrossRefGoogle ScholarPubMed
Bertram, J. E. A, and Biewener, A. A.. 1990. Differential scaling of the long bones in the terrestrial Carnivora and other mammals. Journal of Morphology 204:157–169.CrossRefGoogle Scholar
Biewener, A. A. 1982. Bone strength in small mammals and bipedal birds: do safety factors change with body size? Journal of Experimental Biology 98:289–301.CrossRefGoogle ScholarPubMed
Biewener, A. A. 1989. Scaling body support in mammals: limb posture and muscle mechanics. Science 245:45–48.Google Scholar
Biewener, A. A. 1990. Biomechanics of mammalian terrestrial locomotion. Science 250:1097–1103.CrossRefGoogle ScholarPubMed
Biewener, A. A., and Dial, K. P.. 1995. In vivo strain in the humerus of pigeons (Columba livia) during flight. Journal of Morphology 225:61–75.CrossRefGoogle Scholar
Brusatte, S. L., Lloyd, G. T., Wang, S. C., and Norell, M. A.. 2014. Gradual assembly of the avian body plan culminated in rapid rates of evolution across the dinosaur–bird transition. Current Biology 24:1–7.CrossRefGoogle ScholarPubMed
Campione, N. E., and Evans, D. C.. 2012. A universal scaling relationship between body mass and proximal limb bone dimensions in quadrupedal terrestrial tetrapods. BMC Biology 10:60.CrossRefGoogle ScholarPubMed
Campione, N. E., Evans, D. C., Brown, C. M., and Carrano, M. T.. 2014. Body mass estimation in non-avian bipeds using a theoretical conversion to quadruped stylopodial proportions. Methods in Ecology and Evolution 5:913–923.CrossRefGoogle Scholar
Carrano, M. T. 1998a. Locomotion in non-avian dinosaurs: integrating data from hindlimb kinematics, in vivo strains, and bone morphology. Paleobiology 24:450–469.Google Scholar
Carrano, M. T. 1998b. The evolution of dinosaur locomotion: biomechanics, functional morphology, and modern analogs. Ph.D. thesis. University of Chicago, Chicago, Ill.Google Scholar
Carrano, M. T. 2001. Implications of limb bone scaling, curvature and eccentricity in mammals and non-avian dinosaurs. Journal of Zoology 254:41–55.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 240:237–249.Google Scholar
Christiansen, P. 1999a. Long bone scaling and limb bone posture in non-avian theropods: Evidence for differential allometry. Journal of Vertebrate Paleontology 19:666–680.CrossRefGoogle Scholar
Christiansen, P. 1999b. Scaling of the limb long bones to body mass in terrestrial mammals. Journal of Morphology 239:167–190.Google Scholar
Christiansen, P. 1999c. Scaling of mammalian long bones: small and large mammals compared. Journal of Zoology 247:333–348.CrossRefGoogle Scholar
Christiansen, P., and Fariña, R. A.. 2004. Mass prediction in theropod dinosaurs. Historical Biology 16:85–92.CrossRefGoogle Scholar
Cowin, S. C. 1987. Bone remodelling of diaphyseal surfaces by torsional loads: theoretical predictions. Journal of Biomechanics 20:1111–1120.Google Scholar
Dececchi, T. A., and Larsson, H. C. E.. 2013. Body and limb size dissociation at the origin of birds: uncoupling allometric constraints across a macroevolutionary transition. Evolution 67:2741–2752.CrossRefGoogle ScholarPubMed
De Margerie, E., Sanchez, S., Cubo, J., and Castanet, J.. 2005. Torsional resistance as a principal component of the structural design of long bones: comparative multivariate evidence in birds. Anatomical Record A 282A:49–66.CrossRefGoogle Scholar
Doube, M., Yen, S. C. W., Kłosowski, M. M., Farke, A. A., Hutchinson, J. R., and Shefelbine, S. J.. 2012. Whole-bone scaling of the avian pelvic limb. Journal of Anatomy 221:21–29.Google Scholar
Dunning, J. B. Jr. 2007. CRC Handbook of avian body masses, Second edition. CRC Press, Bacon Raton, Florida.CrossRefGoogle Scholar
Field, D. J., Lynner, C., Brown, C., and Darroch, S.A. F.. 2013. Skeletal correlates for body mass estimation in modern and fossil flying birds. PLoS One 8:e82000. doi: doi:10.1371/journal.pone.0082000.Google Scholar
Gatesy, S. M. 1990. Caudofemoral musculature and the evolution of theropod locomotion. Paleobiology 16:170–186.Google Scholar
Gatesy, S. M. 1991. Hind limb scaling in birds and other theropods: implications for terrestrial locomotion. Journal of Morphology 209:83–96.Google Scholar
Gatesy, S. M., and Biewener, A. A.. 1991. Bipedal locomotion: effects of speed, size and limb posture in birds and humans. Journal of Zoology 224:127–147.Google Scholar
Gatesy, S. M., and Middleton, K. M.. 1997. Bipedalism, flight, and the evolution of theropod locomotor diversity. Journal of Vertebrate Paleontology 17:308–329.Google Scholar
Grossi, B., Iriarte-Diaz, J., Larach, O., Canals, M., and Vásquez, R. A.. 2014. Walking like dinosaurs: chickens with artificial tails provide clues about non-avian theropod locomotion. PLoS ONE 9:e88458. doi:10.1371/journal.pone.0088458.Google Scholar
Heupink, T. H., Huynen, L., and Lambert, D. M.. 2011. Ancient DNA suggests dwarf and “giant” emu are conspecific. PLoS ONE 6:e18728. doi:10.1371/journal.pone.0018728.CrossRefGoogle ScholarPubMed
Hurvich, C. M., and Tsai, C. L.. 1989. Regression and time series model selection in small samples. Biometrika 76:297–307.CrossRefGoogle Scholar
Hutchinson, J. R. 2001. The evolution of femoral osteology and soft tissues on the line to extant birds (Neornithes). Zoological Journal of the Linnean Society 131:169–197.CrossRefGoogle Scholar
Hutchinson, J. R. 2004. Biomechanical modelling and sensitivity analysis of bipedal running ability. II. Extinct taxa. Journal of Morphology 262:441–461.Google Scholar
Hutchinson, J. R., and Allen, V.. 2009. The evolutionary continuum of limb function from early theropods to birds. Naturwissenschaften 96:423–448.Google Scholar
Hutchinson, J. R., and Gatesy, S. M.. 2000. Adductors, abductors, and the evolution of archosaur locomotion. Paleobiology 26:734–751.2.0.CO;2>CrossRefGoogle Scholar
Huxley, T. H. 1868. On the animals which are most nearly intermediate between the birds and reptiles. Geological Magazine 5:357–365.Google Scholar
Huxley, T. H. 1870. Further evidence of the affinities between the dinosaurian reptiles and birds. Quarterly Journal of the Geological Society 26:12–31.CrossRefGoogle Scholar
Jenkins, F. A. Jr. 1993. The evolution of the avian shoulder joint. American Journal of Science 293A:253–267.CrossRefGoogle Scholar
Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K., and Mooers, A. O.. 2012. The global diversity of birds in space and time. Nature 491:444–448.Google Scholar
Kirchman, J. J. 2012. Speciation of flightless rails on islands: a DNA-based phylogeny of the typical rails of the Pacific. Auk 129:56–69.Google Scholar
Kraemer, H. C., and Blasey, C. M.. 2004. Centring in regression analyses: a strategy to prevent errors in statistical inference. International Journal of Methods in Psychiatric Research 13:141–151.Google Scholar
Lamanna, M. C., Sues, H.-D., Schachner, E. R., and Lyson, T. R.. 2014. A new large-bodied oviraptorosaurian theropod dinosaur from the Latest Cretaceous of Western North America. PLoS ONE 9:e92022. doi: doi:10.1371/journal.pone.0092022.Google Scholar
Lee, M. S. Y., Cau, A., Naish, D., and Dyke, G. J.. 2014. Sustained miniaturization and anatomical innovation in the dinosaurian ancestors of birds. Science 345:562.CrossRefGoogle ScholarPubMed
Main, R. P., and Biewener, A. A.. 2007. Skeletal strain patterns and growth in the emu hindlimb during ontogeny. Journal of Experimental Biology 210:2676–2690.Google Scholar
Maloiy, G. M. O., Alexander, R. McN., Njau, R., and Jayes, A. S.. 1979. Allometry of the legs of running birds. Journal of Zoology 187:161–167.CrossRefGoogle Scholar
Mayr, G. 2010. Metaves, Mirandornithes, Strisores and other novelties—a critical review of the higher-level phylogeny of neornithine birds. Journal of Zoological Systematics and Evolutionary Research 49:58–76.Google Scholar
Mayr, G. 2011. Cenozoic mystery birds—on the phylogenetic affinities of bony-toothed birds (Pelagornithidae). Zoologica Scripta 40:448–467.CrossRefGoogle Scholar
Mayr, G. 2014. The origins of crown group birds: molecules and fossils. Palaeontology 57:231–242.Google Scholar
Mazerolle, M. J. 2006. Improving data analysis in herpetology: using Akaike’s Information Criterion (AIC) to assess the strength of biological hypotheses. Amphibia-Reptilia 27:169–180.Google Scholar
Mazerolle, M. J. 2015. AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package, Version 2.0-3. http://CRAN.R project.org/package=AICcmodavg.Google Scholar
McCall, R. A., Nee, S., and Harvey, P. H.. 1998. The role of wing length in the evolution of avian flightlessness. Evolutionary Ecology 12:569–580.Google Scholar
McMahon, T. A. 1973. Size and shape in biology. Science 179:1201–1204.Google Scholar
McMahon, T. A. 1975. Using body size to understand the structural design of animals: quadrupedal locomotion. Journal of Applied Physiology 39:619–627.Google Scholar
Middleton, K. M., and Gatesy, S. M.. 2000. Theropod forelimb design and evolution. Zoological Journal of the Linnean Society 128:149–187.Google Scholar
Murray, P. F., and Vickers-Rich, P.. 2004. Magnificent mihirungs: the colossal flightless birds of the Australian dreamtime. Indiana University Press, Bloomington, Ind.Google Scholar
Naish, D., and Martill, D. M.. 2007. Dinosaurs of Great Britain and the role of the Geological Society of London in their discovery: basal Dinosauria and Saurischia. Journal of the Geological Society 164:493–510.Google Scholar
Nguyen, J. M. T., Boles, W. E., and Hand, S. J.. 2010. New material of Barawertornis tedfordi, a dromornithid bird from the Oligo-Miocene of Australia and its phylogenetic implications. Records of the Australian Museum 62:45–60.CrossRefGoogle Scholar
Ostrom, J. H. 1973. The ancestry of birds. Nature 242:136.CrossRefGoogle Scholar
Ostrom, J. H. 1976. Archaeopteryx and the origin of birds. Biological Journal of the Linnean Society 8:91–182.Google Scholar
Padian, K., and Chiappe, L. M.. 1998. The origin and early evolution of birds. Biological Reviews 73:1–42.Google Scholar
Pinheiro, J., Bates, D., DebRoy, S., and Sarkar, D.. 2014. Nlme: linear and nonlinear mixed effects models. R package, Version 3.1–117. http://CRAN.R-project.org/package=nlme.Google Scholar
Puttick, M. N., Thomas, G. H., and Benton, M. J.. 2014. High rates of evolution preceded the origin of birds. Evolution 68:1497–1510.Google Scholar
Ragan, M. A. 1992. Phylogenetic inference based on matrix representation of trees. Molecular Phylogenetics and Evolution 1:53–58.CrossRefGoogle ScholarPubMed
R Core Development Team. 2014. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Roff, D. A. 1994. The evolution of flightlessness: is history important? Evolutionary Ecology 8:639–657.Google Scholar
Rubenson, J., Lloyd, D. G., Besier, T. F., Heliams, D. B., and Fournier, P. A.. 2007. Running in ostriches (Struthio camelus): three-dimensional joint axes alignment and joint kinematics. Journal of Experimental Biology 210:2548–2562.Google Scholar
Rubin, C. T., and Lanyon, L. E.. 1984. Dynamic strain similarity in vertebrates: an alternative to allometric limb bone scaling. Journal of Theoretical Biology 107:321–327.CrossRefGoogle ScholarPubMed
Senter, P. 2006. Scapular orientation in theropods and basal birds, and the origin of flapping flight. Acta Palaeontologica Polonica 51:305–313.Google Scholar
Stoessel, A., and Fischer, M. S.. 2012. Comparative intralimb coordination in avian bipedal locomotion. Journal of Experimental Biology 215:4055–4069.Google ScholarPubMed
Stoessel, A., Kilbourne, B. M., and Fischer, M. S.. 2013. Morphological integration versus ecological plasticity in the avian pelvic limb skeleton. Journal of Morphology 274:483–495.CrossRefGoogle ScholarPubMed
Turner, A. H., Pol, D., Clarke, J. A., Erickson, G. M., and Norell, M. A.. 2007. A basal dromaeosaurid and size evolution proceeding avian flight. Science 317:1378–1381.Google Scholar
Warton, D. I., Duursma, R. A., Falster, D. S., and Taskinen, S.. 2012. Smatr 3—an R package for estimation and inference about allometric lines. Methods in Ecology and Evolution 3:257–259.Google Scholar
Worthy, T. H., and Scofield, R. P.. 2012. Twenty-first century advances in knowledge of the biology of moa (Aves: Dinornithiformes): a new morphological analysis and moa diagnoses revised. New Zealand Journal of Zoology 39:87–153.CrossRefGoogle Scholar
Worthy, T. H., Hand, S. J., and Archer, M.. 2014. Phylogenetic relationships of the Australian Oligo-Miocene ratite Emuarius gidju Casuariidae. Integrative Zoology 9:148–166.CrossRefGoogle ScholarPubMed
Xu, X., Tan, Q., Wang, J., Zhao, X., and Tan, L.. 2007. A gigantic bird-like dinosaur from the Late Cretaceous of China. Nature 447:844–847.CrossRefGoogle ScholarPubMed
Zeffer, A., Johansson, L. C., and Marmebro, Å.. 2003. Functional correlation between habitat use and leg morphology in birds (Aves). Biological Journal of the Linnean Society 79:461–484.CrossRefGoogle Scholar