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      Walking Like Dinosaurs: Chickens with Artificial Tails Provide Clues about Non-Avian Theropod Locomotion

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          Abstract

          Birds still share many traits with their dinosaur ancestors, making them the best living group to reconstruct certain aspects of non-avian theropod biology. Bipedal, digitigrade locomotion and parasagittal hindlimb movement are some of those inherited traits. Living birds, however, maintain an unusually crouched hindlimb posture and locomotion powered by knee flexion, in contrast to the inferred primitive condition of non-avian theropods: more upright posture and limb movement powered by femur retraction. Such functional differences, which are associated with a gradual, anterior shift of the centre of mass in theropods along the bird line, make the use of extant birds to study non-avian theropod locomotion problematic. Here we show that, by experimentally manipulating the location of the centre of mass in living birds, it is possible to recreate limb posture and kinematics inferred for extinct bipedal dinosaurs. Chickens raised wearing artificial tails, and consequently with more posteriorly located centre of mass, showed a more vertical orientation of the femur during standing and increased femoral displacement during locomotion. Our results support the hypothesis that gradual changes in the location of the centre of mass resulted in more crouched hindlimb postures and a shift from hip-driven to knee-driven limb movements through theropod evolution. This study suggests that, through careful experimental manipulations during the growth phase of ontogeny, extant birds can potentially be used to gain important insights into previously unexplored aspects of bipedal non-avian theropod locomotion.

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          Most cited references 18

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          The origin and early evolution of birds

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            Caudofemoral musculature and the evolution of theropod locomotion

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              The aging of Wolff's "law": ontogeny and responses to mechanical loading in cortical bone.

              The premise that bones grow and remodel throughout life to adapt to their mechanical environment is often called Wolff's law. Wolff's law, however, is not always true, and in fact comprises a variety of different processes that are best considered separately. Here we review the molecular and physiological mechanisms by which bone senses, transduces, and responds to mechanical loads, and the effects of aging processes on the relationship (if any) between cortical bone form and mechanical function. Experimental and comparative evidence suggests that cortical bone is primarily responsive to strain prior to sexual maturity, both in terms of the rate of new bone growth (modeling) as well as rates of turnover (Haversian remodeling). Rates of modeling and Haversian remodeling, however, vary greatly at different skeletal sites. In addition, there is no simple relationship between the orientation of loads in long bone diaphyses and their cross-sectional geometry. In combination, these data caution against assuming without testing adaptationist views about form-function relationships in order to infer adult activity patterns from skeletal features such as cross-sectional geometry, cortical bones density, and musculo-skeletal stress markers. Efforts to infer function from shape in the human skeleton should be based on biomechanical and developmental models that are experimentally tested and validated.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                5 February 2014
                : 9
                : 2
                Affiliations
                [1 ]Institute of Ecology and Biodiversity, Facultad de Ciencias, Universidad de Chile, Santiago, Chile
                [2 ]Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, Santiago, Chile
                [3 ]Department of Oral Biology, University of Illinois at Chicago, Chicago, Illinois, United States of America
                [4 ]Department of Organismal Biology and Anatomy, University of Chicago, Chicago, Illinois, United States of America
                Raymond M. Alf Museum of Paleontology, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: BG JID RAV. Performed the experiments: BG OL. Analyzed the data: BG JID MC RAV. Wrote the paper: BG JID RAV.

                Article
                PONE-D-13-31751
                10.1371/journal.pone.0088458
                3915051

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Pages: 6
                Funding
                This study was supported by the Institute of Ecology and Biodiversity, grants ICM-05-002 and PFB-23 CONICYT ( http://www.conicyt.cl/), FONDECYT ( http://www.conicyt.cl/fondecyt/) grants No. 1020550, 1060186, and 1090764 to RAV, and the 2004 BBVA prize. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Anatomy and Physiology
                Musculoskeletal System
                Biomechanics
                Integrative Physiology
                Evolutionary Biology
                Organismal Evolution
                Animal Evolution
                Paleontology
                Paleobiology
                Zoology
                Animal Physiology
                Ornithology

                Uncategorized

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