Cortical Structure of Hallucal Metatarsals and Locomotor Adaptations in Hominoids

January Cortical Structure of Hallucal Metatarsals and Locomotor Adaptations in Hominoids Tea Jashashvili 0 1 2 Mark R. Dowdeswell 0 1 2 Renaud Lebrun 0 1 2 Kristian J. Carlson 0 1 2 0 1 Evolutionary Studies Institute, University of the Witwatersrand , Wits , South Africa , 2 Department of Geology and Palaeontology, Georgian National Museum , Tbilisi , Georgia , 3 School of Statistics and Actuarial Science, University of the Witwatersrand , Wits , South Africa , 4 Institut des Sciences de l'Evolution de Montpellier-UMR 5554, Montpellier, France, 5 Department of Anthropology, Indiana University , Bloomington, Indiana , United States of America 1 Funding: TJ was funded by a post-doctoral fellowship from the Claude Leon Foundation and the Strategic Planning and Allocation of Resources Committee at the University of the Witwatersrand. The South African Department of Science and Technology and the National Research Foundation, as well as the Centre of Excellence in Palaeosciences and the Evolutionary Studies Institute at the University of the Witwatersrand provided funding in support of the Virtual Imaging in Palaeosciences laboratory. The funders had no role 2 Academic Editor: Luc Malaval, Universite de Lyon-Universite Jean Monnet , FRANCE Diaphyseal morphology of long bones, in part, reflects in vivo loads experienced during the lifetime of an individual. The first metatarsal, as a cornerstone structure of the foot, presumably expresses diaphyseal morphology that reflects loading history of the foot during stance phase of gait. Human feet differ substantially from those of other apes in terms of loading histories when comparing the path of the center of pressure during stance phase, which reflects different weight transfer mechanisms. Here we use a novel approach for quantifying continuous thickness and cross-sectional geometric properties of long bones in order to test explicit hypotheses about loading histories and diaphyseal structure of adult chimpanzee, gorilla, and human first metatarsals. For each hallucal metatarsal, 17 cross sections were extracted at regularly-spaced intervals (2.5% length) between 25% and 65% length. Cortical thickness in cross sections was measured in one degree radially-arranged increments, while second moments of area were measured about neutral axes also in one degree radially-arranged increments. Standardized thicknesses and second moments of area were visualized using false color maps, while penalized discriminant analyses were used to evaluate quantitative species differences. Humans systematically exhibit the thinnest diaphyseal cortices, yet the greatest diaphyseal rigidities, particularly in dorsoplantar regions. Shifts in orientation of maximum second moments of area along the diaphysis also distinguish human hallucal metatarsals from those of chimpanzees and gorillas. Diaphyseal structure reflects different loading regimes, often in predictable ways, with human versus non-human differences probably resulting both from the use of arboreal substrates by non-human apes and by differing spatial relationships between hallux position and orientation of the substrate reaction resultant during stance. The novel morphological approach employed in this study offers the potential for transformative insights into form-function relationships in additional long bones, including those of extinct organisms (e.g., fossils). - in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Humans exhibit a unique foot structure that is distinct from African ape foot structure [14]. The presence and unique form of longitudinal and transverse bony arches, midfoot stability (as opposed to midfoot mobility in the calcaneocuboid and cuboid-metatarsal joints), loss of an opposable hallux, and shortening of pedal phalanges are some of the skeletal features distinguishing human foot form [514]. Accompanying unique ligamentous structures (e.g., plantar aponeurosis and long plantar ligament) reinforce the bony arches, also distinguishing human foot design from that of other apes [11], [1519]. Exactly when these unique features emerged within human evolutionary history is still vigorously debated, but the selective reasons for their differentiation (i.e., confer structural advantages during terrestrial bipedalism) are widely accepted [2023]. Attempts to quantify internal stresses and joint motions within the foot have been rare [24 25] due to the difficult nature of analyzing in vivo foot mechanics without disrupting normal function. Rather, much of the information on loading patterns experienced by the foot has been derived from in vitro cadaver studies [2627] or studies of external pressure and foot kinematics [8], [2830]. That the human hallux functions comparatively better as a stable lever in a metatarsi-fulcrimating foot is likely a consequence of selection favoring a more medial and stereotyped path of the center of pressure during human bipedalism compared to the more lateral and variable path of the center of pressure observed during Pan terrestrial bipedalism or quadrupedalism [8], [2830]. This difference is accentuated even more by speed (i.e., during higher pressures) since the center of pressure in the human foot follows an even more medial trajectory at faster speeds [11]. The comparatively more medial position of the center of pressure during stance would facilitate more close-packing of joints comprising the human bony longitudinal arch and elastic energy return from its associated ligamentous structures such as the plantar aponeurosis [11], [15], [1718]. A comparatively robust and adducted human hallux is thought to reflect a unique human toe-off mechanism during terminal stance phase of bipedal gaits [6], [28], [31], whereas the forefoot configuration of other hominoids, particularly their less robust and abducted first ray, is thought to reflect a design for accommodating retained grasping capabilities [32]. Indeed, these different configurations result in the functional comparability of dorsoplantar cortices of human hallucal metatarsals and ML cortices in chimpanzee hallucal metatarsals due to internal rotation of the abducted hallux in the grasping foot [33 34]. Greater midshaft robusticity of the human hallucal metatarsal compared to those of other apes [3435] would result in the former being better-suited to resist comparatively higher loading (bending) experienced during the last half of stance ending with toe-off. Moreover, since the path of the center of pressure during human stance remains comparatively medial and thus more parallel to the longitudinal axis of the hallucal metatarsal from initial contact between the forefoot and the ground at foot flat (i.e., the point when pressure initially appears below the hallucal metatarsal head) until the heel lifts and toe-off occurs [11], [29], bending experie (...truncated)