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Evolution and Function of the Hominin Forefoot

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Evolution and Function of the Hominin Forefoot Evolution and function of the hominin forefoot Peter J. Fernándeza,b,1, Carrie S. Monglec, Louise Leakeyd,e, Daniel J. Proctorf, Caley M. Orrg,h, Biren A. Pateli,j, Sergio Almécijak,l,m, Matthew W. Tocherin,o, and William L. Jungersa,p aDepartment of Anatomical Sciences, Stony Brook University, Stony Brook, NY 11794; bDepartment of Biomedical Sciences, Marquette University, Milwaukee, WI 53202; cInterdepartmental Doctoral Program in Anthropological Sciences, Stony Brook University, Stony Brook, NY 11794; dDepartment of Anthropology, Stony Brook University, Stony Brook, NY 11794; eTurkana Basin Institute, Stony Brook University, Stony Brook, NY 11794; fDepartment of Anthropology, Lawrence University, Appleton, WI 54911; gDepartment of Cell and Developmental Biology, University of Colorado School of Medicine, Aurora, CO 80045; hDepartment of Anthropology, University of Colorado Denver, Denver, CO 80204; iDepartment of Integrative Anatomical Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033; jHuman and Evolutionary Biology Section, Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089; kDivision of Anthropology, American Museum of Natural History, New York, NY 10024; lCenter for the Advanced Study of Human Paleobiology, Department of Anthropology, The George Washington University, Washington, DC 20052; mInstitut Català de Paleontologia Miquel Crusafont (ICP), Universitat Autònoma de Barcelona, 08193 Cerdanyola del Vallès, Barcelona, Spain; nDepartment of Anthropology, Lakehead University, Thunder Bay, ON P7B 5E1, Canada; oHuman Origins Program, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013; and pAssociation Vahatra, Antananarivo 101, Madagascar Edited by Bruce Latimer, Case Western Reserve University, Cleveland, OH, and accepted by Editorial Board Member C. O. Lovejoy July 12, 2018 (received for review January 15, 2018) The primate foot functions as a grasping organ. As such, its bones, of humans and chimpanzees has shown that dorsal doming is soft tissues, and joints evolved to maximize power and stability in correlated with in vivo ranges of motion at the MTPJs, with a variety of grasping configurations. Humans are the obvious humans displaying greater doming and a greater range of MTPJ exception to this primate pattern, with feet that evolved to support dorsiflexion during bipedalism (9). the unique biomechanical demands of bipedal locomotion. Of key The form and function of the hominin forefoot have been studied functional importance to bipedalism is the morphology of the joints extensively(5,6,13–16), especially in light of more recent discov- at the forefoot, known as the metatarsophalangeal joints (MTPJs), eries of hominin pedal fossils (17–19). However, a quantitative but a comprehensive analysis of hominin MTPJ morphology is currently analysis of the hominin forefoot in a broad phylogenetic context is lacking. Here we present the results of a multivariate shape and lacking, despite the theorized importance of these bony elements to Bayesian phylogenetic comparative analyses of metatarsals (MTs) from the biomechanical demands of bipedalism (10, 20). To better un- a broad selection of anthropoid primates (including fossil apes and derstand the adaptive evolution of bipedalism in early hominins we stem catarrhines) and most of the early hominin pedal fossil record, investigated MTPJ morphology in Plio-Pleistocene fossil hominins (including species of Ardipithecus, Australopithecus, Paranthropus, including the oldest hominin for which good pedal remains exist, Homo Ardipithecus ramidus. Results corroborate the importance of specific and ) and a comparative sample of fossil and extant anthro- bony morphologies such as dorsal MT head expansion and “doming” poids (including modern humans, apes, and monkeys) using shape to the evolution of terrestrial bipedalism in hominins. Further, our evo- analyses and phylogenetic comparative methods to test hypotheses lutionary models reveal that the MT1 of Ar. ramidus shifts away from about the nature and timing of forefoot evolution in the human clade. Three-dimensional geometric morphometric techniques were the reconstructed optimum of our last common ancestor with apes, – but not necessarily in the direction of modern humans. However, the used to quantify MT1 MT5 head shapes, and a multioptima Ornstein- Uhlenbeck (OU) model was used to estimate the placement and lateral rays of Ar. ramidus are transformed in a more human-like direc- tion, suggesting that they were the digits first recruited by hominins into the primary role of terrestrial propulsion. This pattern of evolu- Significance tionary change is seen consistently throughout the evolution of the foot, highlighting the mosaic nature of pedal evolution and the emer- A critical step in the evolutionary history leading to the origins of gence of a derived, modern hallux relatively late in human evolution. humankind was the adoption of habitual bipedal locomotion by our hominin ancestors. We have identified novel bony shape bipedalism | hominin evolution | metatarsals | Ardipithecus | variables in the forefoot across extant anthropoids and extinct functional morphology hominins that are linked functionally to the emergence of bipedal walking. Results indicate a consistent and generalizable pattern in Ardipithecus he obligate terrestrial bipedalism of modern humans is hominin pedal evolution that spans from to early Homo— Tunique among extant primates, and its ancient adoption by the relatively late derivation of a modern hallux in com- early hominins impacted subsequent evolutionary changes in parison with the lateral rays. These data provide novel morpho- social behavior and the development of material culture. A suite logical and macroevolutionary evidence for how and when the of morphological changes in the feet of early hominins is asso- hominin pedal skeleton evolved to accommodate the unique biomechanical demands of bipedalism. ciated with the evolution of habitual bipedal locomotion in the human career and ultimately led to the energetically efficient Author contributions: P.J.F., S.A., and W.L.J. designed research; P.J.F. and C.S.M. per- gait used by modern humans (1–5). formed research; P.J.F., C.S.M., L.L., D.J.P., C.M.O., B.A.P., S.A., M.W.T., and W.L.J. contrib- The forefoot skeleton includes the metatarsals (MT) and uted new reagents/analytic tools; P.J.F. and C.S.M. analyzed data; and P.J.F., C.S.M., and phalanges, and its functional anatomy is strongly tied to the W.L.J. wrote the paper with input from all authors. evolution of bipedalism in hominins (5–9). Thus, hominin fore- The authors declare no conflict of interest. foot fossils can offer key insights into when and how bipedalism This article is a PNAS Direct Submission. B.L. is a guest editor invited by the Editorial evolved in the human lineage. During bipedal walking, modern Board. humans dorsiflex (i.e., hyperextend) their forefoot joints, spe- Published under the PNAS license. cifically at the metatarsophalangeal joints (MTPJs), as part of Data deposition: The raw data are available through Open Science Framework (https:// the push-off phase of gait, which tightens plantar soft tissues to osf.io/4fc7b/). convert the foot into a relatively stiff, propulsive lever (10) (also 1To whom correspondence should be addressed. Email: pedro.fernandez@marquette. see ref. 11). Features of MT head morphology such as “dorsal edu. doming” are thought to facilitate this stiffening mechanism (6, This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. 12); doming occurs when the distal articular surface expands and 1073/pnas.1800818115/-/DCSupplemental. becomes particularly pronounced dorsally. Comparative analysis Published online August 13, 2018. 8746–8751 | PNAS | August 28, 2018 | vol. 115 | no. 35 www.pnas.org/cgi/doi/10.1073/pnas.1800818115 Downloaded by guest on October 2, 2021 magnitude of adaptive shifts in the evolution of MTPJ morphology 23–29% and 12–16% of total variance, respectively) track MT for each toe (21). To better calibrate the ancestral state estimation head orientation and robusticity in a pattern similar to that of the chimpanzee-human and other last common ancestors found by previous research (ref. 8 and Fig. 1). Because the fifth (LCAs), stem catarrhines (e.g., Catopothecus, Epipliopithecus)and MTPJ (MTPJ5) plays a relatively reduced role in bipedal forefoot Miocene apes (e.g., Ekembo sp.) were also included in the analysis. mechanics (9), results for MT5 are not reported in further detail. Although the distal half of the MTPJ joint, the proximal phalangeal PC1 primarily explains variance in MT head shape that is related base, also plays an important role in the articular mechanics of the to expanded articular surfaces (i.e., robusticity). For MT1, as an hominin forefoot (6, 7), a comprehensive analysis of its articular example, high PC1 scores reflect dorsally wider hallucal heads and surface is outside the scope of this study. Moreover, hominin fore- broader plantar surfaces with shallow grooves for the sesamoids, a foot fossils are typically found in isolation, and thus it is informative pattern particularly pronounced in the modern human sample. to discern to what extent locomotor behavior in these extinct Shape warps constructed in 3D using low PC1 scores display groups can be determined from single, isolated elements. Finally, marked plantar wedging of the MT head, with strongly angled there
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