Evolution and function of the hominin forefoot (original) (raw)

The primate foot functions as a grasping organ. As such, its bones, soft tissues, and joints evolved to maximize power and stability in a variety of grasping configurations. Humans are the obvious exception to this primate pattern, with feet that evolved to support the unique biomechanical demands of bipedal locomotion. Of key functional importance to bipedalism is the morphology of the joints at the forefoot, known as the metatarsophalangeal joints (MTPJs), but a comprehensive analysis of hominin MTPJ morphology is currently lacking. Here we present the results of a multivariate shape and Bayesian phylogenetic comparative analyses of metatarsals (MTs) from a broad selection of anthropoid primates (including fossil apes and stem catarrhines) and most of the early hominin pedal fossil record, including the oldest hominin for which good pedal remains exist, Ardipithecus ramidus. Results corroborate the importance of specific bony morphologies such as dorsal MT head expansion and "doming" to the evolution of terrestrial bipedalism in hominins. Further, our evolutionary models reveal that the MT1 of Ar. ramidus shifts away from the reconstructed optimum of our last common ancestor with apes, but not necessarily in the direction of modern humans. However, the lateral rays of Ar. ramidus are transformed in a more human-like direction , suggesting that they were the digits first recruited by hominins into the primary role of terrestrial propulsion. This pattern of evolutionary change is seen consistently throughout the evolution of the foot, highlighting the mosaic nature of pedal evolution and the emergence of a derived, modern hallux relatively late in human evolution. bipedalism | hominin evolution | metatarsals | Ardipithecus | functional morphology T he obligate terrestrial bipedalism of modern humans is unique among extant primates, and its ancient adoption by early hominins impacted subsequent evolutionary changes in social behavior and the development of material culture. A suite of morphological changes in the feet of early hominins is associated with the evolution of habitual bipedal locomotion in the human career and ultimately led to the energetically efficient gait used by modern humans (1-5). The forefoot skeleton includes the metatarsals (MT) and phalanges, and its functional anatomy is strongly tied to the evolution of bipedalism in hominins (5-9). Thus, hominin fore-foot fossils can offer key insights into when and how bipedalism evolved in the human lineage. During bipedal walking, modern humans dorsiflex (i.e., hyperextend) their forefoot joints, specifically at the metatarsophalangeal joints (MTPJs), as part of the push-off phase of gait, which tightens plantar soft tissues to convert the foot into a relatively stiff, propulsive lever (10) (also see ref. 11). Features of MT head morphology such as "dorsal doming" are thought to facilitate this stiffening mechanism (6, 12); doming occurs when the distal articular surface expands and becomes particularly pronounced dorsally. Comparative analysis of humans and chimpanzees has shown that dorsal doming is correlated with in vivo ranges of motion at the MTPJs, with humans displaying greater doming and a greater range of MTPJ dorsiflexion during bipedalism (9). The form and function of the hominin forefoot have been studied extensively (5, 6, 13-16), especially in light of more recent discoveries of hominin pedal fossils (17-19). However, a quantitative analysis of the hominin forefoot in a broad phylogenetic context is lacking, despite the theorized importance of these bony elements to the biomechanical demands of bipedalism (10, 20). To better understand the adaptive evolution of bipedalism in early hominins we investigated MTPJ morphology in Plio-Pleistocene fossil hominins (including species of Ardipithecus, Australopithecus, Paranthropus, and Homo) and a comparative sample of fossil and extant anthro-poids (including modern humans, apes, and monkeys) using shape analyses and phylogenetic comparative methods to test hypotheses about the nature and timing of forefoot evolution in the human clade. Three-dimensional geometric morphometric techniques were used to quantify MT1-MT5 head shapes, and a multioptima Ornstein-Uhlenbeck (OU) model was used to estimate the placement and Significance A critical step in the evolutionary history leading to the origins of humankind was the adoption of habitual bipedal locomotion by our hominin ancestors. We have identified novel bony shape variables in the forefoot across extant anthropoids and extinct hominins that are linked functionally to the emergence of bipedal walking. Results indicate a consistent and generalizable pattern in hominin pedal evolution that spans from Ardipithecus to early Homo-the relatively late derivation of a modern hallux in comparison with the lateral rays. These data provide novel morphological and macroevolutionary evidence for how and when the hominin pedal skeleton evolved to accommodate the unique biomechanical demands of bipedalism.