Trabecular structure of the third metatarsal head distinguishes between a grasping and non-grasping foot

The human foot is unique compared to that of other extant apes in its adaptations for bipedal locomotion. At the metatarsophalangeal joint, bipedal locomotion in humans is associated with a high degree of dorsiflexion at toe-off and this more extreme joint position is reflected in the external morphology of the metatarsal head and base of the proximal pedal phalanx. These morphological features related to dorsiflexion of the toes have been used to determine human-like foot loading in fossil hominins, including dorsal doming of the metatarsal head and the presence of an associated sulcus, and dorsal canting of the proximal pedal phalangeal base [1]. However, the loading regime of the metatarsophalangeal joint in fossil hominins remains uncertain, due to the presence of more primitive traits, for example relatively long, highly curved proximal phalanges [2], morphologies that are also present among more recent hominins belonging to the genus Homo [3]. Phalanges with such a morphology indicate the potential importance of arboreal locomotion, using the foot to grasp branches for stability when navigating unstable arboreal supports. As the internal structure of bone adapts during an individual’s lifetime, it can provide additional information about loading of the metatarsophalangeal joints [4]. As such, trabecular structure of the third metatarsal head may provide signals of human-like toe off and of an ape-like grasping foot. To explore the relationship between locomotor behaviour and internal bone structure, we quantified trabecular bone of the third metatarsal head of Homo sapiens (n = 7), Pan troglodytes (n = 7) and Pongo pygmaeus (n = 4). Using medtool software (www.dr-pahr.at/medtool), 3D morphometric maps of the distribution of bone volume fraction (BV/TV) were generated, and BV/TV and degree of anisotropy (DA) were quantified. Results reveal that the trabecular bone structure of the third metatarsal head discriminates among bipedal humans, arboreal/terrestrial chimpanzees and arboreal orangutans. The distribution of BV/TV reflects loading of the human metatarsal head in dorsiflexion during toe-off and does not indicate loading of the plantar surface. In chimpanzees, in contrast to humans, a localisation of BV/TV across the entire surface of the metatarsal head suggests loading throughout the range of dorso-to-plantar flexion, likely due to a combination of terrestrial and arboreal locomotor modes. In orangutans, the region of highest BV/TV is located on the plantar surface, reflecting frequent use of the foot to grasp arboreal substrates. The human metatarsal head is characterised by a high DA reflecting the stereotypical loading regime of this joint during bipedal locomotion. As is characteristic of trabecular architecture across the skeleton of sedentary human populations, the human metatarsal head has a low BV/TV [5]. This human-typical signal may be due to lower overall activity levels. As the internal bone structure of the third metatarsal head reflects locomotor behaviour among these three extant taxa, it may further inform interpretations of foot use, both during toe-off and grasping, among early hominins.

References:[1] Latimer, B., Lovejoy, C.O., 1990. Metatarsophalangeal joints of Australopithecus afarensis. American Journal of Physical Anthropology 83, 13-23.[2] Stern, J., Susman, R., 1983. The

locomotor anatomy of Australopithecus afarensis. American Journal of Physical Anthropology 60, 279-317.[3] DeSilva, J., McNutt, E., Benoit, J., Zipfel, B., 2019. One small step: A review of Plio-Pleistocene

hominin foot evolution. American Journal of Physical Anthropology 168:S67, 63-140.[4] Komza, K., Skinner, M.M., 2019. First metatarsal trabecular bone structure in extant hominoids and Swartkrans

hominins. Journal of Human Evolution 131, 1-21.[5] Ryan, T.M., Shaw, C.N., 2015. Gracility of the modern Homo sapiens skeleton is the result of decreased biomechanical loading. Proceedings of the

National Academy of Sciences of the United States of America 112, 372-377.