Evolution and function of the hominin forefoot

Abstract

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.

Keywords: Ardipithecus; bipedalism; functional morphology; hominin evolution; metatarsals.

Fig. 1.

PCA scatterplots of PC1 vs. PC2 for MT1–MT4 morphospaces. MT1, most hominins are more ape-like in morphology (except H. naledi); MT2, most hominins are modern human-like; MT3, most hominins are modern human-like except Au. afarensis, but this may be due to taphonomy (see main text) (note that the Ar. ramidus MT3 appears more modern human-like than does its corresponding MT1); MT4, the results are similar to MT3. C. browni, Catopithecus browni; E. vindobonensis, Epipliopithecus vindobonensis; PCA, principal component analysis.

Fig. 2.

Time-scaled phylogenetic tree showing estimated adaptive regimes from the multioptima OU model. Adaptive optima are estimated for the PC2 scores of the MT1 (A) and MT3 (B). Adaptive shifts are indicated with an arrow when the posterior probabilities of a shift at a given node was >0.25. Branches are colored according to different adaptive regimes. Note that two adaptive shifts occur in the MT1 PC2 shape data compared with only one shift in the MT2–MT5 shape data. This finding suggests that the hallux underwent significant shape changes during human evolution even after facultative bipeds (e.g., Ar. ramidus) had evolved (–26), more so than what was seen in the lateral MTs, which had evolved derived modern human-like shapes relatively early in the fossil record (also see ref. 53). (Scale bar in Ma.) PP, posterior probability.

Fig. 3.

Distal (Left) and lateral (Right) views of fossil hominin and modern human first MT (MT1) heads. Note that H. sapiens is characterized by dorsal overlap of the distal articular surface onto the MT shaft and by wide flattening of the dorsal articular surface (arrows). (Scale bar: 1 cm.) H. erectus, Homo erectus; P. troglodytes, Pan troglodytes.

Fig. 4.

Distal (Left) and lateral (Right) views of fossil hominin and modern human lateral MT (MT2–MT5) heads. Note that Homo sapiens is characterized by dorsal overlap of the distal articular surface onto the MT shaft and by wide flattening of the dorsal articular surface. Note epicondylar surface landmarks were removed for MT3 analyses to include Ar. ramidus (ARA-VP-6/505) into the analysis. (Scale bar: 1 cm.) P. troglodytes, Pan troglodytes.