Hip extensor mechanics and the evolution of walking and climbing capabilities in humans, apes, and fossil hominins

Abstract

The evolutionary emergence of humans' remarkably economical walking gait remains a focus of research and debate, but experimentally validated approaches linking locomotor capability to postcranial anatomy are limited. In this study, we integrated 3D morphometrics of hominoid pelvic shape with experimental measurements of hip kinematics and kinetics during walking and climbing, hamstring activity, and passive range of hip extension in humans, apes, and other primates to assess arboreal-terrestrial trade-offs in ischium morphology among living taxa. We show that hamstring-powered hip extension during habitual walking and climbing in living apes and humans is strongly predicted, and likely constrained, by the relative length and orientation of the ischium. Ape pelves permit greater extensor moments at the hip, enhancing climbing capability, but limit their range of hip extension, resulting in a crouched gait. Human pelves reduce hip extensor moments but permit a greater degree of hip extension, which greatly improves walking economy (i.e., distance traveled/energy consumed). Applying these results to fossil pelves suggests that early hominins differed from both humans and extant apes in having an economical walking gait without sacrificing climbing capability. Ardipithecus was capable of nearly human-like hip extension during bipedal walking, but retained the capacity for powerful, ape-like hip extension during vertical climbing. Hip extension capability was essentially human-like in Australopithecus afarensis and Australopithecus africanus, suggesting an economical walking gait but reduced mechanical advantage for powered hip extension during climbing.

Keywords: evolution; hominin; ischium; locomotion; pelvis.

Fig. 1.

Ischial morphology and hip mechanics. (A) The hamstrings muscle group exerts a force F_m, which results in a hip extension moment F_m × r, where r is the orthogonal distance from the F_m vector to the center of rotation for the hip. The resulting force at the knee, F_k, is equal to F_m × (r/B), where B is the orthogonal distance from the F_k vector to the center of rotation for the hip. The hamstrings group inserts on the proximal tibia and fibula, very near the knee, making femur length a useful proxy measure for B. The ratio r/B thus gives the DMA for the hamstrings group (i.e., the force F_k exerted at the knee for a given F_m). DMA is a function of hip flexion angle, Φ. Greater DMA allows the hip extensors to generate greater F_k, but also requires more shortening of the hamstrings group (i.e., muscle strain) per degree of hip extension. This graphic presents a chimpanzee, with its highly flexed hip. (B) Humans’ shorter and reoriented ischium results in lower peak DMA but a greater functional range of hip extension, enabling the hamstrings to hyperextend the hip beyond 200°, as shown here. (C) Ischial length (which defines maximum r) relative to femoral length (which defines B) in fossil and extant taxa. Solid line is the nonhuman primate linear regression (R² = 0.89; P < 0.001), with dashed lines showing 95% prediction interval. The linear relationship test between femur and ischial length in humans yields a P value of 0.12. Arrows for fossil taxa represent ±10% range. Red dots, humans; black dots, nonhuman apes; blue dots, catarrhines; green dots, platyrrhines; green arrow, E. nyanzae; brown arrow, Ar. ramidus; orange, Au. afarensis; yellow, Au. africanus. (See SI Appendix, Tables S1 and S2.)

Fig. 2.

Hip extensor DMA and locomotor mechanics. Red, Homo; gray, Pan; blue; Gorilla; purple, Pongo; green, hylobatidae. (A) Skeletally derived DMA in extant hominoids. Shaded regions represent 95% prediction interval for DMA in each taxon. (B) Bars represent mean range of flexion and extension with SDs while climbing (19) (dark colors), and while walking quadrupedally or bipedally on level ground (light colors). For Homo, only bipedal walking is shown. For level walking in Pan, both P. troglodytes (Upper) and P. paniscus (Lower) are shown. For hylobatidae, only vertical climbing is shown. (C) Hip moments (dimensionless, scaled to body mass and tibia length) in humans, chimpanzees, and bonobos. Red line, Homo level bipedal walking; gray line, P. troglodytes level quadrupedal walking; dashed line, P. paniscus level quadrupedal walking; dot-dashed line, P. paniscus 45° incline climbing; dotted line, P. paniscus vertical climbing. (D) Hamstrings electromyography activity in humans and chimpanzees and gibbons (–27). (I) Human level bipedal walking; (II) P. troglodytes level quadrupedal walking; (III) P. paniscus 45° incline climbing; (IV) P. paniscus vertical climbing; (V) Hylobates vertical climbing. (E) Passive in vivo hip extension ranges for nonhuman primates (pooled sexes) (29) and for humans (30). (Data are in SI Appendix, Table S3.)

Fig. 3.

DMA and pelvic orientation in fossil taxa. (A) Homo, pink; Pan, gray; Ar. ramidus, brown; Au. afarensis, orange; Au. africanus, yellow. Skeletally derived envelopes for hamstrings DMA. Shaded regions for Pan and Homo represent 95% prediction intervals. Shaded regions for fossils represent the full range of mechanically feasible pelvic pitch angles plus a range of reconstructed sacral breadths and femur lengths (see Methods). (B) The range of pelvic tilt angles for bipedal orientation is based on the requirement that some portion of the medial gluteals (red regions on the ilia) must be aligned vertically to oppose gravity and to stabilize the trunk during single-leg stance. In the most dorsal-superior orientation (Left), the anterior border of the medial gluteals is aligned vertically over the acetabulum; in the most ventral-inferior orientation (Right), the posterior border of the medial gluteals is aligned vertically over the acetabulum. (See SI Appendix, Table S5.)