Jeremy M. DeSilva

Homo naledi, a new species of the genus Homo from the Dinaledi Chamber, South Africa

Homo naledi is a previously-unknown species of extinct hominin discovered within the Dinaledi Chamber of the Rising Star cave system, Cradle of Humankind, South Africa. This species is characterized by body mass and stature similar to small-bodied human populations but a small endocranial volume similar to australopiths. Cranial morphology of H. naledi is unique, but most similar to early Homo species including Homo erectus, Homo habilis or Homo rudolfensis. While primitive, the dentition is generally small and simple in occlusal morphology. H. naledi has humanlike manipulatory adaptations of the hand and wrist. It also exhibits a humanlike foot and lower limb. These humanlike aspects are contrasted in the postcrania with a more primitive or australopith-like trunk, shoulder, pelvis and proximal femur. Representing at least 15 individuals with most skeletal elements repeated multiple times, this is the largest assemblage of a single species of hominins yet discovered in Africa. DOI: http://dx.doi.org/10.7554/eLife.09560.001

The Foot and Ankle of Australopithecus sediba

Australopithecus sediba had a human-like ankle and arch but an ape-like heel and tibia, implying that while bipedal, this species was also adept at climbing trees. A well-preserved and articulated partial foot and ankle of Australopithecus sediba, including an associated complete adult distal tibia, talus, and calcaneus, have been discovered at the Malapa site, South Africa, and reported in direct association with the female paratype Malapa Hominin 2. These fossils reveal a mosaic of primitive and derived features that are distinct from those seen in other hominins. The ankle (talocrural) joint is mostly humanlike in form and inferred function, and there is some evidence for a humanlike arch and Achilles tendon. However, Au. sediba is apelike in possessing a more gracile calcaneal body and a more robust medial malleolus than expected. These observations suggest, if present models of foot function are correct, that Au. sediba may have practiced a unique form of bipedalism and some degree of arboreality. Given the combination of features in the Au. sediba foot, as well as comparisons between Au. sediba and older hominins, homoplasy is implied in the acquisition of bipedal adaptations in the hominin foot.

A shift toward birthing relatively large infants early in human evolution

It has long been argued that modern human mothers give birth to proportionately larger babies than apes do. Data presented here from human and chimpanzee infant:mother dyads confirm this assertion: humans give birth to infants approximately 6% of their body mass, compared with approximately 3% for chimpanzees, even though the female body weights of the two species are moderately convergent. Carrying a relatively large infant both pre- and postnatally has important ramifications for birthing strategies, social systems, energetics, and locomotion. However, it is not clear when the shift to birthing large infants occurred over the course of human evolution. Here, known and often conserved relationships between adult brain mass, neonatal brain mass, and neonatal body mass in anthropoids are used to estimate birthweights of extinct hominid taxa. These estimates are resampled with direct measurements of fossil postcrania from female hominids, and also compared with estimates of female body mass to assess when human-like infant:mother mass ratios (IMMRs) evolved. The results of this study suggest that 4.4-Myr-old Ardipithecus possessed IMMRs similar to those found in African apes, indicating that a low IMMR is the primitive condition in hominids. Australopithecus females, in contrast, had significantly heavier infants compared with dimensions of the femoral head (n = 7) and ankle (n = 7) than what is found in chimpanzees, and are estimated to have birthed neonates more than 5% of their body mass. Carrying such proportionately large infants may have limited arboreality in Australopithecus females and may have selected for alloparenting behavior earlier in human evolution than previously thought.

Functional morphology of the ankle and the likelihood of climbing in early hominins

Whether early hominins were adept tree climbers is unclear. Although some researchers have argued that bipedality maladapts the hominin skeleton for climbing, others have argued that early hominin fossils display an amalgamation of features consistent with both locomotor strategies. Although chimpanzees have featured prominently in these arguments, there are no published data on the kinematics of climbing in wild chimpanzees. Without these biomechanical data describing how chimpanzees actually climb trees, identifying correlates of climbing in modern ape skeletons is difficult, thereby limiting accurate interpretations of the hominin fossil record. Here, the first kinematic data on vertical climbing in wild chimpanzees are presented. These data are used to identify skeletal correlates of climbing in the ankle joint of the African apes to more accurately interpret hominin distal tibiae and tali. This study finds that chimpanzees engage in an extraordinary range of foot dorsiflexion and inversion during vertical climbing bouts. Two skeletal correlates of modern ape-like vertical climbing are identified in the ankle joint and related to positions of dorsiflexion and foot inversion. A study of the 14 distal tibiae and 15 tali identified and published as hominins from 4.12 to 1.53 million years ago finds that the ankles of early hominins were poorly adapted for modern ape-like vertical climbing bouts. This study concludes that if hominins included tree climbing as part of their locomotor repertoire, then they were performing this activity in a manner decidedly unlike modern chimpanzees.

The Lower Limb and Mechanics of Walking in Australopithecus sediba

The discovery of a relatively complete Australopithecus sediba adult female skeleton permits a detailed locomotor analysis in which joint systems can be integrated to form a comprehensive picture of gait kinematics in this late australopith. Here we describe the lower limb anatomy of Au. sediba and hypothesize that this species walked with a fully extended leg and with an inverted foot during the swing phase of bipedal walking. Initial contact of the lateral foot with the ground resulted in a large pronatory torque around the joints of the foot that caused extreme medial weight transfer (hyperpronation) into the toe-off phase of the gait cycle (late pronation). These bipedal mechanics are different from those often reconstructed for other australopiths and suggest that there may have been several forms of bipedalism during the Plio-Pleistocene.

Revisiting the “midtarsal break”†

The midtarsal break was first described in this journal nearly 75 years ago to explain the ability of non-human primates to lift their heel independently of the rest of the foot. Since the initial description of the midtarsal break, the calcaneocuboid joint has been assumed to be the anatomical source of this motion. Recently, however, it has been suggested that the midtarsal break may occur at the cuboid-metatarsal joint, rather than at the calcaneocuboid joint. Data compiled from X-rays, dissections, manual manipulation of living primate feet, video of captive catarrhines, and osteological specimens concur that the midtarsal break is a complex motion caused by dorsiflexion at both joints with the cuboid-metatarsal joint contributing roughly 2/3 of total midfoot dorsiflexion, and the calcaneocuboid joint only about 1/3 of total midfoot dorsiflexion. The convexity of the proximal articular surface of the fourth and fifth metatarsals and corresponding concave cuboid facets provide skeletal correlates for the presence of midfoot dorsiflexion at the cuboid-metatarsal joint. Study of hominin metatarsals from Australopithecus afarensis, A. africanus, Homo erectus, and the metatarsals and a cuboid from the OH 8 foot show little capacity for dorsiflexion at the cuboid-metatarsal joint. These results suggest that hominins may have already evolved a stable midfoot region well adapted for the push-off phase of bipedalism by at least 3.2 million years ago. These data illuminate the evolution of the longitudinal arch and show further evidence of constraints on the arboreal capacity in early hominins.

A comparative study of the trabecular bony architecture of the talus in humans, non-human primates, and Australopithecus

This study tested the hypothesis that talar trabecular microarchitecture reflects the loading patterns in the primate ankle joint, to determine whether talar trabecular morphology might be useful for inferring locomotor behavior in fossil hominins. Trabecular microarchitecture was quantified in the anteromedial, anterolateral, posteromedial, and posterolateral quadrants of the talar body in humans and non-human primates using micro-computed tomography. Trabecular bone parameters, including bone volume fraction, trabecular number and thickness, and degree of anisotropy differed between primates, but not in a manner entirely consistent with hypotheses derived from locomotor kinematics. Humans have highly organized trabecular struts across the entirety of the talus, consistent with the compressive loads incurred during bipedal walking. Chimpanzees possess a high bone volume fraction, consisting of plate-like trabecular struts. Orangutan tali are filled with a high number of thin, connected trabeculae, particularly in the anterior portion of the talus. Gorillas and baboons have strikingly similar internal architecture of the talus. Intraspecific analyses revealed no regional differences in trabecular architecture unique to bipedal humans. Of the 22 statistically significant regional differences in the human talus, all can also be found in other primates. Trabecular thickness, number, spacing, and connectivity density had the same regional relationship in the talus of humans, chimpanzees, gorillas, and baboons, suggesting a deeply conserved architecture in the primate talus. Australopithecus tali are human-like in most respects, differing most notably in having more oriented struts in the posteromedial quadrant of the body compared with the posterolateral quadrant. Though this result could mean that australopiths loaded their ankles in a unique manner during bipedal gait, the regional variation in degree of anisotropy was similar in humans, chimpanzees, and gorillas. These results collectively suggest that the microarchitecture of the talus does not simply reflect the loading environment, limiting its utility in reconstructing locomotion in fossil primates.

Brief communication: A midtarsal (midfoot) break in the human foot

The absence of a midtarsal break has long been regarded as a derived feature of the human foot. Humans possess a rigid midfoot that acts as an efficient lever during the propulsive phase of bipedal gait. Non-human primates, in contrast, have a more mobile midfoot that is adaptive for tree climbing. Here, we report plantar pressure and video evidence that a small percentage of modern humans (n = 32/398) possess both elevated lateral midfoot pressures and even exhibit midfoot dorsiflexion characteristic of a midtarsal break. Those humans with a midtarsal break had on average a significantly flatter foot than those without. Midtarsal breakers also had significantly more medial weight transfer (pronation) during the stance phase of gait than those without this midfoot mobility. These data are in accordance with Elftman (Clin Orthop 16 (1960) 41-45) who suggested that pronation aligns the axes of the transverse tarsal joint, permitting elevated midfoot mobility.

Lucy's Flat Feet: The Relationship between the Ankle and Rearfoot Arching in Early Hominins

Background In the Plio-Pleistocene, the hominin foot evolved from a grasping appendage to a stiff, propulsive lever. Central to this transition was the development of the longitudinal arch, a structure that helps store elastic energy and stiffen the foot during bipedal locomotion. Direct evidence for arch evolution, however, has been somewhat elusive given the failure of soft-tissue to fossilize. Paleoanthropologists have relied on footprints and bony correlates of arch development, though little consensus has emerged as to when the arch evolved. Methodology/Principal Findings Here, we present evidence from radiographs of modern humans (n = 261) that the set of the distal tibia in the sagittal plane, henceforth referred to as the tibial arch angle, is related to rearfoot arching. Non-human primates have a posteriorly directed tibial arch angle, while most humans have an anteriorly directed tibial arch angle. Those humans with a posteriorly directed tibial arch angle (8%) have significantly lower talocalcaneal and talar declination angles, both measures of an asymptomatic flatfoot. Application of these results to the hominin fossil record reveals that a well developed rearfoot arch had evolved in Australopithecus afarensis. However, as in humans today, Australopithecus populations exhibited individual variation in foot morphology and arch development, and “Lucy” (A.L. 288-1), a 3.18 Myr-old female Australopithecus, likely possessed asymptomatic flat feet. Additional distal tibiae from the Plio-Pleistocene show variation in tibial arch angles, including two early Homo tibiae that also have slightly posteriorly directed tibial arch angles. Conclusions/Significance This study finds that the rearfoot arch was present in the genus Australopithecus. However, the female Australopithecus afarensis “Lucy” has an ankle morphology consistent with non-pathological flat-footedness. This study suggests that, as in humans today, there was variation in arch development in Plio-Pleistocene hominins.

Earliest complete hominin fifth metatarsal : implications for the evolution of the lateral column of the foot

StW 114/115, from Sterkfontein, South Africa, is the earliest complete hominin fifth metatarsal. Comparisons of StW 114/115 to modern humans, extant apes, and partial hominin metatarsals AL 333-13, AL 333-78, SKX 33380, OH 8, and KNM-ER 803f reveal a similar morphology in all six fossils consistent with habitual bipedality. Although StW 114/115 possesses some primitive characters, the proximal articular morphology and internal torsion of the head are very human-like, suggesting a stable lateral column and the likely presence of lateral longitudinal and transverse tarsal arches. We conclude that, at least in the lateral component of the foot of the StW 114/115 individual, the biomechanical pattern is very similar to that of modern humans. This, however, may not have been the case in the medial column of the foot, as a mosaic pattern of hominin foot evolution and function has been suggested. The results of this study may support the hypothesis of an increased calcaneo-cuboid stability having been an early evolutionary event in the history of terrestrial bipedalism.