The calcaneus of Australopithecus afarensis and its implications for the evolution of bipedality

Calcanei from African apes, modern humans, and Australopithecus afarensis are compared to investigate the anatomical and mechanical changes that occurred in this bone as a result of the transition to terrestrial bipedality. Features analyzed include the cross-sectional area and volume of the calcaneal tuber, the geometry and orientation of the articular surfaces, and the surface topography of the calcaneal corpus. Calcaneal morphology is unequivocal in its partitioning of quadrupedal pongids and bipedal hominids.     

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.     

Trabecular angle of the human talus is associated with the level of cartilage degeneration

The architecture of bone trabeculae is based on the direction of stresses applied to the bone. The human talar dome receives compressive forces from the tibia and, to a much lesser extent, the fibula when standing, walking, and running, and transmits the force downward to the calcaneus through the talar body and anterior to the navicular via the talar head. As a result, the body of the talus has predominately vertical trabeculae. However, here we hypothesize that cartilage degeneration at the articular surface is associated with trabecular angle within the associated bone, as a reflection of joint alignment and/or biomechanics (stability, congruence, angulation, etc). Through measurement of trabecular angle with Fast Fourier Transform Analysis, we show a positive correlation between the cartilage degeneration score of the articular surface of the talar dome and the angle of trabecular deviation from the perpendicular axis of the dome (right talus R=0.75, p<0.01; left talus R=0.79, p<0.01).     

Articular to diaphyseal proportions of human and great ape metatarsals

This study proposes a new way to use metatarsals to identify locomotor behavior of fossil hominins. Metatarsal head articular dimensions and diaphyseal strength in a sample of chimpanzees, gorillas, orangutans, and humans (n = 76) are used to explore the relationships of these parameters with different locomotor modes. Results show that ratios between metatarsal head articular proportions and diaphyseal strength of the hallucal and fifth metatarsal discriminate among extant great apes and humans based on their different locomotor modes. In particular, the hallucal and fifth metatarsal characteristics of humans are functionally related to the different ranges of motion and load patterns during stance phase in the forefoot of humans in bipedal locomotion. This method may be applicable to isolated fossil hominin metatarsals to provide new information relevant to debates regarding the evolution of human bipedal locomotion. The second to fourth metatarsals are not useful in distinguishing among hominoids. Further studies should concentrate on measuring other important qualitative and quantitative differences in the shape of the metatarsal head of hominoids that are not reflected in simple geometric reconstructions of the articulation, and gathering more forefoot kinematic data on great apes to better understand differences in range of motion and loading patterns of the metatarsals. Am J Phys Anthropol 143:198–207, 2010. © 2010 Wiley‐Liss, Inc.     

Talocrural joint in African hominoids: implications for Australopithecus afarensis

Talocrural joints of the African apes, modern humans, and A.L.288-1 are compared in order to investigate ankle function in the Hadar hominids. Comparisons between the hominids and African pongids clearly illustrate the anatomical and mechanical changes that occurred in this joint as a consequence of the evolutionary transition to habitual bipedality. Features which are considered include the obliquity of the distal tibial articular surface, the shape of the talar trochlea, and the location and functional implications of the talocrural axis. In every functionally significant feature examined the A.L.288-1 talocrural joint is fully bipedal. Moreover, the Hadar ankle complex also shows the functional constraints which are necessarily imposed by the adaptation to habitual bipedalism.     

Assessing endocranial variations in great apes and humans using 3D data from virtual endocasts

Modern humans are characterized by their large, complex, and specialized brain. Human brain evolution can be addressed through direct evidence provided by fossil hominid endocasts (i.e. paleoneurology), or through indirect evidence of extant species comparative neurology. Here we use the second approach, providing an extant comparative framework for hominid paleoneurological studies. We explore endocranial size and shape differences among great apes and humans, as well as between sexes. We virtually extracted 72 endocasts, sampling all extant great ape species and modern humans, and digitized 37 landmarks on each for 3D generalized Procrustes analysis. All species can be differentiated by their endocranial shape. Among great apes, endocranial shapes vary from short (orangutans) to long (gorillas), perhaps in relation to different facial orientations. Endocranial shape differences among African apes are partly allometric. Major endocranial traits distinguishing humans from great apes are endocranial globularity, reflecting neurological reorganization, and features linked to structural responses to posture and bipedal locomotion. Human endocasts are also characterized by posterior location of foramina rotunda relative to optic canals, which could be correlated to lesser subnasal prognathism compared to living great apes. Species with larger brains (gorillas and humans) display greater sexual dimorphism in endocranial size, while sexual dimorphism in endocranial shape is restricted to gorillas, differences between males and females being at least partly due to allometry. Our study of endocranial variations in extant great apes and humans provides a new comparative dataset for studies of fossil hominid endocasts.     

A 3D quantitative comparison of trapezium and trapezoid relative articular and nonarticular surface areas in modern humans and great apes

The structure and functions of the modern human hand are critical components of what distinguishes Homo sapiens from the great apes (Gorilla, Pan, and Pongo). In this study, attention is focused on the trapezium and trapezoid, the two most lateral bones of the distal carpal row, in the four extant hominid genera, representing the first time they have been quantified and analyzed together as a morphological-functional complex. Our objective is to quantify the relative articular and nonarticular surface areas of these two bones and to test whether modern humans exhibit significant shape differences from the great apes, as predicted by previous qualitative analyses and the functional demands of differing manipulative and locomotor strategies. Modern humans were predicted to show larger relative first metacarpal and scaphoid surfaces on the trapezium because of the regular recruitment of the thumb during manipulative behaviors; alternatively, great apes were predicted to show larger relative second metacarpal and scaphoid surfaces on the trapezoid because of the functional demands on the hands during locomotor behaviors. Modern humans were also expected to exhibit larger relative mutual joint surfaces between the trapezoid and adjacent carpals than do the great apes because of assumed transverse loads generated by the functional demands of the modern human power grip. Using 3D bone models acquired through laser digitizing, the relative articular and nonarticular areas on each bone are quantified and compared. Multivariate analyses of these data clearly distinguish modern humans from the great apes. In total, the observed differences between modern humans and the great apes support morphological predictions based on the fact that this region of the human wrist is no longer involved in weight-bearing during locomotor behavior and is instead recruited solely for manipulative behaviors. The results provide the beginnings of a 3D comparative standard against which further extant and fossil primate wrist bones can be compared within the contexts of manipulative and locomotor behaviors.     

Functional morphology and anatomy of cervical vertebrae in Nacholapithecus kerioi, a middle Miocene hominoid from Kenya

This paper describes the morphology of cervical vertebrae in Nacholapithecus kerioi, a middle Miocene primate species excavated from Nachola, Kenya in 1999-2002. The cervical vertebrae in Nacholapithecus are larger than those of Papio cynocephalus. They are more robust relative to more caudal vertebral bones. Since Nacholapithecus had large forelimbs, it is assumed that strong cervical vertebrae would have been required to resist muscle reaction forces during locomotion. On the other hand, the vertebral foramen of the lower cervical vertebrae in Nacholapithecus is almost the same size as or smaller than that of P. cynocephalus. Atlas specimens of Nacholapithecus resemble those of extant great apes with regard to the superior articular facet, and they have an anterior tubercle trait intermediate between that of extant apes and other primate species. Nacholapithecus has a relatively short and thick dens on the axis, similar to those of extant great apes and the axis body shape is intermediate between that of extant apes and other primates. Moreover, an intermediate trait between extant great apes and other primate species has been indicated with regard to the angle between the prezygapophyseal articular facets of the axis in Nacholapithecus. Although the atlas of Nacholapithecus is inferred as having a primitive morphology (i.e., possessing a lateral bridge), the shape of the atlas and axis leads to speculation that locomotion or posture in Nacholapithecus involved more orthograde behavior similar to that of extant apes, and, in so far as cervical vertebral morphology is concerned, it is thought that Nacholapithecus was incipiently specialized toward the characteristics of extant hominoids.     

Metatarsophalangeal joint function and positional behavior in Australopithecus afarensis

Recent discussions of the pedal morphology of Australopithecus afarensis have led to conflicting interpretations of australopithecine locomotor behavior. We report the results of a study using computer aided design (CAD) software that provides a quantitative assessment of the functional morphology of australopithecine metatarsophalangeal joints. The sample includes A. afarensis, Homo sapiens, Pan troglodytes, Gorilla gorilla, and Pongo pygmaeus. Angular measurements of the articular surfaces relative to the long axes of the metatarsals and phalanges were taken to determine whether the articular surfaces are plantarly or dorsally oriented. Humans have the most dorsally oriented articular surfaces of the proximal pedal phalanges. This trait appears to be functionally associated with dorsiflexion during bipedal stride. Pongo has the most plantarly oriented articular surfaces of the proximal pedal phalanges, probably reflecting an emphasis on plantarflexion in arboreal positional behaviors, while the African hominoids are intermediate between Pongo and Homo for this characteristic. A. afarensis falls midway between the African apes and humans. Results from an analysis of metatarsal heads are inconclusive with regard to the functional morphology of A. afarensis. Overall, the results are consistent with other evidence indicating that A. afarensis was a capable climber. © 1994 Wiley-Liss, Inc.     

Brief Communication: Shape analysis of the MT 1 proximal articular surface in fossil hominins and shod and unshod Homo

As a follow-up study to Proctor et al. (Am J Phys Anthropol 135 (2008) 216-224), this study quantifies the first metatarsal proximal articular surface using three-dimensional morphometrics to test for differences in articular surface shape between habitually shod and habitually unshod humans. In addition, differences in shape between Homo, Pan, Gorilla, and Hylobates are compared to the fossil hominin specimens A. L. 333-54, Stw 562, Stw 573 ("Little Foot"), OH 8, SKX 5017, and SK 1813. No difference in surface shape was found between habitually shod and habitually unshod humans. There is a clear quantitative division in articular surface shape between humans and apes that is more pronounced than a previous study by Proctor et al. (Am J Phys Anthropol 135 (2008) 216-224), due to additional landmarks present in this study. The specimen OH 8 is indistinguishable from modern Homo. The fossils A. L. 333-54, Stw 562, and Stw 573 are intermediate in shape between humans and apes. The specimens SKX 5017 and SK 1813 have a more apelike articular surface. When combined with other characteristics, this trait suggests that Paranthropus used a degree of abduction during locomotion that was much less than that in extant apes, but greater than that in Australopithecus, allowing for some small degree of grasping ability.     

Talar articular facets (facies articulares talares) in human calcanei

The variations of the talar articular facets in 176 calcanei were studied and classified. Three types were considered: type A = calcanei with two articular facets for the talar head, with four subtypes; type B = calcanei with one articular facet for the talar head, and two subtypes, and type C = unique articular facies in the superior surface of the calcaneus for the talus. We found 53% (94 cases) type B calcanei and 46% (82 cases) type A calcanei. No calcanei of type C were seen.     

External forces and torques generated by the brachiating white-handed gibbon (Hylobates lar)

We compared the kinetics of brachiation to bipedal walking and running. Gibbons use pectoral limbs in continuous contact with their overhead support at slow speeds, but exhibit aerial phases (or ricochetal brachiation) at faster speeds. This basic interaction between limb and support suggests some analogy to walking and running. We quantified the forces in three axes and torque about the vertical axis generated by a brachiating White-handed gibbon (Hylobates lar) and compared them with bipedal locomotion. Handholds oriented perpendicular to the direction of travel (as in ladder rungs) were spaced 0.80, 1.20, 1.60, 1.72, 1.95, and 2.25 m apart. The gibbon proportionally matched forward velocity to stride length. Handhold reaction forces resembled ground reaction forces of running humans except that the order of horizontal braking and propulsion were reversed. Peak vertical forces in brachiation increased with speed as in bipedal locomotion. In contrast to bipedalism, however, peak horizontal forces changed little with speed. Gait transition occurred within the same relative velocity range as the walk-run transition in bipeds (Froude number = 0.3-0.6). We oriented handholds parallel to the direction of travel (as in a continuous pole) at 0.80 and 1.60 m spacings. In ricochetal brachiation, the gibbon generated greater torque with handholds oriented perpendicular as opposed to parallel to the direction of travel. Handhold orientation did not affect peak forces. The similarities and differences between brachiation and bipedalism offer insight into the ubiquity of mechanical principles guiding all limbed locomotion and the distinctiveness of brachiation as a unique mode of locomotion.     

The distal femoral anatomy of Australopithecus

The anatomy of the distal femoral fragments from Sterkfontein is reviewed, including its orthopaedic and biomechanical implications with respect to locomotion pattern. Comparisons are made with other hominids and a number of quadrupedal primates. Items which are considered are the obliquity and robustness of the shaft, the anterior intercondylar groove, the intercondylar notch, and the contour of the medial and lateral articular surfaces. The distinctive hominid status of these specimens is shown by their extensive adaptation to bipedal locomotion. No feature is found which is not fully commensurate with completely bipedal locomotion; rather, their distinctive hominid character points to a need for a reanalysis of the gait pattern in these early Pleistocene hominids.     

A geometric model of the human ankle joint.

A two-dimensional four-bar linkage model of the ankle joint is formulated to describe dorsi/plantarflexion in unloaded conditions as observed in passive tests on ankle complex specimens. The experiments demonstrated that the human ankle joint complex behaves as a single-degree-of-freedom system during passive motion, with a moving axis of rotation. The bulk of the movement occurred at the level of the ankle. Fibres within the calcaneofibular and tibiocalcaneal ligaments remained approximately isometric. The experiments showed that passive kinematics of the ankle complex is governed only by the articular surfaces and the ligaments. It was deduced that the ankle is a single-degree-of-freedom mechanism where mobility is allowed by the sliding of the articular surfaces upon each other and the isometric rotation of two ligaments about their origins and insertions, without tissue deformation. The linkage model is formed by the tibia/fibula and talus/calcaneus bone segments and by the calcaneofibular and tibiocalcaneal ligament segments. The model predicts the path of calcaneus motion, ligament orientations, instantaneous axis of rotation, and conjugate talus surface profile as observed in the experiments. Many features of ankle kinematics such as rolling and multiaxial rotation are elucidated. The geometrical model is a necessary preliminary step to the study of ankle joint stability in response to applied loads and can be used to predict the effects of changes to the original geometry of the intact joint. Careful reconstruction of the original geometry of the ligaments is necessary after injury or during total ankle replacement.     

Degenerative joint disease in African great apes: an evolutionary perspective

Degenerative joint disease is investigated in the spine and major peripheral joints (shoulder, elbow, hip and knee) in samples of chimpanzees (Pan troglodytes schweinfurthii; P. troglodytes troglodytes), lowland gorillas (Gorilla gorilla gorilla), and bonobos (P. paniscus). The P. troglodytes schweinfurthii sample comes from Gombe National Park, Tanzania, while the other samples are derived from museum materials originally collected in west/central Africa. Total data for African ape samples include 5807 surfaces for ascertainment of vertebral osteophytosis, 12,479 surfaces for determination of spinal osteoarthritis, and 1211 joints for evaluation of peripheral joint osteoarthritis. All apes display significantly less spinal disease than in a comparable human sample, and these differences are most likely a consequence of human biomechanical adaptations for bipedal locomotion. Apes are also generally less involved in the major peripheral joints than are humans, but human groups are themselves highly variable in prevalence of peripheral osteoarthritis. These data agree with other findings of low prevalence of degenerative joint prevalence in free-ranging apes, but contrast markedly with evidence derived from colony-reared Old World monkeys.     

Proximal metatarsal articular surface shape and the evolution of a rigid lateral foot in hominins

This study quantifies the proximal articular surface shape of metatarsal (MT) 4 and MT 5 using three-dimensional morphometrics. Humans and apes are compared to test whether they have significantly different shapes that are skeletal correlates to comparative lateral foot function. In addition, shod and unshod humans are compared to test for significant differences in surface shape. The MT 4 fossils OH 8, Stw 628, and AL 333-160, and the MT 5 fossils AL 333-13, AL 333-78, OH 8, and Stw 114/115 are compared with humans and apes to assess whether they bear greater similarities to humans, which would imply a relatively stable lateral foot, or to apes, which would imply a flexible foot with a midfoot break. Apes have a convex curved MT 4 surface, and humans have a flat surface. The MT 4 fossils show greater similarity to unshod humans, suggesting a stable lateral foot. Unshod humans have a relatively flatter MT 4 surface compared with shod humans. There is much overlap in MT 5 shape between humans and apes, with more similarity between humans and Gorilla. The fossil MT 5 surfaces are generally flat, most similar to humans and Gorilla. Because of the high degree of shape overlap between humans and apes, one must use caution in interpreting lateral foot function from the proximal MT 5 surface alone.     

Hindlimb adaptations in Ourayia and Chipetaia, relatively large-bodied omomyine primates from the Middle Eocene of Utah

North American omomyids represent a tremendous Eocene radiation of primates exhibiting a wide range of body sizes and dietary patterns. Despite this adaptive diversity, relatively little is known of the postcranial specializations of the group. Here we describe hindlimb and foot bones of Ourayia uintensis and Chipetaia lamporea that were recovered from the Uinta B member (early Uintan Land Mammal Age), Uinta Formation, Utah. These specimens provide insights into the evolution of postcranial adaptations across different body sizes and dietary guilds within the Eocene primate radiation. Body mass estimates based on talar measurements indicate that Ourayia uintensis and Chipetaia lamporea weighed about 1,500-2,000 g and 500-700 g, respectively. Skeletal elements recovered for Ourayia include the talus, navicular, entocuneiform, first metatarsal, and proximal tibia; bones of Chipetaia include the talus, navicular, entocuneiform, and proximal femur. Both genera had opposable grasping big toes, as indicated by the saddle-shaped joint between the entocuneiform and first metatarsal. Both taxa were arboreal leapers, as indicated by a consistent assemblage of characters in all represented bones, most notably the somewhat elongated naviculars, the high and distinct trochlear crests of the talus, the posteriorly oriented tibial plateau (Ourayia), and the cylindrical head of the femur (Chipetaia). The closest resemblances to Ourayia and Chipetaia are found among the Bridger omomyines, Omomys and Hemiacodon. The results of our comparisons suggest that the later, larger, more herbivorous omomyines from Utah retained a skeletal structure characteristic of earlier, smaller North American omomyids.     

Knuckle-walking anteater: a convergence test of adaptation for purported knuckle-walking features of African Hominidae

Appeals to synapomorphic features of the wrist and hand in African apes, early hominins, and modern humans as evidence of knuckle-walking ancestry for the hominin lineage rely on accurate interpretations of those features as adaptations to knuckle-walking locomotion. Because Gorilla, Pan, and Homo share a relatively close common ancestor, the interpretation of such features is confounded somewhat by phylogeny. The study presented here examines the evolution of a similar locomotor regime in New World anteaters (order Xenarthra, family Myrmecophagidae) and uses the terrestrial giant anteater (Myrmecophaga tridactyla) as a convergence test of adaptation for purported knuckle-walking features of the Hominidae. During the stance phase of locomotion, Myrmecophaga transmits loads through flexed digits and a vertical manus, with hyperextension occurring at the metacarpophalangeal joints of the weight-bearing rays. This differs from the locomotion of smaller, arboreal anteaters of outgroup genera Tamandua and Cyclopes that employ extended wrist postures during above-branch quadrupedality. A number of features shared by Myrmecophaga and Pan and Gorilla facilitate load transmission or limit extension, thereby stabilizing the wrist and hand during knuckle-walking, and distinguish these taxa from their respective outgroups. These traits are a distally extended dorsal ridge of the distal radius, proximal expansion of the nonarticular surface of the dorsal capitate, a pronounced articular ridge on the dorsal aspects of the load-bearing metacarpal heads, and metacarpal heads that are wider dorsally than volarly. Only the proximal expansion of the nonarticular area of the dorsal capitate distinguishes knuckle-walkers from digitigrade cercopithecids, but features shared with digitigrade primates might be adaptive to the use of a vertical manus of some sort in the stance phase of terrestrial locomotion. The appearance of capitate nonarticular expansion and the dorsal ridge of the distal radius in the hominin lineage might be indicative of a knuckle-walking ancestry for bipedal hominins if interpreted within the biomechanical and phylogenetic context of hominid locomotor evolution.     

Variations in blood supply allocations for quadrupedal and for bipedal posture and locomotion

Hemodynamics and orthodynamics were investigated in quadrupeds (dogs) and in bipeds (humans). The subjects were investigated at rest in supine or lateral posture, in quadrupedal and then in bipedal posture, and during locomotion. Quadrupedalism in humans was with subjects on their hands and knees. Bipedalism in dogs was on hindlimbs with the forelimbs held by a technician. Blood flow in the main arteries of the body (aorta, external and internal carotid, subclavian, and femoral) was measured by sonography. Positional variations between the main bones of the body were determined from X-rays. This study investigated the reallocation of blood supply to different regions of the body when it switches from quadrupedal to bipedal posture and locomotion. Compared with resting posture, the principal findings are 1) cardiac output shows a minimal increase for humans in bipedal stance and a noticeable increase for dogs as well as humans in quadrupedal stance; 2) quadrupedal stance in humans and dogs and bipedal stance in dogs require increased blood supply to the muscles of the neck, back, and limbs, while human bipedal stance requires none of these; 3) cerebral blood flow (internal carotid) in humans did not change as a result of bipedal posture or locomotion, but showed a noticeable drop in quadrupedal posture and an even further drop in quadrupedal locomotion. The conclusion is that erect posture and encephalization produced a noticeable readjustment and reallocation of blood flow among the different regions of the body: This consisted in shifting a large volume of blood supply from the musculature to the human brain.