Adaptations for bipedal walking: Musculoskeletal structure and three-dimensional joint mechanics of humans and bipedal chimpanzees (Pan troglodytes).

Humans are unique among apes and other primates in the musculoskeletal design of their lower back, pelvis, and lower limbs. Here, we describe the three-dimensional ground reaction forces and lower/hindlimb joint mechanics of human and bipedal chimpanzees walking over a full stride and test whether: 1) the estimated limb joint work and power during the stance phase, especially the single-support period, is lower in humans than bipedal chimpanzees, 2) the limb joint work and power required for limb swing is lower in humans than in bipedal chimpanzees, and 3) the estimated total mechanical power during walking, accounting for the storage of passive elastic strain energy in humans, is lower in humans than in bipedal chimpanzees. Humans and bipedal chimpanzees were compared at matched dimensionless and dimensional velocities. Our results indicate that humans walk with significantly less work and power output in the first double-support period and the single-support period of stance, but markedly exceed chimpanzees in the second double-support period (i.e., push-off). Humans generate less work and power in limb swing, although the species difference in limb swing power was not statistically significant. We estimated that total mechanical positive 'muscle fiber' work and power were 46.9% and 35.8% lower, respectively, in humans than in bipedal chimpanzees at matched dimensionless speeds. This is due in part to mechanisms for the storage and release of elastic energy at the ankle and hip in humans. Furthermore, these results indicate distinct 'heel strike' and 'lateral balance' mechanics in humans and bipedal chimpanzees and suggest a greater dissipation of mechanical energy through soft tissue deformations in humans. Together, our results document important differences between human and bipedal chimpanzee walking mechanics over a full stride, permitting a more comprehensive understanding of the mechanics and energetics of chimpanzee bipedalism and the evolution of hominin walking.

The loss of the 'pelvic step' in human evolution.

Human bipedalism entails relatively short strides compared with facultatively bipedal primates. Unique non-sagittal-plane motions associated with bipedalism may account for part of this discrepancy. Pelvic rotation anteriorly translates the hip, contributing to bipedal stride length (i.e. the 'pelvic step'). Facultative bipedalism in non-human primates entails much larger pelvic rotation than in humans, suggesting that a larger pelvic step may contribute to their relatively longer strides. We collected data on the pelvic step in bipedal chimpanzees and over a wide speed range of human walking. At matched dimensionless speeds, humans have 26.7% shorter dimensionless strides, and a pelvic step 5.4 times smaller than bipedal chimpanzees. Differences in pelvic rotation explain 31.8% of the difference in dimensionless stride length between the two species. We suggest that relative stride lengths and the pelvic step have been significantly reduced throughout the course of hominin evolution.

Great ape thorax and shoulder configuration-An adaptation for arboreality or knuckle-walking?

Great apes exhibit a suite of morphological traits of the shoulder and upper thorax that have traditionally been linked to orthograde arborealism. Recently it has been proposed that these traits are instead adaptations for knuckle-walking, and more broadly, that knuckle-walking itself is an adaptation for shock absorption during terrestriality. Here we test several tenets of these hypotheses using kinematic and kinetic data from chimpanzees and macaques, and electromyographic data of shoulder muscle activity in chimpanzees. We collected 3D kinematic data to quantify motion of the acromion and trunk during quadrupedalism and vertical climbing in chimpanzees as well as ground reaction forces to investigate the presence and magnitude of impact transient forces during terrestrial locomotion in chimpanzees and macaques. We also investigated patterns of recruitment of select forelimb musculature (triceps brachii and serratus anterior) using previously collected data in chimpanzees to determine whether these muscles may function to absorb impact transient forces. We found that the acromion is significantly more elevated in vertical climbing than during knuckle-walking, while dorsoventral ranges and magnitudes of motion were similar between gaits. Ground reaction forces indicate that only a minority of strides in either chimpanzees or macaques have transient forces and, when present, these transient forces as well as loading rates are small. Electromyographic results show that activity of the triceps brachii may facilitate energy absorption while serratus anterior likely functions to support the trunk, as in other primates. Our data suggest there is little to no evidence supporting recent hypotheses that the African ape upper thorax and shoulder configuration is an adaptation for knuckle-walking, or more broadly, that knuckle-walking exists as an adaptation to absorb impact shock during terrestriality. We do however find some evidence that shoulder configuration allows greater scapular elevation in chimpanzees during arboreal behaviors (e.g., vertical climbing).

Chimpanzee super strength and human skeletal muscle evolution.

Since at least the 1920s, it has been reported that common chimpanzees (Pan troglodytes) differ from humans in being capable of exceptional feats of "super strength," both in the wild and in captive environments. A mix of anecdotal and more controlled studies provides some support for this view; however, a critical review of available data suggests that chimpanzee mass-specific muscular performance is a more modest 1.5 times greater than humans on average. Hypotheses for the muscular basis of this performance differential have included greater isometric force-generating capabilities, faster maximum shortening velocities, and/or a difference in myosin heavy chain (MHC) isoform content in chimpanzee relative to human skeletal muscle. Here, we show that chimpanzee muscle is similar to human muscle in its single-fiber contractile properties, but exhibits a much higher fraction of MHC II isoforms. Unlike humans, chimpanzee muscle is composed of ∼67% fast-twitch fibers (MHC IIa+IId). Computer simulations of species-specific whole-muscle models indicate that maximum dynamic force and power output is 1.35 times higher in a chimpanzee muscle than a human muscle of similar size. Thus, the superior mass-specific muscular performance of chimpanzees does not stem from differences in isometric force-generating capabilities or maximum shortening velocities-as has long been suggested-but rather is due in part to differences in MHC isoform content and fiber length. We propose that the hominin lineage experienced a decline in maximum dynamic force and power output during the past 7-8 million years in response to selection for repetitive, low-cost contractile behavior.

Distinct functional roles of primate grasping hands and feet during arboreal quadrupedal locomotion.

It has long been thought that quadrupedal primates successfully occupy arboreal environments, in part, by relying on their grasping feet to control balance and propulsion, which frees their hands to test unstable branches and forage. If this interlimb decoupling of function is real, there should be discernible differences in forelimb versus hind limb musculoskeletal control, specifically in how manual and pedal digital flexor muscles are recruited to grasp during arboreal locomotion. New electromyography data from extrinsic flexor muscles in red ruffed lemurs (Varecia rubra) walking on a simulated arboreal substrate reveal that toe flexors are activated at relatively higher levels and for longer durations than finger flexors during stance phase. This demonstrates that the extremities of primates indeed have different functional roles during arboreal locomotion, with the feet emphasizing maintenance of secure grips. When this dichotomous muscle activity pattern between the forelimbs and hind limbs is coupled with other features of primate quadrupedal locomotion, including greater hind limb weight support and the use of diagonal-sequence footfall patterns, a complex suite of biomechanical characters emerges in primates that allow for the co-option of hands toward non-locomotor roles. Early selection for limb functional differentiation in primates probably aided the evolution of fine manipulation capabilities in the hands of bipedal humans.

Surprising trunk rotational capabilities in chimpanzees and implications for bipedal walking proficiency in early hominins.

Human walking entails coordinated out-of-phase axial rotations of the thorax and pelvis. A long-held assumption is that this ability relies on adaptations for trunk flexibility present in humans, but not in chimpanzees, other great apes, or australopithecines. Here we use three-dimensional kinematic analyses to show that, contrary to current thinking, chimpanzees walking bipedally rotate their lumbar and thoracic regions in a manner similar to humans. This occurs despite differences in the magnitude of trunk motion, and despite morphological differences in truncal 'rigidity' between species. These results suggest that, like humans and chimpanzees, early hominins walked with upper body rotations that countered pelvic rotation. We demonstrate that even if early hominins walked with pelvic rotations 50% larger than humans, they may have accrued the energetic and mechanical benefits of out-of-phase thoracic rotations. This would have allowed early hominins to reduce work and locomotor cost, improving walking efficiency early in hominin evolution.

Three-dimensional kinematics of the pelvis and hind limbs in chimpanzee (Pan troglodytes) and human bipedal walking.

The common chimpanzee (Pan troglodytes) is a facultative biped and our closest living relative. As such, the musculoskeletal anatomies of their pelvis and hind limbs have long provided a comparative context for studies of human and fossil hominin locomotion. Yet, how the chimpanzee pelvis and hind limb actually move during bipedal walking is still not well defined. Here, we describe the three-dimensional (3-D) kinematics of the pelvis, hip, knee and ankle during bipedal walking and compare those values to humans walking at the same dimensionless and dimensional velocities. The stride-to-stride and intraspecific variations in 3-D kinematics were calculated using the adjusted coefficient of multiple correlation. Our results indicate that humans walk with a more stable pelvis than chimpanzees, especially in tilt and rotation. Both species exhibit similar magnitudes of pelvis list, but with segment motion that is opposite in phasing. In the hind limb, chimpanzees walk with a more flexed and abducted limb posture, and substantially exceed humans in the magnitude of hip rotation during a stride. The average stride-to-stride variation in joint and segment motion was greater in chimpanzees than humans, while the intraspecific variation was similar on average. These results demonstrate substantial differences between human and chimpanzee bipedal walking, in both the sagittal and non-sagittal planes. These new 3-D kinematic data are fundamental to a comprehensive understanding of the mechanics, energetics and control of chimpanzee bipedalism.

Electromyography of crural and pedal muscles in tufted capuchin monkeys (Sapajus apella): Implications for hallucal grasping behavior and first metatarsal morphology in euprimates.

A hypertrophied peroneal process of the hallucal metatarsal, as seen in prosimians, has been linked to a powerful hallucal grasp via the contraction of the peroneus longus (PL) muscle causing adduction of the big toe. Electromyography (EMG) studies of lemurs and lorises, however, have concluded that PL is not substantially recruited during small branch locomotion when powerful hallucal grasping is needed most, and have suggested that there is no link between PL activity and peroneal process size. If this is correct, then we should also observe no change in PL activity when strong hallucal grasping is required in anthropoids because they have a relatively smaller peroneal process for PL to act on. This study addresses this hypothesis by evaluating EMG of crural and pedal muscles in capuchins (Sapajus apella) walking on substrates of different diameters. During locomotion on the narrow substrate (3.1 cm) that should elicit a strong hallucal grasp, we observed an intense increased recruitment of adductor hallucis, but only sustained, rather than markedly increased, PL activity. This indicates that PL is not involved in powerful hallucal grasping in capuchins, and confirms similar findings previously documented in prosimians. We continue to reject the hypothesis that a large peroneal process is an adaptation for powerful grasping and further argue that its morphology may not be related to PL's ability to adduct the hallux at all. In addition, the morphology of the peroneal process should not be used to assess hallucal grasping performance in fossils.

Rotator cuff muscle size and the interpretation of scapular shape in primates.

Scapular shape variation among primates is widely viewed as being strongly related to locomotor differences. The relative importance of overhead forelimb elevation in the locomotor repertoire of a species, as reflected in muscular leverage for scapular rotation or in the sizes of attachment areas for muscles involved in glenohumeral elevation, has proven to be a useful organizing principle for understanding this variation. While generally successful in sorting primate scapulae into functional groups, the scapulae of some species do not entirely match predictions based on the perceived importance of forelimb elevation. A recent study has shown that scapular fossa sizes in apes are not as accurate predictors of the sizes of the muscles arising from them as has been assumed. To further explore the degree of correspondence between actual and predicted muscle size based on the perceived importance of forelimb elevation, the current study examines the relative sizes of the rotator cuff muscles in a wider sample of primate taxa using published data on muscle mass and cross-sectional area. The results do not support some of the accepted generalizations about the relative sizes of members of the rotator cuff based on measurements of the sizes of scapular fossae. For example, orthograde apes do not display enlarged supraspinatus muscles compared to pronograde monkeys. Differences in assessments of relative muscle size based on mass compared to those based on cross-sectional area suggest that poor correspondence between muscle size predicted from scapular fossa size and actual muscle size may be related to constraints on scapular form associated with muscular leverage for scapular rotation and with scapular position on the thorax.

Brief communication: Cineradiographic analysis of the chimpanzee (Pan troglodytes) talonavicular and calcaneocuboid joints.

During terrestrial locomotion, chimpanzees exhibit dorsiflexion of the midfoot between midstance and toe-off of stance phase, a phenomenon that has been called the "midtarsal break." This motion is generally absent during human bipedalism, and in chimpanzees is associated with more mobile foot joints than in humans. However, the contribution of individual foot joints to overall foot mobility in chimpanzees is poorly understood, particularly on the medial side of the foot. The talonavicular (TN) and calcaneocuboid (CC) joints have both been suggested to contribute significantly to midfoot mobility and to the midtarsal break in chimpanzees. To evaluate the relative magnitude of motion that can occur at these joints, we tracked skeletal motion of the hindfoot and midfoot during passive plantarflexion and dorsiflexion manipulations using cineradiography. The sagittal plane range of motion was 38 ± 10° at the TN joint and 14 ± 8° at the CC joint. This finding indicates that the TN joint is more mobile than the CC joint during ankle plantarflexion-dorsiflexion. We suggest that the larger range of motion at the TN joint during dorsiflexion is associated with a rotation (inversion-eversion) across the transverse tarsal joint, which may occur in addition to sagittal plane motion.

A three-dimensional musculoskeletal model of the chimpanzee (Pan troglodytes) pelvis and hind limb.

Musculoskeletal models have become important tools for studying a range of muscle-driven movements. However, most work has been in modern humans, with few applications in other species. Chimpanzees are facultative bipeds and our closest living relatives, and have provided numerous important insights into our own evolution. A chimpanzee musculoskeletal model would allow integration across a wide range of laboratory-based experimental data, providing new insights into the determinants of their locomotor performance capabilities, as well as the origins and evolution of human bipedalism. Here, we described a detailed three-dimensional (3D) musculoskeletal model of the chimpanzee pelvis and hind limb. The model includes geometric representations of bones and joints, as well as 35 muscle-tendon units that were represented using 44 Hill-type muscle models. Muscle architecture data, such as muscle masses, fascicle lengths and pennation angles, were drawn from literature sources. The model permits calculation of 3D muscle moment arms, muscle-tendon lengths and isometric muscle forces over a wide range of joint positions. Muscle-tendon moment arms predicted by the model were generally in good agreement with tendon-excursion estimates from cadaveric specimens. Sensitivity analyses provided information on the parameters that model predictions are most and least sensitive to, which offers important context for interpreting future results obtained with the model. Comparisons with a similar human musculoskeletal model indicate that chimpanzees are better suited for force production over a larger range of joint positions than humans. This study represents an important step in understanding the integrated function of the neuromusculoskeletal systems in chimpanzee locomotion.

Rotator cuff muscle function and its relation to scapular morphology in apes.

It is widely held that many differences among primate species in scapular morphology can be functionally related to differing demands on the shoulder associated with particular locomotor habits. This perspective is largely based on broad scale studies, while more narrow comparisons of scapular form often fail to follow predictions based on inferred differences in shoulder function. For example, the ratio of supraspinous fossa/infraspinous fossa size in apes is commonly viewed as an indicator of the importance of overhead use of the forelimb, yet paradoxically, the African apes, the most terrestrial of the great apes, have higher scapular fossa ratios than the more suspensory orangutan. The recent discovery of several nearly complete early hominin scapular specimens, and their apparent morphological affinities to scapulae of orangutans and gorillas rather than chimpanzees, has led to renewed interest in the comparative analysis of human and extant ape scapular form. To facilitate the functional interpretation of differences in ape scapulae, particularly in regard to relative scapular fossa size, we used electromyography (EMG) to document the activity patterns in all four rotator cuff muscles in orangutans and gibbons, comparing the results with previously published data for chimpanzees. The EMG results indicate that the distinctive contributions of each cuff muscle to locomotion are the same in the three ape species, failing to support inferences of differences in rotator cuff function based on relative scapular fossa size comparisons. It is also shown that relative scapular fossa size is not in fact a good predictor of either the relative masses or cross-sectional areas of the rotator cuff muscles in apes, and relative fossa size gives a false impression of the importance of individual cuff muscles to locomotor differences among apes. A possible explanation for the disparity between fossa and muscle size relates to the underappreciated role of the scapular spine in structural reinforcement of the blade.

Electromyography of wrist and finger flexor muscles in olive baboons (Papio anubis).

Some non-human primates use digitigrade hand postures when walking slowly on the ground. As a component of an extended limb, a digitigrade posture can help minimize wrist joint moments thereby requiring little force production directly from wrist flexors (and/or from the assistance of finger flexors) to maintain limb posture. As a consequence, less active muscle volume would be required from these anti-gravity muscles and overall metabolic costs associated with locomotion could be reduced. To investigate whether the use of digitigrade hand postures during walking in primates entails minimal use of anti-gravity muscles, this study examined electromyography (EMG) patterns in both the wrist and finger flexor muscles in facultatively digitigrade olive baboons (Papio anubis) across a range of speeds. The results demonstrate that baboons can adopt a digitigrade hand posture when standing and moving at slow speeds without requiring substantial EMG activity from distal anti-gravity muscles. Higher speed locomotion, however, entails increasing EMG activity and is accompanied by a dynamic shift to a more palmigrade-like limb posture. Thus, the ability to adopt a digitigrade hand posture by monkeys is an adaptation for ground living, but it was never co-opted for fast locomotion. Rather, digitigrady in primates appears to be related to energetic efficiency for walking long distances.

Hallucal grasping in Nycticebus coucang: further implications for the functional significance of a large peroneal process.

Euprimate grasping feet are characterized by a suite of morphological traits, including an enlarged peroneal process on the base of the first metatarsal, which serves as the insertion site of the peroneus longus muscle. In prosimians, a large process has typically been associated with a powerful hallucal grasp via the contraction of the peroneus longus to adduct the hallux. Recent electromyography (EMG) studies have documented that peroneus longus does not contribute substantially to hallucal grasping in lemurids (Boyer et al., 2007). However, non-lemurid prosimians have a I-V opposable grasp complex that is morphologically different and phylogenetically more primitive than the I-II adductor grasp complex of the lemurids previously studied. Therefore, it is possible that peroneus longus did function during grasping in early euprimates, but lost this function in large-bodied lemurids. The present study tests the hypothesis that a large peroneal process is related to powerful grasping ability in primates displaying the more primitive I-V grasp complex. We use EMG to evaluate the recruitment of peroneus longus, other crural muscles, and adductor hallucis in static and locomotor grasping activities of the slow loris (Nycticebus coucang). Results show that peroneus longus is active during grasping behaviors that require the subject to actively resist inversion of the foot, and likely contributes to a hallucal grasp in these activities. Peroneus longus activity level does not differ between grasping and power grasping activities, nor does it differ between grasping and non-grasping locomotor modes. Conversely, the digital flexors and hallucal adductor are recruited at higher levels during power grasping and grasping locomotor modes. Consequently, we reject the hypothesis that an enlarged peroneal process represents an adaptation specifically to enhance the power of the I-V grasp, but accept that the muscle likely plays a role in adducting the hallux during grasping behaviors that require stabilization of the ankle, and suggest that further work is necessary to determine if this role is sufficient to drive selection for a large peroneal process.

Hip extensor EMG and forelimb/hind limb weight support asymmetry in primate quadrupeds.

Higher weight support on the hind limb than forelimb is among the distinctive characteristics of primate quadrupeds. Although often assumed to be due to a more posteriorly positioned whole body center of mass, there are little data to support such a difference. Reynolds (1985. Am J Phys Anthropol 67:335-349) notes that the distribution of forces on the limbs can also be influenced by average limb posture, but suggests that this effect is too small to account for the asymmetry in weight support observed in primates. Instead, he proposes that high hind limb forces are brought about by an active process of shifting weight off the forelimbs and onto the hind limbs through use of hind limb retractors. In this study, we use video records of walking animals to explore the degree to which average limb posture in primates and other quadrupedal mammals deviates from vertical, and use electromyography to test Reynolds' model of hind limb retractor activity and posterior weight shift. The limb posture results indicate that primate forelimbs oscillate about a vertical or slightly retracted axis, and though the hind limbs are slightly protracted, the magnitude of deviation from vertical is too small to have a major effect on weight support distribution. The electromyographic results reveal higher levels of hip extensor activity in antipronograde primates that bear a higher proportion of weight on their hind limbs. This lends support to Reynolds' suggestion that some primates use muscles to actively shift weight onto hind limbs to relieve stresses on forelimbs less well structured for weight support.

The primitive wrist of Homo floresiensis and its implications for hominin evolution.

Whether the Late Pleistocene hominin fossils from Flores, Indonesia, represent a new species, Homo floresiensis, or pathological modern humans has been debated. Analysis of three wrist bones from the holotype specimen (LB1) shows that it retains wrist morphology that is primitive for the African ape-human clade. In contrast, Neandertals and modern humans share derived wrist morphology that forms during embryogenesis, which diminishes the probability that pathology could result in the normal primitive state. This evidence indicates that LB1 is not a modern human with an undiagnosed pathology or growth defect; rather, it represents a species descended from a hominin ancestor that branched off before the origin of the clade that includes modern humans, Neandertals, and their last common ancestor.

Homo floresiensis and the evolution of the hominin shoulder.

The holotype of Homo floresiensis, diminutive hominins with tiny brains living until 12,000 years ago on the island of Flores, is a partial skeleton (LB1) that includes a partial clavicle (LB1/5) and a nearly complete right humerus (LB1/50). Although the humerus appears fairly modern in most regards, it is remarkable in displaying only 110 degrees of humeral torsion, well below modern human average values. Assuming a modern human shoulder configuration, such a low degree of humeral torsion would result in a lateral set to the elbow. Such an elbow joint would function more nearly in a frontal than in a sagittal plane, and this is certainly not what anyone would have predicted for a tool-making Pleistocene hominin. We argue that Homo floresiensis probably did not have a modern human shoulder configuration: the clavicle was relatively short, and we suggest that the scapula was more protracted, resulting in a glenoid fossa that faced anteriorly rather than laterally. A posteriorly directed humeral head was therefore appropriate for maintaining a normally functioning elbow joint. Similar morphology in the Homo erectus Nariokotome boy (KNM-WT 15000) suggests that this shoulder configuration may represent a transitional stage in pectoral girdle evolution in the human lineage.