Variation, mosaicism and degeneracy in the hominin foot.

The fossil record is scarce and incomplete by nature. Animals and ecological processes devour soft tissue and important bony details over time and, when the dust settles, we are faced with a patchy record full of variation. Fossil taxa are usually defined by craniodental characteristics, so unless postcranial bones are found associated with a skull, assignment to taxon is unstable. Naming a locomotor category based on fossil bone morphology by analogy to living hominoids is not uncommon, and when no single locomotor label fits, postcrania are often described as exhibiting a 'mosaic' of traits. Here, we contend that the unavoidable variation that characterises the fossil record can be described far more rigorously based on extensive work in human neurobiology and neuroanatomy, movement sciences and motor control and biomechanics research. In neurobiology, degeneracy is a natural mechanism of adaptation allowing system elements that are structurally different to perform the same function. This concept differs from redundancy as understood in engineering, where the same function is performed by identical elements. Assuming degeneracy, structurally different elements are able to produce different outputs in a range of environmental contexts, favouring ecological robusticity by enabling adaptations. Furthermore, as degeneracy extends to genome level, genetic variation is sustained, so that genes which might benefit an organism in a different environment remain part of the genome, favouring species' evolvability.

Human bipedal instability in tree canopy environments is reduced by "light touch" fingertip support.

Whether tree canopy habitats played a sustained role in the ecology of ancestral bipedal hominins is unresolved. Some argue that arboreal bipedalism was prohibitively risky for hominins whose increasingly modern anatomy prevented them from gripping branches with their feet. Balancing on two legs is indeed challenging for humans under optimal conditions let alone in forest canopy, which is physically and visually highly dynamic. Here we quantify the impact of forest canopy characteristics on postural stability in humans. Viewing a movie of swaying branches while standing on a branch-like bouncy springboard destabilised the participants as much as wearing a blindfold. However "light touch", a sensorimotor strategy based on light fingertip support, significantly enhanced their balance and lowered their thigh muscle activity by up to 30%. This demonstrates how a light touch strategy could have been central to our ancestor's ability to avoid falls and reduce the mechanical and metabolic cost of arboreal feeding and movement. Our results may also indicate that some adaptations in the hand that facilitated continued access to forest canopy may have complemented, rather than opposed, adaptations that facilitated precise manipulation and tool use.

Does footprint depth correlate with foot motion and pressure?

Footprints are the most direct source of evidence about locomotor biomechanics in extinct vertebrates. One of the principal suppositions underpinning biomechanical inferences is that footprint geometry correlates with dynamic foot pressure, which, in turn, is linked with overall limb motion of the trackmaker. In this study, we perform the first quantitative test of this long-standing assumption, using topological statistical analysis of plantar pressures and experimental and computer-simulated footprints. In computer-simulated footprints, the relative distribution of depth differed from the distribution of both peak and pressure impulse in all simulations. Analysis of footprint samples with common loading inputs and similar depths reveals that only shallow footprints lack significant topological differences between depth and pressure distributions. Topological comparison of plantar pressures and experimental beach footprints demonstrates that geometry is highly dependent on overall print depth; deeper footprints are characterized by greater relative forefoot, and particularly toe, depth than shallow footprints. The highlighted difference between 'shallow' and 'deep' footprints clearly emphasizes the need to understand variation in foot mechanics across different degrees of substrate compliance. Overall, our results indicate that extreme caution is required when applying the 'depth equals pressure' paradigm to hominin footprints, and by extension, those of other extant and extinct tetrapods.

A new method for recording complex positional behaviours and habitat interactions in primates.

In an arboreal habitat, primates have to cope with a complex meshwork of flexible supports in order to obtain food, find mates and avoid predators. To understand how animals interact with such complex environments we can study their positional behaviour. However, due to the intricate variation in locomotion and posture it can be difficult to capture details such as limb use (i.e. weight and balance), limb flexion and substrate use. This paper presents a suitable method replicable for any primate species, based on the movement notation technique, Sutton Movement Writing (SMW), aiming to record the spatial arrangement of limbs during positional behaviours on multiple, compliant supports. This method was piloted during a year-long field study of wild orangutans (Pongo abelii) and validated and tested for inter- and intraobserver reliability using videos from the field. Overall, SMW shows considerable promise for increasing the resolution with which positional behaviours can be recorded under field conditions and provides a way to extract numerical data for use in statistical analyses. This will facilitate our understanding of how behaviours vary in response to the environment, and the capabilities of primates to perform key tasks in their distinct niches.

The biomechanics of leaping in gibbons.

Gibbons are skilled brachiators but they are also highly capable leapers, crossing distances in excess of 10 m in the wild. Despite this impressive performance capability, no detailed biomechanical studies of leaping in gibbons have been undertaken to date. We measured ground reaction forces and derived kinematic parameters from high-speed videos during gibbon leaps in a captive zoo environment. We identified four distinct leap types defined by the number of feet used during take-off and the orientation of the trunk, orthograde single-footed, orthograde two-footed, orthograde squat, and pronograde single-footed leaps. The center of mass trajectories of three of the four leap types were broadly similar, with the pronograde single-footed leaps exhibiting less vertical displacement of the center of mass than the other three types. Mechanical energy at take-off was similar in all four leap types. The ratio of kinetic energy to mechanical energy was highest in pronograde single-footed leaps and similar in the other three leap types. The highest mechanical work and power were generated during orthograde squat leaps. Take-off angle decreased with take-off velocity and the hind limbs showed a proximal to distal extension sequence during take-off. In the forelimbs, the shoulder joints were always flexed at take-off, while the kinematics of the distal joints (elbow and wrist joints) were variable between leaps. It is possible that gibbons may utilize more metabolically expensive orthograde squat leaps when a safe landing is uncertain, while more rapid (less expensive) pronograde single-footed leaps might be used during bouts of rapid locomotion when a safe landing is more certain.

Nonlinear spatial warping for between-subjects pedobarographic image registration.

Foot size and shape vary between individuals and the foot adopts arbitrary stance phase postures, so traditional pedobarographic analyses regionalize foot pressure images to afford homologous data comparison. An alternative approach that does not require explicit anatomical labelling and that is used widely in other functional imaging domains is to register images such that homologous structures optimally overlap and then to compare images directly at the pixel level. Image registration represents the preprocessing cornerstone of such pixel-level techniques, so its performance warrants independent attention. The purpose of this study was to evaluate the performance of four between-subjects warping registration algorithms including: Principal Axes (PA), four-parameter Optimal Scaling (OS4), eight-parameter Optimal Projective (OP8), and locally affine Nonlinear (NL). Fifteen subjects performed 10 trials of self-paced walking, and their peak pressure images were registered within-subjects using an optimal rigid body transformation. The resulting mean images were then registered between-subjects using all four methods in all 210 (15x14) subject combinations. All registration methods improved alignment, and each method performed qualitatively well for certain image pairs. However, only the NL consistently performed satisfactorily because of disproportionate anatomical variation in toe lengths and rearfoot/forefoot width, for example. Using three independent image (dis)similarity metrics, MANOVA confirmed that the NL method yielded superior registration performance (p<0.001). These data demonstrate that nonlinear spatial warping is necessary for robust between-subject pedobarographic image registration and, by extension, robust homologous data comparison at the pixel level.

Masticatory loading and bone adaptation in the supraorbital torus of developing macaques.

Research on the evolution and adaptive significance of primate craniofacial morphologies has focused on adult, fully developed individuals. Here, we investigate the possible relationship between the local stress environment arising from masticatory loadings and the emergence of the supraorbital torus in the developing face of the crab-eating macaque Macaca fascicularis. By using finite element analysis (FEA), we are able to evaluate the hypothesis that strain energy density (SED) magnitudes are high in subadult individuals with resulting bone growth in the supraorbital torus. We developed three micro-CT-based FEA models of M. fascicularis skulls ranging in dental age from deciduous to permanent dentitions and validated them against published experimental data. Applied masticatory muscle forces were estimated from physiological cross-sectional areas of macaque cadaveric specimens. The models were sequentially constrained at each working side tooth to simulate the variation of the bite point applied during masticatory function. Custom FEA software was used to solve the voxel-based models and SED and principal strains were computed. A physiological superposition SED map throughout the face was created by allocating to each element the maximum SED value from each of the load cases. SED values were found to be low in the supraorbital torus region throughout ontogeny, while they were consistently high in the zygomatic arch and infraorbital region. Thus, if the supraorbital torus arises to resist masticatory loads, it is either already adapted in each of our subadult models so that we do not observe high SED or a lower site-specific bone deposition threshold must apply.

Locomotion and posture from the common hominoid ancestor to fully modern hominins, with special reference to the last common panin/hominin ancestor.

Based on our knowledge of locomotor biomechanics and ecology we predict the locomotion and posture of the last common ancestors of (a) great and lesser apes and their close fossil relatives (hominoids); (b) chimpanzees, bonobos and modern humans (hominines); and (c) modern humans and their fossil relatives (hominins). We evaluate our propositions against the fossil record in the context of a broader review of evolution of the locomotor system from the earliest hominoids of modern aspect (crown hominoids) to early modern Homo sapiens. While some early East African stem hominoids were pronograde, it appears that the adaptations which best characterize the crown hominoids are orthogrady and an ability to abduct the arm above the shoulder - rather than, as is often thought, manual suspension sensu stricto. At 7-9 Ma (not much earlier than the likely 4-8 Ma divergence date for panins and hominins, see Bradley, 2008) there were crown hominoids in southern Europe which were adapted to moving in an orthograde posture, supported primarily on the hindlimb, in an arboreal, and possibly for Oreopithecus, a terrestrial context. By 7 Ma, Sahelanthropus provides evidence of a Central African hominin, panin or possibly gorilline adapted to orthogrady, and both orthogrady and habitually highly extended postures of the hip are evident in the arboreal East African protohominin Orrorin at 6 Ma. If the traditional idea that hominins passed through a terrestrial 'knuckle-walking' phase is correct, not only does it have to be explained how a quadrupedal gait typified by flexed postures of the hindlimb could have preadapted the body for the hominin acquisition of straight-legged erect bipedality, but we would have to accept a transition from stem-hominoid pronogrady to crown hominoid orthogrady, back again to pronogrady in the African apes and then back to orthogrady in hominins. Hand-assisted arboreal bipedality, which is part of a continuum of orthograde behaviours, is used by modern orangutans to forage among the small branches at the periphery of trees where the core hominoid dietary resource, ripe fruit, is most often to be found. Derivation of habitual terrestrial bipedality from arboreal hand-assisted bipedality requires fewer transitions, and is also kinematically and kinetically more parsimonious.

Origin of human bipedalism as an adaptation for locomotion on flexible branches.

Human bipedalism is commonly thought to have evolved from a quadrupedal terrestrial precursor, yet some recent paleontological evidence suggests that adaptations for bipedalism arose in an arboreal context. However, the adaptive benefit of arboreal bipedalism has been unknown. Here we show that it allows the most arboreal great ape, the orangutan, to access supports too flexible to be negotiated otherwise. Orangutans react to branch flexibility like humans running on springy tracks, by increasing knee and hip extension, whereas all other primatesdothe reverse. Human bipedalism is thus less an innovation than an exploitation of a locomotor behavior retained from the common great ape ancestor.

Orangutans use compliant branches to lower the energetic cost of locomotion.

Within the forest canopy, the shortest gaps between tree crowns lie between slender terminal branches. While the compliance of these supports has previously been shown to increase the energetic cost of gap crossing in arboreal animals (e.g. Alexander 1991 Z. Morphol. Anthropol. 78, 315-320; Demes et al. 1995 Am. J. Phys. Anthropol. 96, 419-429), field observations suggest that some primates may be able to use support compliance to increase the energetic efficiency of locomotion. Here, we calculate the energetic cost of alternative methods of gap crossing in orangutans (Pongo abelii). Tree sway (in which orangutans oscillate a compliant tree trunk with increasing magnitude to bridge a gap) was found to be less than half as costly as jumping, and an order of magnitude less costly than descending the tree, walking to the vine and climbing it. Observations of wild orangutans suggest that they actually use support compliance in many aspects of their locomotor behaviour. This study seems to be the first to show that elastic compliance in arboreal supports can be used to reduce the energetic cost of gap crossing.

Assessing mechanical function of the zygomatic region in macaques: validation and sensitivity testing of finite element models.

Crucial to the interpretation of the results of any finite element analysis of a skeletal system is a test of the validity of the results and an assessment of the sensitivity of the model parameters. We have therefore developed finite element models of two crania of Macaca fascicularis and investigated their sensitivity to variations in bone material properties, the zygomatico-temporal suture and the loading regimen applied to the zygomatic arch. Maximum principal strains were validated against data derived from ex vivo strain gauge experiments using non-physiological loads applied to the macaque zygomatic arch. Elastic properties of the zygomatic arch bone and the zygomatico-temporal suture obtained by nanoindentation resulted in a high degree of congruence between experimental and simulated strains. The findings also indicated that the presence of a zygomatico-temporal suture in the model produced strains more similar to experimental values than a completely separated or fused arch. Strains were distinctly higher when the load was applied through the modelled superficial masseter compared with loading an array of nodes on the arch. This study demonstrates the importance of the accurate selection of the material properties involved in predicting strains in a finite element model. Furthermore, our findings strongly highlight the influence of the presence of craniofacial sutures on strains experienced in the face. This has implications when investigating craniofacial growth and masticatory function but should generally be taken into account in functional analyses of the craniofacial system of both extant and extinct species.

Morphological analysis of the hindlimb in apes and humans. II. Moment arms.

Flexion/extension moment arms were obtained for the major muscles crossing the hip, knee and ankle joints in the orang-utan, gibbon, gorilla (Eastern and Western lowland) and bonobo. Moment arms varied with joint motion and were generally longer in proximal limb muscles than distal limb muscles. The shape of the moment arm curves (i.e. the plots of moment arm against joint angle) differed in different hindlimb muscles and in the same muscle in different subjects (both in the same and in different ape species). Most moment arms increased with increasing joint flexion, a finding which may be understood in the context of the employment of flexed postures by most non-human apes (except orang-utans) during both terrestrial and arboreal locomotion. When compared with humans, non-human great apes tended to have muscles better designed for moving the joints through large ranges. This was particularly true of the pedal digital flexors in orang-utans. In gibbons, the only lesser ape studied here, many of the moment arms measured were relatively short compared with those of great apes. This study was performed on a small sample of apes and thus differences noted here warrant further investigation in larger populations.

Morphological analysis of the hindlimb in apes and humans. I. Muscle architecture.

We present quantitative data on the hindlimb musculature of Pan paniscus, Gorilla gorilla gorilla, Gorilla gorilla graueri, Pongo pygmaeus abelii and Hylobates lar and discuss the findings in relation to the locomotor habits of each. Muscle mass and fascicle length data were obtained for all major hindlimb muscles. Physiological cross-sectional area (PCSA) was estimated. Data were normalized assuming geometric similarity to allow for comparison of animals of different size/species. Muscle mass scaled closely to (body mass)(1.0) and fascicle length scaled closely to (body mass)(0.3) in most species. However, human hindlimb muscles were heavy and had short fascicles per unit body mass when compared with non-human apes. Gibbon hindlimb anatomy shared some features with human hindlimbs that were not observed in the non-human great apes: limb circumferences tapered from proximal-to-distal, fascicle lengths were short per unit body mass and tendons were relatively long. Non-human great ape hindlimb muscles were, by contrast, characterized by long fascicles arranged in parallel, with little/no tendon of insertion. Such an arrangement of muscle architecture would be useful for locomotion in a three dimensionally complex arboreal environment.

Analysis of the human and ape foot during bipedal standing with implications for the evolution of the foot.

The ratio of the power arm (the distance from the heel to the talocrural joint) to the load arm (that from the talocrural joint to the distal head of the metatarsals), or RPL, differs markedly between the human and ape foot. The arches are relatively higher in the human foot in comparison with those in apes. This study evaluates the effect of these two differences on biomechanical effectiveness during bipedal standing, estimating the forces acting across the talocrural and tarsometatarsal joints, and attempts to identify which type of foot is optimal for bipedal standing. A simple model of the foot musculoskeletal system was built to represent the geometric and force relationships in the foot during bipedal standing, and measurements for a variety of human and ape feet applied. The results show that: (1) an RPL of around 40% (as is the case in the human foot) minimizes required muscle force at the talocrural joint; (2) the presence of an high arch in the human foot reduces forces in the plantar musculature and aponeurosis; and (3) the human foot has a lower total of force in joints and muscles than do the ape feet. These results indicate that the proportions of the human foot, and the height of the medial arch are indeed better optimized for bipedal standing than those of apes, further suggesting that their current state is to some extent the product of positive selection for enhanced bipedal standing during the evolution of the foot.

Stresses exerted in the hindlimb muscles of common chimpanzees (Pan troglodytes) during bipedal locomotion.

Recent studies have indicated that chimpanzee bipedality is mechanically inefficient and dynamically unlike that of humans, thus undermining the chimpanzee analogy for mechanical aspects of the early evolution of hominid bipedalism. This paper continues this theme by measuring the forces and stresses engendered by the muscles during bipedal locomotion, for an untrained chimpanzee and for data from chimpanzees which have been encouraged to walk bipedally, presented in the literature. Peak stresses in the triceps surae were lower for the untrained chimpanzee than for the trained subjects because during the late stance phase, when peak ankle moments occur, the centre of pressure of the ground reaction force on the foot of the untrained chimpanzee stayed close to the ankle joint. In contrast, for the trained subjects it moved closer to the toes, as in human bipedalism. Quadriceps and hip extensor stresses are approximately 30% larger for the untrained chimpanzee than for the trained subjects, because the trained chimpanzees walked with a more erect posture. These results may reflect the way in which muscles can develop in response to training, since research on humans has shown that muscle physiological cross-sectional area increases as a result of exercise, resulting in smaller stresses for a given muscle force. During a slow walk, untrained chimpanzees were found to exert far greater muscle stresses than humans do when running at moderate speed, particularly in the muscles that extend the hip, because of the bent-hip, bent-knee posture.

Automatic monitoring of primate locomotor behaviour using accelerometers.

Accelerometry data were transmitted by a radio collar attached to a hand-reared red-ruffed lemur housed in a large indoor/outdoor enclosure at Chester Zoo. An observer simultaneously recorded locomotor behaviour using a manually operated event recorder. Both data streams were recorded directly to hard disk to ensure accurate synchrony. Leaps were modelled using a y = x2 - x3 formulation for the take-off acceleration, to link peak acceleration to leap distance. Cyclic locomotor modes were analysed using power spectra and the modal frequency used to estimate stride periodicity. Comparison of the dual data shows that leaping behaviour can be recorded reliably, and acceleration magnitude provides accurate predictions of the distance travelled. Cyclic activities were less well characterised, but calibration should permit travel distance estimations equalling or bettering those from conventional techniques.

The role of load-carrying in the evolution of modern body proportions.

The first unquestionably bipedal early human ancestors, the species Australopithecus afarensis, were markedly different to ourselves in body proportions, having a long trunk and short legs. Some have argued that 'chimpanzee-like' features such as these suggest a 'bent-hip, bent-knee' (BHBK) posture would have been adopted during gait. Computer modelling studies, however, indicate that this early human ancestor could have walked in a reasonably efficient upright posture, whereas BHBK posture would have nearly doubled the mechanical energy cost of locomotion, as it does the physiological cost of locomotion in ourselves. More modern body proportions first appear at around 1.8-1.5 Ma, with Homo ergaster (early African Homo erectus), represented by the Nariokotome skeleton KNM-WT 15000, in which the legs were considerably longer in relation to the trunk than they are in human adults, although this skeleton represents an adolescent. Several authors have suggested that this morphology would have allowed faster, more endurant walking. But during the same period, the archaeological record indicates a sharp rise in distances over which stone tools or raw materials are transported. Is this coincidental, or can load-carrying also be implicated in selection for a more modern morphology? Computer simulations of loaded walking, verified against kinetic data for humans, show that BHBK gait is even more ineffective while load-carrying. However, walking erect, the Nariokotome individual could have carried loads of 10-15% body mass for less cost, relative to body size, than AL 288-1 walking erect but unloaded. In fact, to the extent that our sample of humans is typical, KNM-WT 15000 would have had better mechanical effectiveness in bearing light loads on the back than modern human adults. Thus, selection for effectiveness in load-carrying, as well as in endurant walking, is indeed likely to have been implicated in the evolution of modern body proportions.

Size and power required for motion with implication for the evolution of early hominids.

The fossil record of early hominids (early human ancestors) suggests that their stature and weight had a tendency to increase, but their robusticity (the proportion of radius to length) to decrease. Using a simple musculo-skeletal model, this paper explores possible relationships between size, power required for motion (PRM) and cycle-time, deriving relationships which indicate that PRM per unit of mass and velocity is proportional to robusticity, but inversely proportional to stature. The results derived appear to be in general agreement with published data from physiological experiments. If the material properties of early hominids were similar to those of modern humans and the achievement of minimum PRM was the selective criterion, human stature might tend to increase slightly in human evolution (and, if selective pressures are not removed, might do so in the future but at lower rate). If mobility and stability under loading are the selective criteria, however, human size should not substantially increase in the future.

Energy transformation during erect and 'bent-hip, bent-knee' walking by humans with implications for the evolution of bipedalism.

We have previously reported that predictive dynamic modeling suggests that the 'bent-hip, bent-knee' gait, which some attribute to Australopithecus afarensis AL-288-1, would have been much more expensive in mechanical terms for this hominid than an upright gait. Normal walking by modern adult humans owes much of its efficiency to conservation of energy by transformation between its potential and kinetic states. These findings suggest the question if, and to what extent, energy transformation exists in 'bent-hip, bent-knee' gait. This study calculates energy transformation in humans walking upright, at three different speeds, and walking 'bent-hip, bent-knee'. Kinematic data were gathered from video sequences and kinetic (ground reaction force) data from synchronous forceplate measurement. Applying Newtonian mechanics to our experimental data, the fluctuations of kinetic and potential energy in the body centre of mass were obtained and the effects of energy transformation evaluated and compared. In erect walking the fluctuations of two forms of energy are indeed largely out-of-phase, so that energy transformation occurs and total energy is conserved. In 'bent-hip, bent-knee' walking, however, the fluctuations of the kinetic and potential energy are much more in-phase, so that energy transformation occurs to a much lesser extent. Among all modes of walking the highest energy recovery is obtained in subjectively 'comfortable' walking, the next highest in subjectively 'fast' or 'slow' walking, and the least lowest in 'bent-hip, bent-knee' walking. The results imply that if 'bent-hip, bent-knee' gait was indeed habitually practiced by early bipedal hominids, a very substantial (and in our view as yet unidentified) selective advantage would have had to accrue, to offset the selective disadvantages of 'bent-hip, bent-knee' gait in terms of energy transformation.

Predicting the metabolic energy costs of bipedalism using evolutionary robotics.

To understand the evolution of bipedalism among the hominoids in an ecological context we need to be able to estimate the energetic cost of locomotion in fossil forms. Ideally such an estimate would be based entirely on morphology since, except for the rare instances where footprints are preserved, this is the only primary source of evidence available. In this paper we use evolutionary robotics techniques (genetic algorithms, pattern generators and mechanical modeling) to produce a biomimetic simulation of bipedalism based on human body dimensions. The mechanical simulation is a seven-segment, two-dimensional model with motive force provided by tension generators representing the major muscle groups acting around the lower-limb joints. Metabolic energy costs are calculated from the muscle model, and bipedal gait is generated using a finite-state pattern generator whose parameters are produced using a genetic algorithm with locomotor economy (maximum distance for a fixed energy cost) as the fitness criterion. The model is validated by comparing the values it generates with those for modern humans. The result (maximum efficiency of 200 J m(-1)) is within 15% of the experimentally derived value, which is very encouraging and suggests that this is a useful analytic technique for investigating the locomotor behaviour of fossil forms. Initial work suggests that in the future this technique could be used to estimate other locomotor parameters such as top speed. In addition, the animations produced by this technique are qualitatively very convincing, which suggests that this may also be a useful technique for visualizing bipedal locomotion.