Liza J. Shapiro

Fetal load and the evolution of lumbar lordosis in bipedal hominins.

As predicted by Darwin, bipedal posture and locomotion are key distinguishing features of the earliest known hominins. Hominin axial skeletons show many derived adaptations for bipedalism, including an elongated lumbar region, both in the number of vertebrae and their lengths, as well as a marked posterior concavity of wedged lumbar vertebrae, known as a lordosis. The lordosis stabilizes the upper body over the lower limbs in bipeds by positioning the trunk’s centre of mass (COM) above the hips. However, bipedalism poses a unique challenge to pregnant females because the changing body shape and the extra mass associated with pregnancy shift the trunk’s COM anterior to the hips. Here we show that human females have evolved a derived curvature and reinforcement of the lumbar vertebrae to compensate for this bipedal obstetric load. Similarly dimorphic morphologies in fossil vertebrae of Australopithecus suggest that this adaptation to fetal load preceded the evolution of Homo.

Positional behavior and vertebral morphology in atelines and cebines

Atelines are of particular interest to primate evolutionary studies because they converge with hominoids in postcranial anatomy, including the vertebral column. Currently, our understanding of ateline vertebral morphology is limited to mainly qualitative descriptions and functional interpretations based on general categories of positional behavior. Even less is known about the vertebrae of other platyrrhines. This study more closely examines vertebral form and function in atelines and cebines by combining direct field observations of axial postures and movements, assessments of spinal loading regimes, and a detailed vertebral morphometric analysis. Field observations (Corcovado, Costa Rica) on Ateles geoffroyi, Alouatta palliata, Cebus capucinus, and Saimiri oerstedii were quantified in conjunction with a morphometric analysis of ateline and cebine lumbar vertebrae. Hylobates was also included for comparison. Compared to Cebus and Saimiri, atelines engage more frequently in postures and locomotor behaviors that induce pronounced bending loads on the spine. All atelines share lumbar adaptations for resisting bending, including ventrodorsally elongated vertebral bodies and perpendicularly oriented transverse processes. Among atelines, lumbar region lengths and vertebral bodies are shortest in Ateles and Brachyteles, longest in Alouatta (resembling Cebus), and intermediate in Lagothrix. Compared to Cebus and all atelines, Saimiri has a relatively longer lumbar region, longer and less ventrodorsally expanded vertebral bodies, and more ventrally oriented transverse processes. These features accentuate bending loads, but increase the sagittal flexibility required for leaping. Vertebral convergence between hylobatids and atelines is more readily interpretable as a product of shared spinal loading patterns than shared positional behaviors.

Kinematics of quadrupedal locomotion in sugar gliders (Petaurus breviceps): effects of age and substrate size

SUMMARY Arboreal mammals face unique challenges to locomotor stability. This is particularly true with respect to juveniles, who must navigate substrates similar to those traversed by adults, despite a reduced body size and neuromuscular immaturity. Kinematic differences exhibited by juveniles and adults on a given arboreal substrate could therefore be due to differences in body size relative to substrate size, to differences in neuromuscular development, or to both. We tested the effects of relative body size and age on quadrupedal kinematics in a small arboreal marsupial (the sugar glider, Petaurus breviceps; body mass range of our sample 33-97 g). Juvenile and adult P. breviceps were filmed moving across a flat board and three poles 2.5, 1.0 and 0.5 cm in diameter. Sugar gliders (regardless of age or relative speed) responded to relative decreases in substrate diameter with kinematic adjustments that promote stability; they increased duty factor, increased the average number of supporting limbs during a stride, increased relative stride length and decreased relative stride frequency. Limb phase increased when moving from the flat board to the poles, but not among poles. Compared with adults, juveniles (regardless of relative body size or speed) used lower limb phases, more pronounced limb flexion, and enhanced stability with higher duty factors and a higher average number of supporting limbs during a stride. We conclude that although substrate variation in an arboreal environment presents similar challenges to all individuals, regardless of age or absolute body size, neuromuscular immaturity confers unique problems to growing animals, requiring kinematic compensation.

Reevaluation of the lumbosacral region of Oreopithecus bambolii.

Functional interpretations of the postcranium of the late Miocene ape Oreopithecus bambolii are controversial. The claim that Oreopithecus practiced habitual terrestrial bipedalism is partly based on restored postcranial remains originally recovered from Baccinello, Tuscany (Köhler and Moyà-Solà, 1997). The lower lumbar vertebrae of BA#72 were cited as evidence that Oreopithecus exhibits features indicative of a lordotic lumbar spine, including dorsal wedging of the vertebral bodies and a caudally progressive increase in postzygapophyseal interfacet distance. Here, we demonstrate why the dorsal wedging index value obtained by Köhler and Moyà-Solà (1997) for the BA#72 last lumbar vertebra is questionable due to distortion in that region, present a more reliable way to measure postzygapophyseal interfacet distance, and include an additional metric (laminar width) with which to examine changes in the transverse dimensions of the neural arches. We also quantify the external morphology of the BA#72 proximal sacrum, which, despite well-documented links between sacral morphology and bipedal locomotion, and excellent preservation of the sacral prezygapophyses, first sacral vertebral body, and right ala, was not evaluated by Köhler and Moyà-Solà (1997). Measures of postzygapophyseal interfacet distance and laminar width on the penultimate and last lumbar vertebrae of BA#72 reveal a pattern encompassed within the range of living nonhuman hominoids and unlike that of modern humans, suggesting that Oreopithecus did not possess a lordotic lumbar spine. Results further show that the BA#72 sacrum exhibits relatively small prezygapophyseal articular facet surface areas and mediolaterally narrow alae compared with modern humans, indicating that the morphology of the Oreopithecus sacrum is incompatible with the functional demands of habitual bipedal stance and locomotion. The Oreopithecus lumbosacral region does not exhibit adaptations for habitual bipedal locomotion.

Quadrupedal Locomotion of Saimiri boliviensis: A Comparison of Field and Laboratory-based Kinematic Data

As a result of a plethora of lab-based studies focusing on primate quadrupedalism, it is well known that compared to most other mammals, primates exhibit distinctive quadrupedal kinematics when moving on artificial “terrestrial” or “arboreal” substrates. However, we have little knowledge of how quadrupedal kinematics are impacted by the complexity of natural habitats, in which pathways may be obstructed, unstable, or vary dramatically in size, orientation, shape, or texture. In this study, we compared data on the quadrupedal kinematics of Saimiri boliviensis in both laboratory and field settings by comparing kinematic responses across laboratory substrates (pole, floor) and natural substrates (branches that varied in size and orientation). Field results indicate that Saimiri boliviensis adjusted to larger branches by increasing limb duty factors, but used a wide variety of gait types (as measured by limb phase) across all branch sizes and orientations, rather than fine tuning limb phase to these aspects of substrate. Lab poles elicited similar average limb phases and duty factors, but reduced gait flexibility compared to branches. Lab studies would benefit from greater complexity of simulated arboreal substrates, and field studies should strive to measure numerous substrate characteristics to most effectively test hypotheses about the adaptive nature of primate locomotion.

Human quadrupeds, primate quadrupedalism, and Uner Tan Syndrome.

Since 2005, an extensive literature documents individuals from several families afflicted with “Uner Tan Syndrome (UTS),” a condition that in its most extreme form is characterized by cerebellar hypoplasia, loss of balance and coordination, impaired cognitive abilities, and habitual quadrupedal gait on hands and feet. Some researchers have interpreted habitual use of quadrupedalism by these individuals from an evolutionary perspective, suggesting that it represents an atavistic expression of our quadrupedal primate ancestry or “devolution.” In support of this idea, individuals with “UTS” are said to use diagonal sequence quadrupedalism, a type of quadrupedal gait that distinguishes primates from most other mammals. Although the use of primate-like quadrupedal gait in humans would not be sufficient to support the conclusion of evolutionary “reversal,” no quantitative gait analyses were presented to support this claim. Using standard gait analysis of 518 quadrupedal strides from video sequences of individuals with “UTS”, we found that these humans almost exclusively used lateral sequence–not diagonal sequence–quadrupedal gaits. The quadrupedal gait of these individuals has therefore been erroneously described as primate-like, further weakening the “devolution” hypothesis. In fact, the quadrupedalism exhibited by individuals with UTS resembles that of healthy adult humans asked to walk quadrupedally in an experimental setting. We conclude that quadrupedalism in healthy adults or those with a physical disability can be explained using biomechanical principles rather than evolutionary assumptions.

A new look at the Dynamic Similarity Hypothesis: the importance of swing phase

Summary The Dynamic Similarity Hypothesis (DSH) suggests that when animals of different size walk at similar Froude numbers (equal ratios of inertial and gravitational forces) they will use similar size-corrected gaits. This application of similarity theory to animal biomechanics has contributed to fundamental insights in the mechanics and evolution of a diverse set of locomotor systems. However, despite its popularity, many mammals fail to walk with dynamically similar stride lengths, a key element of gait that determines spontaneous speed and energy costs. Here, we show that the applicability of the DSH is dependent on the inertial forces examined. In general, the inertial forces are thought to be the centripetal force of the inverted pendulum model of stance phase, determined by the length of the limb. If instead we model inertial forces as the centripetal force of the limb acting as a suspended pendulum during swing phase (determined by limb center of mass position), the DSH for stride length variation is fully supported. Thus, the DSH shows that inter-specific differences in spatial kinematics are tied to the evolution of limb mass distribution patterns. Selection may act on morphology to produce a given stride length, or alternatively, stride length may be a “spandrel” of selection acting on limb mass distribution.

Ontogenetic changes in limb postures and their impact on effective limb length in baboons (Papio cynocephalus)

OBJECTIVES Digitigrade hand and foot postures and extended elbows and knees are considered adaptations to running in cursorial mammals because they increase effective limb lengths (ELLs). However, the relationship between digitigrady and ELL in primates is not well understood. We documented the ontogeny of limb postures in baboons to better understand the function of digitigrady during walking. We hypothesized that the hand and foot would become more elevated and the elbow and knee more extended, leading to increased relative ELLs throughout ontogeny. MATERIALS AND METHODS Longitudinal kinematic data were collected on four infant yellow baboons (Papio cynocephalus) as they aged from two to nine months, and again at two to three years. Hand/foot postures, elbow/knee angles, relative fore/hind limb ELLs, and dimensionless velocity were measured for 404 symmetrical walking strides. RESULTS Digitigrade hand and foot postures were preferred at all ages. The elbow extended slightly and the knee flexed slightly with age. Elevated proximal hands, extended elbows, and extended knees were associated with long relative ELLs. For a given age, relative hind limb ELL was longer than relative forelimb ELL. DISCUSSION In the forelimb, digitigrade hand postures and extended elbows function to increase relative ELL at slow walking velocity. Increased forelimb ELL may be an attempt to equalize forelimb and hind limb ELLs in baboons with an absolutely longer hind limb. Pedal digitigrady is not a main contributing factor to hind limb ELL. Results suggest that manual and pedal digitigrady in terrestrial cercopithecoids does not function to increase velocity.

Ontogenetic changes in foot strike pattern and calcaneal loading during walking in young children

The assumption that the morphology of the human calcaneus reflects high and cyclical impact forces at heel strike during adult human walking has never been experimentally tested. Since a walking step with a heel strike is an emergent behavior in children, an ontogenetic study provides a natural experiment to begin testing the relationship between the mechanics of heel strike and calcaneal anatomy. This study examined the ground reaction forces (GRFs) of stepping in children to determine the location of the center of pressure (COP) relative to the calcaneus and the orientation and magnitude of ground reaction forces during foot contact. Three-dimensional kinematic and kinetic data were analyzed for 18 children ranging in age from 11.5 to 43.1 months. Early steppers used a flat foot contact (FFC) and experienced relatively high vertical and resultant GRFs with COP often anterior to the calcaneus. More experienced walkers used an initial heel contact (IHC) in which GRFs were significantly lower but the center of pressure remained under the heel a greater proportion of time. Thus, during FFC the foot experienced higher loading, but the heel itself was relatively wider and the load was distributed more evenly. In IHC walkers load was concentrated on the anterior calcaneus and a narrower heel, suggesting a need for increased calcaneal robusticity during development to mitigate injury. These results provide new insight into foot loading outside of typical mature contact patterns, inform structure-function relationships during development, and illuminate potential causes of heel injury in young walkers.

A user's guide for the quantitative analysis of substrate characteristics and locomotor kinematics in free-ranging primates

OBJECTIVES Laboratory studies have yielded important insights into primate locomotor mechanics. Nevertheless, laboratory studies fail to capture the range of ecological and structural variation encountered by free-ranging primates. We present techniques for collecting kinematic data on wild primates using consumer grade high-speed cameras and demonstrate novel methods for quantifying metric variation in arboreal substrates. MATERIALS AND METHODS These methods were developed and applied to our research examining platyrrhine substrate use and locomotion at the Tiputini Biodiversity Station, Ecuador. Modified GoPro cameras equipped with varifocal zoom lenses provided high-resolution footage (1080 p.; 120 fps) suitable for digitizing gait events. We tested two methods for remotely measuring branch diameter: the parallel laser method and the distance meter photogrammetric method. A forestry-grade laser rangefinder was used to quantify substrate angle and a force gauge was used to measure substrate compliance. We also introduce GaitKeeper, a graphical user interface for MATLAB, designed for coding quadrupedal gait. RESULTS Parallel laser and distance meter methods provided accurate estimations of substrate diameter (percent error: 3.1-4.5%). The laser rangefinder yielded accurate estimations of substrate orientation (mean error = 2.5°). Compliance values varied tremendously among substrates but were largely explained by substrate diameter, substrate length, and distance of measurement point from trunk. On average, larger primates used relatively small substrates and traveled higher in the canopy. DISCUSSION Ultimately, these methods will help researchers identify more precisely how primate gait kinematics respond to the complexity of arboreal habitats, furthering our understanding of the adaptive context in which primate quadrupedalism evolved.