Morphological and evolutionary insights into the keystone element of the human foot's medial longitudinal arch.

The evolution of the medial longitudinal arch (MLA) is one of the most impactful adaptations in the hominin foot that emerged with bipedalism. When and how it evolved in the human lineage is still unresolved. Complicating the issue, clinical definitions of flatfoot in living Homo sapiens have not reached a consensus. Here we digitally investigate the navicular morphology of H. sapiens (living, archaeological, and fossil), great apes, and fossil hominins and its correlation with the MLA. A distinctive navicular shape characterises living H. sapiens with adult acquired flexible flatfoot, while the congenital flexible flatfoot exhibits a 'normal' navicular shape. All H. sapiens groups differentiate from great apes independently from variations in the MLA, likely because of bipedalism. Most australopith, H. naledi, and H. floresiensis navicular shapes are closer to those of great apes, which is inconsistent with a human-like MLA and instead might suggest a certain degree of arboreality. Navicular shape of OH 8 and fossil H. sapiens falls within the normal living H. sapiens spectrum of variation of the MLA (including congenital flexible flatfoot and individuals with a well-developed MLA). At the same time, H. neanderthalensis seem to be characterised by a different expression of the MLA.

Trabecular bone ontogeny tracks neural development and life history among humans and non-human primates.

Trabecular bone-the spongy bone inside marrow cavities-adapts to its mechanical environment during growth and development. Trabecular structure can therefore be interpreted as a functional record of locomotor behavior in extinct vertebrates. In this paper, we expand upon traditional links between form and function by situating ontogenetic trajectories of trabecular bone in four primate species into the broader developmental context of neural development, locomotor control, and ultimately life history. Our aim is to show that trabecular bone structure provides insights into ontogenetic variation in locomotor loading conditions as the product of interactions between increases in body mass and neuromuscular maturation. Our results demonstrate that age-related changes in trabecular bone volume fraction (BV/TV) are strongly and linearly associated with ontogenetic changes in locomotor kinetics. Age-related variation in locomotor kinetics and BV/TV is in turn strongly associated with brain and body size growth in all species. These results imply that age-related variation in BV/TV is a strong proxy for both locomotor kinetics and neuromuscular maturation. Finally, we show that distinct changes in the slope of age-related variation in bone volume fraction correspond to the age of the onset of locomotion and the age of locomotor maturity. Our findings compliment previous studies linking bone development to locomotor mechanics by providing a fundamental link to brain development and life history. This implies that trabecular structure of fossil subadults can be a proxy for the rate of neuromuscular maturation and major life history events like locomotor onset and the achievement of adult-like locomotor repertoires.

Evolutionary loss of complexity in human vocal anatomy as an adaptation for speech.

Human speech production obeys the same acoustic principles as vocal production in other animals but has distinctive features: A stable vocal source is filtered by rapidly changing formant frequencies. To understand speech evolution, we examined a wide range of primates, combining observations of phonation with mathematical modeling. We found that source stability relies upon simplifications in laryngeal anatomy, specifically the loss of air sacs and vocal membranes. We conclude that the evolutionary loss of vocal membranes allows human speech to mostly avoid the spontaneous nonlinear phenomena and acoustic chaos common in other primate vocalizations. This loss allows our larynx to produce stable, harmonic-rich phonation, ideally highlighting formant changes that convey most phonetic information. Paradoxically, the increased complexity of human spoken language thus followed simplification of our laryngeal anatomy.

Growth and development of trabecular structure in the calcaneus of Japanese macaques (Macaca fuscata) reflects locomotor behavior, life history, and neuromuscular development.

Bone structure dynamically adapts to its mechanical environment throughout ontogeny by altering the structure of trabecular bone, the three-dimensional mesh-like structure found underneath joint surfaces. Trabecular structure, then, can provide a record of variation in loading directions and magnitude; and in ontogenetic samples, it can potentially be used to track developmental shifts in limb posture. We aim to broaden the analysis of trabecular bone ontogeny by incorporating interactions between ontogenetic variation in locomotor repertoire, neuromuscular maturation, and life history. We examine the associations between these variables and age-related variation in trabecular structure in the calcaneus of Japanese macaques (Macaca fuscata). We used high-resolution micro-computed tomography scanning to image the calcaneus in a cross-sectional sample of 34 juvenile M. fuscata aged between 0 and 7 years old at the Primate Research Institute, Japan. We calculated whole bone averages of standard trabecular properties and generated whole-bone morphometric maps of bone volume fraction and Young's modulus. Trabecular structure becomes increasingly heterogeneous in older individuals. Bone volume fraction (BV/total volume [TV]) decreases during the first month of life and increases afterward, coinciding with the onset of independent locomotion in M. fuscata. At birth, primary Young's modulus is oriented orthogonal to the ossification center, but after locomotor onset bone structure becomes stiffest in the direction of joint surfaces and muscle attachments. Age-related variation in bone volume fraction is best predicted by an interaction between the estimated percentage of adult brain size, body mass, and locomotor onset. To explain our findings, we propose a model where interactions between age-related increases in body weight and maturation of the neuromuscular system alter the loading environment of the calcaneus, to which the internal trabecular structure dynamically adapts. This model cannot be directly tested based on our cross-sectional data. However, confirmation of the model by longitudinal experiments and in multiple species would show that trabecular structure can be used both to infer behavior from fossil morphology and serve as a valuable proxy for neuromuscular maturation and life history events like locomotor onset and the achievement of an adult-like gait. This approach could significantly expand our knowledge of the biology and behavior of fossil species.

Unique foot posture in Neanderthals reflects their body mass and high mechanical stress.

Neanderthal foot bone proportions and morphology are mostly indistinguishable from those of Homo sapiens, with the exception of several distinct Neanderthal features in the talus. The biomechanical implications of these distinct talar features remain contentious, fueling debate around the adaptive meaning of this distinctiveness. With the aim of clarifying this controversy, we test phylogenetic and behavioral factors as possible contributors, comparing tali of 10 Neanderthals and 81 H. sapiens (Upper Paleolithic and Holocene hunter-gatherers, agriculturalists, and postindustrial group) along with the Clark Howell talus (Omo, Ethiopia). Variation in external talar structures was assessed through geometric morphometric methods, while bone volume fraction and degree of anisotropy were quantified in a subsample (n = 45). Finally, covariation between point clouds of site-specific trabecular variables and surface landmark coordinates was assessed. Our results show that although Neanderthal talar external and internal morphologies were distinct from those of H. sapiens groups, shape did not significantly covary with either bone volume fraction or degree of anisotropy, suggesting limited covariation between external and internal talar structures. Neanderthal external talar morphology reflects ancestral retentions, along with various adaptations to high levels of mobility correlated to their presumably unshod hunter-gatherer lifestyle. This pairs with their high site-specific trabecular bone volume fraction and anisotropy, suggesting intense and consistently oriented locomotor loading, respectively. Relative to H.sapiens, Neanderthals exhibit differences in the talocrural joint that are potentially attributable to cultural and locomotor behavior dissimilarity, a talonavicular joint that mixes ancestral and functional traits, and a derived subtalar joint that suggests a predisposition for a pronated foot during stance phase. Overall, Neanderthal talar variation is attributable to mobility strategy and phylogenesis, while H. sapiens talar variation results from the same factors plus footwear. Our results suggest that greater Neanderthal body mass and/or higher mechanical stress uniquely led to their habitually pronated foot posture.

Using point clouds to investigate the relationship between trabecular bone phenotype and behavior: An example utilizing the human calcaneus.

OBJECTIVES: The objective of this study is to demonstrate a new method for analyzing trabecular bone volume fraction and degree of anisotropy in three dimensions. METHODS: We use a combination of automatic mesh registration, point-cloud correspondence registration, and P-value corrected univariate statistical tests to compare bone volume fraction and degree of anisotropy on a point by point basis across the entire calcaneus of two human groups with different subsistence strategies. RESULTS: We found that the patterns of high and low bone volume fraction and degree of anisotropy distribution between the Black Earth (hunter-gatherers) and Norris Farms (mixed-strategy agriculturalists) are very similar, but differ in magnitude. The hunter-gatherers exhibit higher levels of bone volume fraction and less anisotropic trabecular bone organization. Additionally, patterns of bone volume fraction and degree of anisotropy in the calcaneus correspond well with biomechanical expectations of relative forces experienced during walking and running. CONCLUSIONS: We conclude that comparing site-specific, localized differences in trabecular bone variables such as bone volume fraction and degree of anisotropy in three-dimensions is a powerful analytical tool. This method makes it possible to determine where similarities and differences between groups are located within the whole skeletal element of interest. The visualization of multiple variables also provides a way for researchers to see how the trabecular bone variables interact within the morphology, and allows for a more nuanced understanding of how they relate to one another and the broader mechanical environment.

Combinations of trabecular and cortical bone properties distinguish various loading modalities between athletes and controls.

OBJECTIVES: Variation in trabecular and cortical bone properties is often used to infer habitual behavior in the past. However, the structures of both types of bone are rarely considered together and may even contradict each other in functional interpretations. We examine trabecular and cortical bone properties in various athletes and sedentary controls to clarify the associations between combinations of cortical and trabecular bone properties and various loading modalities. MATERIALS AND METHODS: We compare trabecular and cortical bone properties using peripheral quantitative computed tomography scans of the tibia between groups of 83 male athletes (running, hockey, swimming, cricket) and sedentary controls using Bayesian multilevel models. We quantify midshaft cortical bone rigidity and area (J, CA), midshaft shape index (Imax/Imin), and mean trabecular bone mineral density (BMD) in the distal tibia. RESULTS: All groups show unique combinations of biomechanical properties. Cortical bone rigidity is high in sports that involve impact loading (cricket, running, hockey) and low in nonimpact loaded swimmers and controls. Runners have more anteroposteriorly elliptical midshafts compared to other groups. Interestingly, all athletes have greater trabecular BMD compared to controls, but do not differ credibly among each other. DISCUSSION: Results suggest that cortical midshaft hypertrophy is associated with impact loading while trabecular BMD is positively associated with both impact and nonimpact loading. Midshaft shape is associated with directionality of loading. Individuals from the different categories overlap substantially, but group means differ credibly, suggesting that nuanced group-level inferences of habitual behavior are possible when combinations of trabecular and cortical bone are analyzed.

Automated resolution independent method for comparing in vivo and dry trabecular bone.

OBJECTIVES: Variation in human trabecular bone morphology can be linked to habitual behavior, but it is difficult to investigate in vivo due to the radiation required at high resolution. Consequently, functional interpretations of trabecular morphology remain inferential. Here we introduce a method to link low- and high-resolution CT data from dry and fresh bone, enabling bone functional adaptation to be studied in vivo and results compared to the fossil and archaeological record. MATERIALS AND METHODS: We examine 51 human dry bone distal tibiae from Nile Valley and UK and two pig tibiae containing soft tissues. We compare low-resolution peripheral quantitative computed tomography (pQCT) parameters and high-resolution micro CT (µCT) in homologous single slices at 4% bone length and compare results to our novel Bone Ratio Predictor (BRP) method. RESULTS: Regression slopes between linear attenuation coefficients of low-resolution pQCT images and bone area/total area (BA/TA) of high-resolution µCT scans differ substantially between geographical subsamples, presumably due to diagenesis. BRP accurately predicts BA/TA (R2 = .97) and eliminates the geographic clustering. BRP accurately estimates BA/TA in pigs containing soft tissues (R2 = 0.98) without requiring knowledge of true density or phantom calibration of the scans. DISCUSSION: BRP allows automated comparison of image data from different image modalities (pQCT, µCT) using different energy settings, in archeological bone and wet specimens. The method enables low-resolution data generated in vivo to be compared with the fossil and archaeological record. Such experimental approaches would substantially improve behavioral inferences based on trabecular bone microstructure.

Intrapopulation variation in lower limb trabecular architecture.

OBJECTIVES: Trabecular structure is frequently used to differentiate between highly divergent mechanical environments. Less is known regarding the response of the structural properties to more subtle behavioral differences, as the range of intrapopulation variation in trabecular architecture is rarely studied. Examining the extent to which lower limb trabecular architecture varies when inferred mobility levels and environment are consistent between groups within a relatively homogenous population may aid in the contextualization of interpopulation differences, improve detectability of sexual dimorphism in trabecular structure, and improve our understanding of trabecular bone functional adaptation. MATERIALS AND METHODS: The study sample was composed of adult individuals from three high/late medieval cemeteries from Cambridge (10th-16th c.), a hospital (n = 57), a parish cemetery (n = 44) and a friary (n = 14). Trabecular architecture was quantified in the epiphyses of the femur and tibia, using high resolution computed tomography. RESULTS: The parish individuals had the lowest bone volume fraction and trabecular thickness in most regions. Multiple sex differences were observed, but the patterns were not consistent across volumes of interest. DISCUSSION: Differences between the three groups highlight the great variability of trabecular bone architecture, even within a single sedentary population. This indicates that trabecular bone may be used in interpreting subtle behavioral differences, and suggests that multiple archaeological sites need to be studied to characterize structural variation on a population level. Variation in sex and group differences across anatomical locations further demonstrates the site-specificity in trabecular bone functional adaptation, which might explain why little consistent sexual dimorphism has been reported previously.

Baby steps towards linking calcaneal trabecular bone ontogeny and the development of bipedal human gait.

Trabecular bone structure in adulthood is a product of a process of modelling during ontogeny and remodelling throughout life. Insight into ontogeny is essential to understand the functional significance of trabecular bone structural variation observed in adults. The complex shape and loading of the human calcaneus provides a natural experiment to test the relationship between trabecular morphology and locomotor development. We investigated the relationship between calcaneal trabecular bone structure and predicted changes in loading related to development of gait and body size in growing children. We sampled three main trabecular regions of the calcanei using micro-computed tomography scans of 35 individuals aged between neonate to adult from the Norris Farms #36 site (1300 AD, USA) and from Cambridge (1200-1500 AD, UK). Trabecular properties were calculated in volumes of interest placed beneath the calcaneocuboid joint, plantar ligaments, and posterior talar facet. At birth, thin trabecular struts are arranged in a dense and relatively isotropic structure. Bone volume fraction strongly decreases in the first year of life, whereas anisotropy and mean trabecular thickness increase. Dorsal compressive trabecular bands appear around the onset of bipedal walking, although plantar tensile bands develop prior to predicted propulsive toe-off. Bone volume fraction and anisotropy increase until the age of 8, when gait has largely matured. Connectivity density gradually reduces, whereas trabeculae gradually thicken from birth until adulthood. This study demonstrates that three different regions of the calcaneus develop into distinct adult morphologies through varying developmental trajectories. These results are similar to previous reports of ontogeny in human long bones and are suggestive of a relationship between the mechanical environment and trabecular bone architecture in the human calcaneus during growth. However, controlled experiments combined with more detailed biomechanical models of gait maturation are necessary to establish skeletal markers linking growth to loading. This has the potential to be a novel source of information for understanding loading levels, activity patterns, and perhaps life history in the fossil record.

Trabecular bone structure scales allometrically in the foot of four human groups.

The human foot is highly derived relative to that of other hominoids and therefore a topic of intense research in paleoanthropology. While trabecular bone is thought to be highly plastic in response to habitual behavior, knowledge of how trabecular structure scale with body size is essential for making functional inferences from trabecular bone morphology. Trabecular bone properties scale with negative allometry in interspecific studies that includes a wide range of body size; however, intraspecific scaling patterns often differ from interspecific trends. In this paper we examine patterns of trabecular bone scaling in the calcaneus, talus, and first metatarsal of four human populations with different subsistence strategies and associated levels of terrestrial mobility. We report Bayesian linear regressions between the natural logarithms of femoral head diameter and five standard trabecular variables calculated in five spherical volumes of interest. We additionally report regressions on population-specific z-scores of femoral head diameter and trabecular variables as a way of placing the four populations on a common scale. Results show that with increasing body size there is no change in bone volume fraction (BV/TV) and trabecular thickness (Tb.Th), a slight increase in trabecular spacing (Tb.Sp), and a sharp decrease in connectivity density (Conn.D). Degree of anisotropy was found to scale with positive allometry in the calcaneus, negative allometry in the talar trochlea, and shows no relationship with femoral head diameter in the talar and first metatarsal heads. These results show that scaling of the degree of anisotropy can vary substantially within and between bones. Degree of anisotropy is often used as a proxy for directionality in joint loading when interpreting variation in trabecular structures of fossils and extant primates. Body size should therefore be an important consideration when trabecular bone structure is used to interpret function from fossil morphology.

Complex variation of trabecular bone structure in the proximal humerus and femur of five modern human populations.

OBJECTIVE: This project investigates trabecular bone structural variation in the proximal humerus and femur of hunter-gatherer, mixed-strategy agricultural, medieval, and human groups to address three questions: (a) What is the extent of trabecular bone structural variation in the humerus and femur between populations with different inferred activity levels? (b) How does variation in the proximal humerus relate to variation in the proximal femur? (c) Are trabecular bone microstructural variables sexually dimorphic? METHODS: The proximal humerus and femur of 73 adults from five human groups with distinct subsistence strategies were scanned using a micro-computed tomography system. Centralized volumes of interest within the humeral and femoral heads were extracted and analyzed to quantify bone volume fraction, trabecular thickness, trabecular separation, connectivity density, degree of anisotropy, and bone surface density. RESULTS: In the humerus and femur, groups with the highest inferred activity levels have higher bone volume fraction and trabecular thickness, and lower bone surface density than those with lower inferred activity levels. However, the humeral pattern does not exactly mirror that of the femur, which demonstrates a steeper gradient of difference between subsistence groups. No significant differences were identified in trabecular separation. No consistent patterns of sexual dimorphism were present in the humerus or femur. CONCLUSIONS: Reduced skeletal robusticity of proximal humeral and femoral trabecular bone corresponds with reduced activity level inferred from subsistence strategy. However, human trabecular bone structural variation is complex and future work should explore how other factors (diet, climate, genetics, disease load, etc.), in addition to activity, influence bone structural variation.

Trabecular bone functional adaptation and sexual dimorphism in the human foot.

OBJECTIVES: Trabecular bone adapts to the strains placed upon the skeleton during life. Anthropological research has largely focused on linking variation in primate trabecular bone to locomotor mode, to provide a context for interpreting fossil morphology. However, intraspecific variation and its underlying mechanisms are still poorly understood. Trabecular bone is influenced by a variety of factors including body mass, age, diet, temperature, genetics, sex, and behavior. Before trabecular structure can be used to infer habitual behavior in the past, the effects of these factors need to be understood. In this article, we examine variation in trabecular structure in the human foot in four archaeological groups in relation to inferred levels of terrestrial mobility and sex. MATERIALS AND METHODS: We use high-resolution µCT scanning to examine variation in trabecular structure in the human calcaneus, talus, and first metatarsal in two relatively mobile and two relatively sedentary archaeological groups. RESULTS: The four population samples show similar patterns of trabecular variation throughout the foot, influenced by mechanical loading. Greater inferred terrestrial mobility is associated with greater bone volume fraction and thicker, more widely spaced, and less interconnected trabeculae. However, contrary to diaphyseal rigidity, only limited sexual dimorphism was found in trabecular structure. DISCUSSION: This work demonstrates that trabecular bone may serve as a useful proxy of habitual behavior in the fossil and archaeological record when other factors are carefully considered. However, the mechanisms underlying sexual dimorphism are not well understood. As such, inferring sex differences in habitual behavior is currently challenging.

Trabecular bone structural variation throughout the human lower limb.

Trabecular bone is responsive to mechanical loading, and thus may be a useful tool for interpreting past behaviour from fossil morphology. However, the ability to meaningfully interpret variation in archaeological and hominin trabecular morphology depends on the extent to which trabecular bone properties are integrated throughout the postcranium or are locally variable in response to joint specific loading. We investigate both of these factors by comparing trabecular bone throughout the lower limb between a group of highly mobile foragers and two groups of sedentary agriculturalists. Trabecular bone structure is quantified in four volumes of interest placed within the proximal and distal joints of the femur and tibia. We determine how trabecular structures correspond to inferred behavioural differences between populations and whether the patterns are consistent throughout the limb. A significant correlation was found between inferred mobility level and trabecular bone structure in all volumes of interest along the lower limb. The greater terrestrial mobility of foragers is associated with higher bone volume fraction, and thicker and fewer trabeculae (lower connectivity density). In all populations, bone volume fraction decreases while anisotropy increases proximodistally throughout the lower limb. This observation mirrors reductions in cortical bone mass resulting from proximodistal limb tapering. The reduction in strength associated with reduced bone volume fraction may be compensated for by the increased anisotropy in the distal tibia. A similar pattern of trabecular structure is found throughout the lower limb in all populations, upon which a signal of terrestrial mobility appears to be superimposed. These results support the validity of using lower limb trabecular bone microstructure to reconstruct terrestrial mobility levels from the archaeological and fossil records. The results further indicate that care should be taken to appreciate variation resulting from differences in habitual activity when inferring behaviour from the trabecular structure of hominin fossils through comparisons with modern humans.