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.The research leading to these results has received funding from the European Research Council under the European Union’s Seventh Framework Programme (FP/2007-2013) / ERC Grant Agreement n.617627 (to JTS), the Arts and Humanities Research Council Doctoral Training Programme, AH/14/Archaeology/3 (to JPPS), and National Science Foundation Grant BCS-0617097 (to TMR).This is the author accepted manuscript. It is currently under an indefinite embargo pending publication by Elsevier

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

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.</jats:p

Skeletal indicators of developmental changes in arboreality and locomotor maturation in extant apes and their relevance to hominin paleobiology

Peer reviewed: TrueAcknowledgements: I am grateful to Dr. Rachel Jennings of the Powell Cotton Museum for facilitating access and loans of the skeletal sample. I am also grateful to Prof. Jay Stock of Western University, CA, whose RCUK/BBSRC grant number BB/R01292X/1 funded the CT scanning of the skeletal sample. This project has received funding from the European Union’s Horizon 2021 research and innovation programme under the Marie Skłodowska Curie grant agreement number 101066276. This work used the Dutch national e-infrastructure with the support of the SURF Cooperative using grant no. EINF-5670.IntroductionModern humans are the only fully terrestrial ape. All other apes are partially arboreal, particularly as infants and juveniles. Precocial locomotor development, high frequency of arboreal locomotion in early ontogeny, and increased terrestriality throughout development are ubiquitous amongst the hominines and likely represent the ancestral state. The role of climbing in hominin evolution has been debated for decades, but if hominins climbed regularly then subadults likely relied on it most frequently. Investigating the role of climbing throughout hominin evolution requires reliable developmentally plastic traits that are responsive to locomotor loading and can be identified in the fossil record. Chimpanzees and gorillas provide a natural experiment to examine the relationship between age-related variation locomotor activities and bone structure. Chimpanzees and gorillas are most arboreal during infancy and become more terrestrial throughout development. Gorillas are comparatively more terrestrial and transition to predominantly terrestrial locomotion at an earlier age. This paper has two main objectives. First, to examine if interspecific differences in the rate of locomotor development is reflected in bone structure. Second, to determine if ontogenetic reductions in the frequency of arboreal locomotion correspond to age-related variation in bone structure.MethodsThe humerus, tibia, calcaneus, and seventh cervical vertebrae of an ontogenetic series of gorillas and chimpanzees from the Powell Cotton Museum (n = 71) were uCT scanned. Trabecular, cortical, and total bone volume fraction (BV/TV) were calculated in developmentally homologous regions of interest.ResultsBV/TV scales with positive allometry throughout ontogeny. The achievement of adult-like locomotor behaviour can be identified by a significant change in the slope of Total.BV/TV with age. Younger, more arboreal individuals have relatively greater upper limb Total.BV/TV relative to the neck and lower limb than older, more terrestrial individuals in gorillas and chimpanzees. More arboreal chimpanzees have relatively more Total.BV/TV in the upper limb relative to the lower limb and neck.DiscussionThe correspondence between developmental trajectories of BV/TV and locomotor ontogeny in extant apes suggests that analyses of hominin skeletal ontogeny can provide new insights into the evolution of two characteristic human traits: our slow rate of maturation and the evolution of fully terrestrial bipedalism.</jats:sec

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 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.Funding: RCUK/BBSRC BB/R01292X/1, travel to the PRI was facilitated by a grant from the DM McDonald Fund, University of Cambridg

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

A Habitual Activity in Pre-industrial Rural and Urban Dutch Populations: A Study of Lower Limb Cross-sectional Geometry

This study combines historical data and the principles of bone functional adaptation to examine variation in terrestrial mobility in men and women from pre-industrial urban (Alkmaar 7M, 9F) and rural (Klaaskinderk- erke 12M, 8F; Middenbeemster 21M, 22F) Dutch populations. Cross-sectional properties of the femoral and tib- ial midshaſt are determined to investigate variation in lower limb mechanical loading. All populations had comparable age ranges. Rural Middenbeemster males had significantly more elliptically shaped tibiae compared to the other populations. Rural males from Klaaskinderkerke had significantly greater femoral cross-sectional area and torsional rigidity compared to females. In the tibia, the males from both rural populations had greater torsional rigidity and cross-sectional area compared to females. In the rural Middenbeemster population the males also had significantly more elliptically shaped tibiae compared to females. While no sexual dimorphism was found in the urban Alkmaar, significantly greater variation in lower limb cross-sectional properties was found for both males and females relative to the rural populations. These results conform to predictions based on the historical literature of greater lower limb loading in rural males compared to females as well as a greater variety of tasks performed in urban environments. The lack of significant differences in lower limb torsional rigidity or shape between populations in either sex suggests that rural life was not necessarily more physically strenuous than urban life in pre-industrial Dutch populations. However, variation in sexual dimorphism sug- gests that labor between males and females was differently organized in the rural and urban samples