Bone modeling involves the addition of bone material through osteoblast-mediated deposition or the removal of bone material via osteoclast-mediated resorption in response to perceived changes in loads by osteocytes. This process is characterized by the independent occurrence of deposition and resorption, which can take place simultaneously at different locations within the bone due to variations in stress levels across its different regions. The principle of bone functional adaptation states that cortical and trabecular bone tissues will respond to mechanical stimuli by adjusting (i.e., bone modeling) their morphology and architecture to mechanically improve their mechanical function in line with the habitual in vivo loading direction. This principle is relevant to various research areas, such as the development of improved orthopedic implants, preventative medicine for osteopenic elderly patients, and the investigation of locomotion behavior in extinct species. In the present review, the mammalian tibia is used as an example to explore cortical and trabecular bone modeling and to examine its implications for the functional adaptation of bones. Following a short introduction and an exposition on characteristics of mechanical stimuli that influence bone modeling, a detailed critical appraisal of the literature on cortical and trabecular bone modeling and bone functional adaptation is given. By synthesizing key findings from studies involving small mammals (rodents), large mammals, and humans, it is shown that examining both cortical and trabecular bone structures is essential for understanding bone functional adaptation. A combined approach can provide a more comprehensive understanding of this significant physiological phenomenon, as each structure contributes uniquely to the phenomenon.

This study tests if femoral and humeral cross-sectional geometry (CSG) and cross-sectional properties (CSPs) in an ontogenetic series of wild-caught chimpanzees (Pan troglodytes ssp.) reflect locomotor behavior during development. The goal is to clarify the relationship between limb bone structure and locomotor behavior during ontogeny in Pan.
The latex cast method was used to reconstruct cross sections at the midshaft femur and mid-distal humerus. Second moments of area (SMAs) (Ix, Iy, Imax, Imin), which are proportional to bending rigidity about a specified axis, and the polar SMA (J), which is proportional to average bending rigidity, were calculated at section locations. Cross-sectional shape (CSS) was assessed from Ix/Iy and Imax/Imin ratios. Juvenile and adult subsamples were compared.
Juveniles and adults have significantly greater femoral J compared to humeral J. Mean interlimb proportions of J are not significantly different between the groups. There is an overall decreasing trend in diaphyseal circularity between the juvenile phase of development and adulthood, although significant differences are only found in the humerus.
Juvenile chimpanzee locomotion includes forelimb- and hindlimb-biased behaviors. Juveniles and adults preferentially load their hindlimbs relative to their forelimbs. This may indicate similar locomotor behavior, although other explanations including a diversity of hindlimb-biased locomotor behaviors in juveniles cannot be ruled out. Different ontogenetic trends in forelimb and hindlimb CSS are consistent with limb bone CSG reflecting functional adaptation, albeit the complex nature of bone functional adaptation requires cautious interpretations of skeletal functional morphology from biomechanical analyses.

UNASSIGNED: Captivity alters the locomotor behavior of wild artiodactyls and affects the mechanical loading of the calcaneus; however, the resulting adaptive changes in calcaneus morphology have not been sufficiently studied to date. This study aimed to investigate the morphological and mechanical adaptive variations in the calcaneus of Saiga tatarica to understand further the functional adaptation of the calcaneus in wild artiodactyl to captivity.
UNASSIGNED: Paired calcanei from autopsy samples of six captive wild artiodactyls (S. tatarica) and six domesticated artiodactyls (Ovis aries) were divided into skeletally immature and mature groups using X-ray evaluation of growth plate closure. High-resolution microcomputed tomography revealed a calcaneal diaphyseal cross-section. The mechanical and nanomorphological characteristics of the trabecular bone were determined by atomic force microscopy.
UNASSIGNED: The percent cortical bone area (%CA), cortical thickness ratio (CTR), and Young\'s modulus (E) differed between species in the immature groups but not in the mature groups. S. tatarica had significantly higher growth rates for %CA, CTR, and E in the mid-shaft than O. aries (p < 0.05).
UNASSIGNED: The calcaneus morphology of S. tatarica converges with that of domesticated O. aries during ontogeny. These results indicate that the calcaneus of wild artiodactyls can undergo potentially transitional changes during the short-term adaptation to captivity. The above parameters can be preliminarily identified as morphological signs of functional bone adaptation in artiodactyls.

Bone functional adaptation is routinely invoked to interpret skeletal morphology despite ongoing debate regarding the limits of the bone response to mechanical stimuli. The wide variation in human body mass presents an opportunity to explore the relationship between mechanical load and skeletal response in weight-bearing elements. Here, we examine variation in femoral macroscopic morphology as a function of body mass index (BMI), which is used as a metric of load history. A sample of 80 femora (40 female; 40 male) from recent modern humans was selected from the Texas State University Donated Skeletal Collection. Femora were imaged using x-ray computed tomography (voxel size ~0.5 mm), and segmented to produce surface models. Landmark-based geometric morphometric analyses based on the Coherent Point Drift algorithm were conducted to quantify shape. Principal components analyses were used to summarize shape variation, and component scores were regressed on BMI. Within the male sample, increased BMI was associated with a mediolaterally expanded femoral shaft, as well as increased neck-shaft angle and decreased femoral neck anteversion angle. No statistically significant relationships between shape and BMI were found in the female sample. While mechanical stimulus has traditionally been applied to changes in long bong diaphyseal shape it appears that bone functional adaptation may also result in fundamental changes in the shape of skeletal elements.

We propose a variational approach that employs a generalized principle of virtual work to estimate both the mechanical response and the changes in living bone tissue during the remodeling process. This approach provides an explanation for the adaptive regulation of the bone substructure in the context of orthotropic material symmetry. We specifically focus upon the crucial gradual adjustment of bone tissue as a structural material that adapts its mechanical features, such as materials stiffnesses and microstructure, in response to the evolving loading conditions. We postulate that the evolution process relies on a feedback mechanism involving multiple stimulus signals. The mechanical and remodeling behavior of bone tissue is clearly a complex process that is difficult to describe within the framework of classical continuum theories. For this reason, a generalized continuum elastic theory is employed as a proper mathematical context for an adequate description of the examined phenomenon. To simplify the investigation, we considered a two-dimensional problem. Numerical simulations have been performed to illustrate bone evolution in a few significant cases: the bending of a rectangular cantilever plate and a three-point flexure test. The results are encouraging because they can replicate the optimization process observed in bone remodeling. The proposed model provides a likely distribution of stiffnesses and accurately represents the arrangement of trabeculae macroscopically described by the orthotropic symmetry directions, as supported by experimental evidence from the trajectorial theory.

The addition of information regarding obesity status to the forensic anthropological biological profile could significantly contribute to the identification of human skeletal remains since over 40% of the U.S. adult population is currently obese. This study examines the differences in talar shape and trabecular bone structure between obese and non-obese individuals. A sample of 20 obese and 20 non-obese divided evenly by sex was selected from the Texas State University Donated Skeletal Collection. Tali were imaged using x-ray computed tomography (voxel size: 28-38.7 μm). Image stacks were processed to produce binary images as well as trabecular thickness and spacing maps. Landmark-based geometric morphometric analyses were conducted to quantify shape variation. Shape coordinates were used to locate 100 geometrically homologous volumes of interest within each talus. Bone volume fraction, trabecular thickness, and trabecular spacing were extracted at each volume of interest. Within each sex, a one-way ANCOVA was used to determine if significant differences exist between obese and non-obese individuals in trabecular bone after controlling for age. The size of the talus as well as subtle aspects of shape were found to distinguish the sexes. The results further indicate that bone volume fraction significantly differs between obese and non-obese males. In females, bone volume fraction is correlated with age but does not differ between obese and non-obese. The study demonstrates that bone microstructure is a promising approach to estimating body mass or body mass index category but age effects diminish the potential for the talus to be used alone.

BACKGROUND: There is a genetic component to the minimum effective strain (MES)-a threshold which determines when bone will adapt to function-which suggests ancestry should play a role in bone (re)modelling. Further elucidating this is difficult in living human populations because of the high global genetic admixture. We examined femora from an anthropological skeletal assemblage (Mán Bạc, Vietnam) representing distinct ancestral groups. We tested whether femur morphological and histological markers of modelling and remodelling differed between ancestries despite their similar lifestyles.
METHODS: Static histomorphometry data collected from subperiosteal cortical bone of the femoral midshaft, and gross morphometric measures of femur robusticity, were studied in 17 individuals from the Mán Bạc collection dated to 1906-1523 cal. BC. This assemblage represents agricultural migrants with affinity to East Asian groups, who integrated with the local hunter-gatherers with affinity to Australo-Papuan groups during the mid-Holocene. Femur robusticity and histology data were compared between groups of \'Migrant\' (n = 8), \'Admixed\' (n = 4), and \'Local\' (n = 5).
RESULTS: Local individuals had more robust femoral diaphyses with greater secondary osteon densities, and relatively large secondary osteon and Haversian canal parameters than the migrants. The Migrant group showed gracile femoral shafts with the least dense bone made up of small secondary osteons and Haversian canals. The Admixed individuals fell between the Migrant and Local categories in terms of their femoral data. However, we also found that measures of how densely bone is remodelled per unit area were in a tight range across all three ancestries.
CONCLUSIONS: Bone modelling and remodelling markers varied with ancestral histories in our sample. This suggests that there is an ancestry related predisposition to bone optimising its metabolic expenditure likely in relation to the MES. Our results stress the need to incorporate population genetic history into hierarchical bone analyses. Understanding ancestry effects on bone morphology has implications for interpreting biomechanical loading history in past and modern human populations.

In 1994, Hunt published the \'postural feeding hypothesis\'-a seminal paper on the origins of hominin bipedalism-founded on the detailed study of chimpanzee positional behavior and the functional inferences derived from the upper and lower limb morphology of the Australopithecus afarensis A.L. 288-1 partial skeleton. Hunt proposed a model for understanding the potential selective pressures on hominins, made robust, testable predictions based on Au. afarensis functional morphology, and presented a hypothesis that aimed to explain the dual functional signals of the Au. afarensis and, more generally, early hominin postcranium. Here we synthesize what we have learned about Au. afarensis functional morphology and the dual functional signals of two new australopith discoveries with relatively complete skeletons (Australopithecus sediba and StW 573 \'Australopithecus prometheus\'). We follow this with a discussion of three research approaches that have been developed for the purpose of drawing behavioral inferences in early hominins: (1) developments in the study of extant apes as models for understanding hominin origins; (2) novel and continued developments to quantify bipedal gait and locomotor economy in extant primates to infer the locomotor costs from the anatomy of fossil taxa; and (3) novel developments in the study of internal bone structure to extract functional signals from fossil remains. In conclusion of this review, we discuss some of the inherent challenges of the approaches and methodologies adopted to reconstruct the locomotor modes and behavioral repertoires in extinct primate taxa, and notably the assessment of habitual terrestrial bipedalism in early hominins.

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.

African apes engage in a distinct form of locomotion called knuckle-walking, but there is much ambiguity as to when and how this locomotor behavior evolved. This study aims to elucidate potential differences in knuckle-walking elbow posture and loading in African apes through the study of trabecular bone. Using a whole-epiphysis approach, we quantified variation in the trabecular structure of the distal humerus of chimpanzees, western lowland gorillas, and mountain gorillas in comparison to orang-utans, siamangs, and a sample of Old and New World monkeys. Results demonstrate differences in the distribution of trabecular bone within the distal humerus that are consistent across taxa that habitually use a flexed-elbow posture in comparison to those that use an extended elbow during locomotion. Western lowland gorillas show an extended-elbow pattern consistent with the straight forelimb position during knuckle-walking, whereas chimpanzees show a flexed-elbow pattern. Unexpectedly, mountain gorillas show an intermediate pattern between their western counterparts and chimpanzees. The differences found in elbow joint posture between chimpanzees and gorillas, and between gorilla species, point to diversification in the knuckle-walking biomechanical strategies among African apes, which has implications in the debate regarding the locomotor behavior from which human bipedalism arose.