The postcranial skeleton of modern Homo sapiens is relatively gracile compared with other hominoids and earlier hominins. This gracility predisposes contemporary humans to osteoporosis and increased fracture risk. Explanations for this gracility include reduced levels of physical activity, the dissipation of load through enlarged joint surfaces, and selection for systemic physiological characteristics that differentiate modern humans from other primates. This study considered the skeletal remains of four behaviorally diverse recent human populations and a large sample of extant primates to assess variation in trabecular bone structure in the human hip joint. Proximal femur trabecular bone structure was quantified from microCT data for 229 individuals from 31 extant primate taxa and 59 individuals from four distinct archaeological human populations representing sedentary agriculturalists and mobile foragers. Analyses of mass-corrected trabecular bone variables reveal that the forager populations had significantly higher bone volume fraction, thicker trabeculae, and consequently lower relative bone surface area compared with the two agriculturalist groups. There were no significant differences between the agriculturalist and forager populations for trabecular spacing, number, or degree of anisotropy. These results reveal a correspondence between human behavior and bone structure in the proximal femur, indicating that more highly mobile human populations have trabecular bone structure similar to what would be expected for wild nonhuman primates of the same body mass. These results strongly emphasize the importance of physical activity and exercise for bone health and the attenuation of age-related bone loss. trabecular bone | gracilization | human evolution | biomechanics | mobility C ompared with other hominoids and extinct hominin species, more recent humans possess relatively gracile postcranial skeletons (1-9). One of the consequences of this gracility in contemporary humans is an increased fracture risk associated with age-related bone loss and osteoporosis [hip fractures alone are projected to reach 6.26 million per year globally by 2050 (10)] (11-15). The etiology of this relative gracility remains uncertain, and this uncertainty hinders the development of strategies for mitigating fracture risk and morbidity. The progressive gracilization of the Homo postcranial skeleton was originally detected in cortical bone structure (1, 2), but has now been demonstrated in the trabecular bone microstructure of joints (12,14,(16)(17)(18)(19), where osteoporotic fracture risk is highest (20). Most notably, in an analysis of thoracic vertebral bodies, Cotter et al. (12) found that young adult humans have significantly lower trabecular bone volume fraction (BV/TV) and thinner vertebral shells than similarly sized apes. Griffin et al. (16) also found significantly lower BV/TV in the human first and second metatarsal heads compared with hominoid primates. The results of these studies are corroborated by work on the hominoid...

Variation in upper limb long bone cross-sectional properties may reflect a phenotypically plastic response to habitual loading patterns. Structural differences between limb bones have often been used to infer past behavior from hominin remains; however, few studies have examined direct relationships between behavioral differences and bone structure in humans. To help address this, cross-sectional images (50% length) of the humeri and ulnae of university varsity-level swimmers, cricketers, and controls were captured using peripheral quantitative computed tomography. High levels of humeral robusticity were found in the dominant arms of cricketers, and bilaterally among swimmers, whereas the most gracile humeri were found in both arms of controls, and the nondominant arms of cricketers. In addition, the dominant humeri of cricketers were more circular than controls. The highest levels of ulnar robusticity were also found in the dominant arm of cricketers, and bilaterally amongst swimmers. Bilateral asymmetry in humeral rigidity among cricketers was greater than swimmers and controls, while asymmetry for ulnar rigidity was greater in cricketers than controls. The results suggest that more mechanically loaded upper limb elements--unilaterally or bilaterally--are strengthened relative to less mechanically loaded elements, and that differences in mechanical loading may have a more significant effect on proximal compared to distal limb segments. The more circular humerus in the dominant arm in cricketers may be an adaptation to torsional strain associated with throwing activities. The reported correspondence between habitual activity patterns and upper limb diaphyseal properties may inform future behavioral interpretations involving hominin skeletal remains.

Mobility patterns affect the loads placed on the lower limbs during locomotion and may influence variation in lower limb diaphyseal robusticity and shape. This relationship commonly forms the basis for inferring mobility patterns from hominin fossil and skeletal remains. This study assesses the correspondence between athletic histories, varying by loading intensity, repetition and directionality, measured using a recall questionnaire, and peripheral quantitative computed tomography-derived measurements of tibial diaphysis rigidity and shape. Participants included male university varsity cross-country runners (n = 15), field hockey players (n = 15), and controls (n = 20) [mean age: 22.1 (SD +/- 2.6) years]. Measurements of tibial rigidity (including J, %CA, Imax, Imin, and average cortical thickness) of both runners and field hockey players were greater than controls (P < or = 0.05). Differences in tibial shape (Imax/Imin, P < or = 0.05) between runners and hockey players reflect pronounced maximum plane (Imax) rigidity in runners, and more symmetrical hypertrophy (Imax, Imin) among hockey players. This corresponds with the generally unidirectional locomotor patterns of runners, and the multidirectional patterns of hockey players. These results support the relationship between mobility and tibial diaphysis morphology as it is generally interpreted in the anthropological literature, with greater levels of mobility associated with increased diaphyseal robusticity and shape variation. Although exercise intensity may be the primary influence on these properties, the repetitiveness of the activity also deserves consideration. In conclusion, bone morphological patterns can reflect habitual behaviors, with adaptation to locomotor activities likely contributing to variation in tibial rigidity and shape properties in archaeological and fossil samples.

Measures of diaphyseal robusticity have commonly been used to investigate differences in bone strength related to body size, behavior, climate, and other factors. The most common methods of quantifying robusticity involve external diameters, or cross-sectional geometry. The data derived from these different methods are often used to address similar research questions, yet the compatibility of the resulting data has not been thoroughly tested. This study provides the first systematic comparison of externally derived measures of postcranial robusticity, with those based upon cross-sectional geometry. It includes sections taken throughout the skeleton, comparisons of prediction errors associated with different measurements, and analysis of the implications of different methods of body size standardization on the prediction of relative bone strength. While the results show reasonable correlations between diaphyseal diameters and strengths derived from cross-sectional geometry, considerable prediction errors are found in many cases. A new approach to externally based quantification of diaphyseal robusticity based upon moulding of sub-periosteal contours is proposed. This method maximizes correlation with cross-sectional geometry (r(2) = .998) and minimizes prediction errors in all cases. The results underscore the importance of accurate periosteal measurement in the quantification of bone strength, and suggest that, regardless of theoretical scaling predictions, external area based robusticity estimates involving the product of diaphyseal diameters are most directly comparable to cross-sectional geometric properties when they are standardized using the product of body mass and bone length.

Most analyses of trabecular microarchitecture in mammals have focused on the functional significance of interspecific variation, but they have not effectively considered the influence of body size or phylogeny on bone architecture. The goals of this study were to determine the relationship between trabecular bone and body size in the humeral and femoral heads of extant primates, and to assess the influence of phylogeny on bone microstructure. Using a sample of 235 individuals from 34 primate species, ranging in body size from 0.06 to 130 kg, the relationships between trabecular bone structure and body size were assessed by using conventional and phylogenetic regression analyses. Bone volume fraction, trabecular thickness and trabecular spacing increase with body size, whereas bone surface-area-to-volume ratio decreases. Shape variables such as trabecular number, connectivity density and degree of anisotropy scale inversely with size. Most of these variables scale with significant negative allometry, except bone surface-area-to-volume ratio, which scales with slight positive allometry. Phylogenetic regressions indicate a relatively weak phylogenetic signal in some trabecular bone variables. These data demonstrate that, relative to body size, large primates have thinner and more tightly packed trabeculae than small primates. The relatively thin trabeculae in large primates and other mammals, coupled with constraints on trabecular thickness related to osteocyte function, suggest that increased skeletal loads in the postcranial joints of large mammals are probably mitigated not only through alterations in trabecular microarchitecture, but also through other mechanisms such as changes in cortical bone distribution, limb posture and gait speed.

Understanding the mechanically-mediated response of trabecular bone to locomotion-specific loading patterns would be of great benefit to comparative mammalian evolutionary morphology. Unfortunately, assessments of the correspondence between individual trabecular bone features and inferred behavior patterns have failed to reveal a strong locomotion-specific signal. This study assesses the relationship between inferred locomotor activity and a suite of trabecular bone structural features that characterize bone architecture. High-resolution computed tomography images were collected from the humeral and femoral heads of 115 individuals from eight anthropoid primate genera (Alouatta, Homo, Macaca, Pan, Papio, Pongo, Trachypithecus, Symphalangus). Discriminant function analyses reveal that subarticular trabecular bone in the femoral and humeral heads is significantly different among most locomotor groups. The results indicate that when a suite of femoral head trabecular features is considered, trabecular number and connectivity density, together with fabric anisotropy and the relative proportion of rods and plates, differentiate locomotor groups reasonably well. A similar, yet weaker, relationship is also evident in the trabecular architecture of the humeral head. The application of this multivariate approach to analyses of trabecular bone morphology in recent and fossil primates may enhance our ability to reconstruct locomotor behavior in the fossil record.

Although the correspondence between habitual activity and diaphyseal cortical bone morphology has been demonstrated for the fore- and hind-limb long bones of primates, the relationship between trabecular bone architecture and locomotor behavior is less certain. If sub-articular trabecular and diaphyseal cortical bone morphology reflects locomotor patterns, this correspondence would be a valuable tool with which to interpret morphological variation in the skeletal and fossil record. To assess this relationship, high-resolution computed tomography images from both the humeral and femoral head and midshaft of 112 individuals from eight anthropoid genera (Alouatta, Homo, Macaca, Pan, Papio, Pongo, Trachypithecus, and Symphalangus) were analyzed. Within-bone (sub-articular trabeculae vs. mid-diaphysis), between-bone (forelimb vs. hind limb), and among-taxa relative distributions (femoral:humeral) were compared. Three conclusions are evident: (1) Correlations exists between humeral head sub-articular trabecular bone architecture and mid-humerus diaphyseal bone properties; this was not the case in the femur. (2) In contrast to comparisons of inter-limb diaphyseal bone robusticity, among all species femoral head trabecular bone architecture is significantly more substantial (i.e., higher values for mechanically relevant trabecular bone architectural features) than humeral head trabecular bone architecture. (3) Interspecific comparisons of femoral morphology relative to humeral morphology reveal an osteological "locomotor signal" indicative of differential use of the forelimb and hind limb within mid-diaphysis cortical bone geometry, but not within sub-articular trabecular bone architecture.

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.