Does skeletal anatomy reflect adaptation to locomotor patterns? cortical and trabecular architecture in human and nonhuman anthropoids

Abstract

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.

Gracility of the modernHomo sapiensskeleton is the result of decreased biomechanical loading

“…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 calcaneus (17), the anthropoid proximal femur (18), and several other clinical studies of femoral head trabecular bone architecture in contemporary adult humans (21-24). The results of these studies suggest that relative trabecular bone volume in the axial skeleton and lower limbs is significantly lower in modern humans compared with quadrupeds, despite the legs and vertebral column bearing a higher proportion of body mass and peak substrate reaction forces during bipedal locomotion (25)(26)(27).…”

“…Human proximal femora were scanned on the OMNI-X HD600 microcomputed tomography scanner (Varian Medical Systems) at the Center for Quantitative Imaging, Pennsylvania State University. All nonhuman primates included in the study were scanned at the Center for Quantitative Imaging or at the University of Texas at Austin's High-Resolution X-Ray Computed Tomography Facility (18,52,(64)(65)(66). Voxel dimensions ranged from 0.0068 and 0.0687 mm, depending on size of the specimen.…”

“…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.…”

The Effect of the Achilles Tendon on Trabecular Structure in the Primate Calcaneus

“…Comparative studies characterizing the microarchitecture of trabecular bone have consistently found that humans have a lower bone volume fraction (BV/TV) than chimpanzees. Whether in the humeral head (Shaw and Ryan, 2012;Scherf et al, 2013), first metacarpal head (Lazenby et al, 2011), thoracic vertebra (Cotter et al, 2011), femoral head (Shaw and Ryan, 2012), calcaneal body (Maga et al, 2006), talar body (DeSilva and Devlin, 2012), or medial metatarsal heads (Griffin et al, 2010), humans consistently possess lower BV/TV than chimpanzees. Under the Achilles tendon insertion, however, we found a trend towards slightly higher BV/TV in humans than in chimpanzees, though this trend was not statistically significant.…”

“…Alternatively, if our model for how the Achilles tendon loads calcaneal trabecular bone is correct, then our findings contradict some predictions of Wolff's "Law." Although many have found evidence for trabecular bone adaptation to changes in diet and hormones (Hodgkinson et al, 1978;Reeve et al, 1980;Devlin et al, 2010), and loading (Pontzer et al, 2006;Barak et al, 2011), others (Fajardo et al, 2007;Ryan and Walker, 2010;Shaw and Ryan, 2012;DeSilva and Devlin, 2012) have found the relationship between trabecular bone and inferred mechanical loading in primates to be more complicated. Although trabecular bone clearly is responsive to a variety of factors, Achilles tendon length may not affect trabecular properties as we had predicted.…”