An official website of the United States government
Synopsis Mammals exhibit a diverse range of limb morphologies that are associated with different locomotor ecologies and structural mechanics. Much remains to be investigated, however, about the combined effects of locomotor modes and scaling on the external shape and structural properties of limb bones. Here, we used squirrels (Sciuridae) as a model clade to examine the effects of locomotor mode and scaling on the external shape and structure of the two major limb bones, the humerus and femur. We quantified humeral and femoral morphologies using 3D geometric morphometrics and bone structure analyses on a sample of 76 squirrel species across their four major ecotypes. We then used phylogenetic generalized linear models to test how locomotor ecology, size, and their interaction influenced morphological traits. We found that size and locomotor mode exhibit different relationships with the external shape and structure of the limb bones, and that these relationships differ between the humerus and femur. External shapes of the humerus and, to a lesser extent, the femur are best explained by locomotor ecology rather than by size, whereas structures of both bones are best explained by interactions between locomotor ecology and scaling. Interestingly, the statistical relationships between limb morphologies and ecotype were lost when accounting for phylogenetic relationships among species under Brownian motion. That assuming Brownian motion confounded these relationships is not surprising considering squirrel ecotypes are phylogenetically clustered; our results suggest that humeral and femoral variation partitioned early between clades and their ecomorphologies were maintained to the present. Overall, our results show how mechanical constraints, locomotor ecology, and evolutionary history may enact different pressures on the shape and structure of limb bones in mammals.
more »
« less
Complex variation of trabecular bone structure in the proximal humerus and femur of five modern human populations
Abstract ObjectiveThis 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? MethodsThe 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. ResultsIn 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. ConclusionsReduced 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.
more »
« less
- PAR ID:
- 10462389
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- American Journal of Physical Anthropology
- Volume:
- 168
- Issue:
- 1
- ISSN:
- 0002-9483
- Page Range / eLocation ID:
- p. 104-118
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract ObjectivesHumans exhibit significant ecogeographic variation in bone size and shape. However, it is unclear how significantly environmental temperature influences cortical and trabecular bone, making it difficult to recognize adaptation versus acclimatization in past populations. There is some evidence that cold‐induced bone loss results from sympathetic nervous system activation and can be reduced by nonshivering thermogenesis (NST) via uncoupling protein (UCP1) in brown adipose tissue (BAT). Here we test two hypotheses: (1) low temperature induces impaired cortical and trabecular bone acquisition and (2) UCP1, a marker of NST in BAT, increases in proportion to degree of low‐temperature exposure. MethodsWe housed wildtype C57BL/6J male mice in pairs at 26 °C (thermoneutrality), 22 °C (standard), and 20 °C (cool) from 3 weeks to 6 or 12 weeks of age with access to food and water ad libitum (N= 8/group). ResultsCool housed mice ate more but had lower body fat at 20 °C versus 26 °C. Mice at 20 °C had markedly lower distal femur trabecular bone volume fraction, thickness, and connectivity density and lower midshaft femur cortical bone area fraction versus mice at 26 °C (p< .05 for all). UCP1 expression in BAT was inversely related to temperature. DiscussionThese results support the hypothesis that low temperature was detrimental to bone mass acquisition. Nonshivering thermogenesis in brown adipose tissue increased in proportion to low‐temperature exposure but was insufficient to prevent bone loss. These data show that chronic exposure to low temperature impairs bone architecture, suggesting climate may contribute to phenotypic variation in humans and other hominins.more » « less
-
Abstract ObjectivesThe objective of this study is to demonstrate a new method for analyzing trabecular bone volume fraction and degree of anisotropy in three dimensions. MethodsWe use a combination of automatic mesh registration, point‐cloud correspondence registration, andP‐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. ResultsWe 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. ConclusionsWe 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.more » « less
-
ABSTRACT The gut microbiome impacts bone mass, which implies a disruption to bone homeostasis. However, it is not yet clear how the gut microbiome affects the regulation of bone mass and bone quality. We hypothesized that germ‐free (GF) mice have increased bone mass and decreased bone toughness compared with conventionally housed mice. We tested this hypothesis using adult (20‐ to 21‐week‐old) C57BL/6J GF and conventionally raised female and male mice (n = 6–10/group). Trabecular microarchitecture and cortical geometry were measured from micro–CT of the femur distal metaphysis and cortical midshaft. Whole‐femur strength and estimated material properties were measured using three‐point bending and notched fracture toughness. Bone matrix properties were measured for the cortical femur by quantitative back‐scattered electron imaging and nanoindentation, and, for the humerus, by Raman spectroscopy and fluorescent advanced glycation end product (fAGE) assay. Shifts in cortical tissue metabolism were measured from the contralateral humerus. GF mice had reduced bone resorption, increased trabecular bone microarchitecture, increased tissue strength and decreased whole‐bone strength that was not explained by differences in bone size, increased tissue mineralization and fAGEs, and altered collagen structure that did not decrease fracture toughness. We observed several sex differences in GF mice, most notably for bone tissue metabolism. Male GF mice had a greater signature of amino acid metabolism, and female GF mice had a greater signature of lipid metabolism, exceeding the metabolic sex differences of the conventional mice. Together, these data demonstrate that the GF state in C57BL/6J mice alters bone mass and matrix properties but does not decrease bone fracture resistance. © 2023 The Authors.Journal of Bone and Mineral Researchpublished by Wiley Periodicals LLC on behalf of American Society for Bone and Mineral Research (ASBMR).more » « less
-
Abstract ObjectivesVariation 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 methodsWe 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. ResultsAll 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. DiscussionResults 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.more » « less
