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Trabecular bone structure correlates with hand posture and use in hominoids.

ABSTRACT: Bone is capable of adapting during life in response to stress. Therefore, variation in locomotor and manipulative behaviours across extant hominoids may be reflected in differences in trabecular bone structure. The hand is a promising region for trabecular analysis, as it is the direct contact between the individual and the environment and joint positions at peak loading vary amongst extant hominoids. Building upon traditional volume of interest-based analyses, we apply a whole-epiphysis analytical approach using high-resolution microtomographic scans of the hominoid third metacarpal to investigate whether trabecular structure reflects differences in hand posture and loading in knuckle-walking (Gorilla, Pan), suspensory (Pongo, Hylobates and Symphalangus) and manipulative (Homo) taxa. Additionally, a comparative phylogenetic method was used to analyse rates of evolutionary changes in trabecular parameters. Results demonstrate that trabecular bone volume distribution and regions of greatest stiffness (i.e., Young's modulus) correspond with predicted loading of the hand in each behavioural category. In suspensory and manipulative taxa, regions of high bone volume and greatest stiffness are concentrated on the palmar or distopalmar regions of the metacarpal head, whereas knuckle-walking taxa show greater bone volume and stiffness throughout the head, and particularly in the dorsal region; patterns that correspond with the highest predicted joint reaction forces. Trabecular structure in knuckle-walking taxa is characterised by high bone volume fraction and a high degree of anisotropy in contrast to the suspensory brachiators. Humans, in which the hand is used primarily for manipulation, have a low bone volume fraction and a variable degree of anisotropy. Finally, when trabecular parameters are mapped onto a molecular-based phylogeny, we show that the rates of change in trabecular structure vary across the hominoid clade. Our results support a link between inferred behaviour and trabecular structure in extant hominoids that can be informative for reconstructing behaviour in fossil primates.

SUBMITTER: Tsegai ZJ

PROVIDER: S-EPMC3828321 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Trabecular bone structure correlates with hand posture and use in hominoids.

Tsegai Zewdi J ZJ Kivell Tracy L TL Gross Thomas T Nguyen N Huynh NH Pahr Dieter H DH Smaers Jeroen B JB Skinner Matthew M MM

PloS one 20131114 11

Bone is capable of adapting during life in response to stress. Therefore, variation in locomotor and manipulative behaviours across extant hominoids may be reflected in differences in trabecular bone structure. The hand is a promising region for trabecular analysis, as it is the direct contact between the individual and the environment and joint positions at peak loading vary amongst extant hominoids. Building upon traditional volume of interest-based analyses, we apply a whole-epiphysis analyti ...[more]

PMID: 24244359

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Project description:Morphological variation in the hominoid capitate has been linked to differences in habitual locomotor activity due to its importance in movement and load transfer at the midcarpal joint proximally and carpometacarpal joints distally. Although the shape of bones and their articulations are linked to joint mobility, the internal structure of bones has been shown experimentally to reflect, at least in part, the loading direction and magnitude experienced by the bone. To date, it is uncertain whether locomotor differences among hominoids are reflected in the bone microarchitecture of the capitate. Here, we apply a whole-bone methodology to quantify the cortical and trabecular architecture (separately and combined) of the capitate across bipedal (modern Homo sapiens), knuckle-walking (Pan paniscus, Pan troglodytes, Gorilla sp.), and suspensory (Pongo sp.) hominoids (n = 69). It is hypothesized that variation in bone microarchitecture will differentiate these locomotor groups, reflecting differences in habitual postures and presumed loading force and direction. Additionally, it is hypothesized that trabecular and cortical architecture in the proximal and distal regions, as a result of being part of mechanically divergent joints proximally and distally, will differ across these portions of the capitate. Results indicate that the capitate of knuckle-walking and suspensory hominoids is differentiated from bipedal Homo primarily by significantly thicker distal cortical bone. Knuckle-walking taxa are further differentiated from suspensory and bipedal taxa by more isotropic trabeculae in the proximal capitate. An allometric analysis indicates that size is not a significant determinate of bone variation across hominoids, although sexual dimorphism may influence some parameters within Gorilla. Results suggest that internal trabecular and cortical bone is subjected to different forces and functional adaptation responses across the capitate (and possibly other short bones). Additionally, while separating trabecular and cortical bone is normal protocol of current whole-bone methodologies, this study shows that when applied to carpals, removing or studying the cortical bone separately potentially obfuscates functionally relevant signals in bone structure.

Project description:Structure model index (SMI) is widely used to measure rods and plates in trabecular bone. It exploits the change in surface curvature that occurs as a structure varies from spherical (SMI?=?4), to cylindrical (SMI?=?3) to planar (SMI?=?0). The most important assumption underlying SMI is that the entire bone surface is convex and that the curvature differential is positive at all points on the surface. The intricate connections within the trabecular continuum suggest that a high proportion of the surface could be concave, violating the assumption of convexity and producing regions of negative differential. We implemented SMI in the BoneJ plugin and included the ability to measure the amounts of surface that increased or decreased in area after surface mesh dilation, and the ability to visualize concave and convex regions. We measured SMI and its positive (SMI(+)) and negative (SMI(-)) components, bone volume fraction (BV/TV), the fraction of the surface that is concave (CF), and mean ellipsoid factor (EF) in trabecular bone using 38 X-ray microtomography (XMT) images from a rat ovariectomy model of sex steroid rescue of bone loss, and 169 XMT images from a broad selection of 87 species' femora (mammals, birds, and a crocodile). We simulated bone resorption by eroding an image of elephant trabecule and recording SMI and BV/TV at each erosion step. Up to 70%, and rarely <20%, of the trabecular surface is concave (CF 0.155-0.700). SMI is unavoidably influenced by aberrations induced by SMI(-), which is strongly correlated with BV/TV and CF. The plate-to-rod transition in bone loss is an erroneous observation resulting from the close and artifactual relationship between SMI and BV/TV. SMI cannot discern between the distinctive trabecular geometries typical of mammalian and avian bone, whereas EF clearly detects birds' more plate-like trabecule. EF is free from confounding relationships with BV/TV and CF. SMI results reported in the literature should be treated with suspicion. We propose that EF should be used instead of SMI for measurements of rods and plates in trabecular bone.

Project description:The trabecular bone morphology of adult extant primates has been shown to reflect mechanical loading related to locomotion. However, ontogenetic studies of humans and other mammals suggest an adaptive lag between trabecular bone response and current mechanical loading patterns that could result in adult trabecular bone morphology reflecting juvenile behaviours. This study investigates ontogenetic changes in the trabecular bone structure of the third metacarpal of mountain gorillas (Gorilla beringei beringei; n = 26) and western lowland gorillas (Gorilla gorilla gorilla; n = 26) and its relationship to expected changes in locomotor loading patterns. Results show that trabecular bone reflects predicted mechanical loading throughout ontogeny. Bone volume fraction, trabecular thickness and trabecular number are low at birth and increase with age, although degree of anisotropy remains relatively stable throughout ontogeny. A high concentration of bone volume fraction can be observed in the distopalmar region of the third metacarpal epiphysis in early ontogeny, consistent with the high frequency of climbing, suspensory and other grasping behaviours in young gorillas. High trabecular bone concentration increases dorsally in the epiphysis during the juvenile period as terrestrial knuckle-walking becomes the primary form of locomotion. However, fusion of the epiphysis does not take place until 10-11 years of age, and overall trabecular structure does not fully reflect the adult pattern until 12 years of age, indicating a lag between adult-like behaviours and adult-like trabecular morphology. We found minimal differences in trabecular ontogeny between mountain and western lowland gorillas, despite presumed variation in the frequencies of arboreal locomotor behaviours. Altogether, ontogenetic changes in Gorilla metacarpal trabecular structure reflect overall genus-level changes in locomotor behaviours throughout development, but with some ontogenetic lag that should be considered when drawing functional conclusions from bone structure in extant or fossil adolescent specimens.

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Trabecular bone structure correlates with hand posture and use in hominoids.

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Trabecular bone structure correlates with hand posture and use in hominoids.

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