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.
Highlights
Understanding the functional significance of skeletal morphology plays a critical role in addressing fundamental questions of primate evolution and questions of human evolution
Functional interpretations of skeletal or fossil remains have been based on external morphology and, informative, researchers argue over which features are functionally relevant for reconstructing behaviour in the past versus features that are possibly primitive retentions and no longer ‘functionally important’
Much experimental research has demonstrated the response of trabecular bone to mechanical stress throughout life [2,3,4,5], previous studies of trabecular bone structure in primate epiphyses – especially the humeral and femoral head – have often failed to identify clear differences in joint loading associated with habitual behaviours (e.g. [11,16,21,25])
Summary
Understanding the functional significance of skeletal morphology plays a critical role in addressing fundamental questions of primate evolution and questions of human evolution. Functional interpretations of skeletal or fossil remains have been based on external morphology and, informative, researchers argue over which features are functionally relevant for reconstructing behaviour in the past versus features that are possibly primitive retentions and no longer ‘functionally important’ (see review in [1]). Such debates have profound effects on our reconstruction of behaviour in fossil ancestors and the evolutionary pathways of humans and other primates. Since trabecular bone remodels rapidly throughout life [9], its structure can offer a more direct window into an individual’s behaviour and, in particular, to joint posture during predominant stress [3,5]
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