Functional adaptation of internal bone structure in the wrist of extant hominids and fossil hominins

The shape of wrist bones (carpals) in living hominids are thought to be adapted to the primary function of the hand, which in Homo sapiens is for manipulation, and in non-human hominids, locomotion. However, the hominid hand is inherently versatile in its use, and parsimony would suggest that the hominid last common ancestor was capable of manipulating and using simple tools. Therefore, key questions in palaeoanthropology ask when, why, and how tool use moved from facultative, as it is in other hominids, to obligate, as it is in H. sapiens. Inferring this transition within the fossil record is challenging as habitual behaviours are not always reflected in the external morphology of the skeleton. As the internal microstructure of bone is known to adapt to load dynamically, bone functional adaptation analyses provide an avenue to investigate how a joint has actually been loaded over an individual’s lifetime. The central question asked by this thesis was: ‘How and why does the internal structure of wrist bones differ among extant and extinct hominids?’. To achieve this aim, I investigated 1) whether functionally meaningful differences exist in the microarchitecture of extant hominid carpals; 2) how to detect signals of functional adaptation within the complex biomechanical environment of the wrist; 3) what can be inferred about hand use from the proximal capitate bone of fossil hominins? This thesis undertook three research projects, which all use ‘whole-bone’ methodologies for investigating functional signals of hand use. Using micro-computed tomography, I quantified and compared trabecular and cortical bone microarchitecture in 264 individual carpal bones across four extant hominids (Pongo, Gorilla, Pan, and H. sapiens) and four extinct hominins (Australopithecus sediba, Homo naledi, Homo floresiensis and Neanderthals). In the first project, I used inter- and intraspecific analyses to compare the trabecular and cortical microstructure of the proximal and distal capitate in extant hominids. Unique combinations of microarchitecture across the two segments of the bone differentiated the extant taxa. Notably, non-human hominids exhibited a distinctive pattern of extremely thick cortical bone in the distal capitate. This result suggested that highly localised functional adaptation responses were occurring across the capitate, and studying biomechanically distinct subregions of the carpus may be required to detect signals of functional adaptation. I then conducted intraspecific analyses on the scaphoid, lunate and triquetrum's trabecular and cortical bone microstructure across extant hominids. Results identified that microarchitectural differences across the three bones could be linked to the known or assumed biomechanics of the proximal row. Relative differences in the three bones differentiated locomotor mode between the genera: Gorilla and Pan expressed the same relative patterns of architecture, with Pongo and H. sapiens showing unique patterns. This project demonstrated that establishing relative patterns across a biomechanically distinct subregion of the wrist can differentiate hand use among extant hominids. Using a novel canonical holistic morphometric analysis, my final research project indicated that extant hominids have statistically distinct distributions of relative bone volume in the proximal capitate. Neanderthals and fossil H. sapiens exhibited the same pattern of relative bone distribution in the proximal capitate as modern H. sapiens suggesting a functional commitment to tool use leaves a distinct distribution of bone in the proximal capitate. Despite being the geologically oldest fossil, A. sediba was the only other species to exhibit a human-like distribution of bone, with evidence of a highly strained capitolunate and capitoscaphoid joint. Although H. naledi has human-like carpal morphology, it showed no evidence for human-like force transfer and loading at the midcarpal joint suggesting its hand use was not similar to a typical modern H. sapiens. The distribution of bone in H. floresiensis suggested that Oldowan-type tools were made and used with high ulnar-side loading of the hand and relatively lower loading of the thumb. This thesis demonstrated that a hand used primarily for manipulation has distinctive and statistically differentiated microarchitecture in the carpal bones. Unique microarchitectural features within the hominin species support a model of adaptive radiations of hand and tool behaviours among hominins. The similarity in microarchitecture at the midcarpal joint of H. sapiens and Neanderthals suggests it may be a strong signal of human-like commitment to tool use but is unlikely to capture variation in tool behaviour. Further analyses are needed to better understand how manipulation and arboreality are reflected in bone architecture. In particular, this thesis discussed how both climbing and transverse grips might be biomechanically compatible behaviours, as both emphasise high loading at the ulnar side of the hand and wrist and deemphasise the use of the thumb. Thus the use of transverse-type grips may have provided fossil hominins with an opportunity to improve the functional efficiency of tool behaviours without highly compromising climbing ability. Future analyses are likely to be most informative when numerous bones across biomechanically meaningful subregions of the wrist are analysed together. Analyses at the ulnar side of the wrist may be informative for identifying signals of climbing and grip preference differences in H. sapiens and Neanderthals.