Trabecular architecture of the distal femur in extant hominids.

Extant great apes are characterized by a wide range of locomotor, postural and manipulative behaviours that each require the limbs to be used in different ways. In addition to external bone morphology, comparative investigation of trabecular bone, which (re-)models to reflect loads incurred during life, can provide novel insights into bone functional adaptation. Here, we use canonical holistic morphometric analysis (cHMA) to analyse the trabecular morphology in the distal femoral epiphysis of Homo sapiens (n = 26), Gorilla gorilla (n = 14), Pan troglodytes (n = 15) and Pongo sp. (n = 9). We test two predictions: (1) that differing locomotor behaviours will be reflected in differing trabecular architecture of the distal femur across Homo, Pan, Gorilla and Pongo; (2) that trabecular architecture will significantly differ between male and female Gorilla due to their different levels of arboreality but not between male and female Pan or Homo based on previous studies of locomotor behaviours. Results indicate that trabecular architecture differs among extant great apes based on their locomotor repertoires. The relative bone volume and degree of anisotropy patterns found reflect habitual use of extended knee postures during bipedalism in Homo, and habitual use of flexed knee posture during terrestrial and arboreal locomotion in Pan and Gorilla. Trabecular architecture in Pongo is consistent with a highly mobile knee joint that may vary in posture from extension to full flexion. Within Gorilla, trabecular architecture suggests a different loading of knee in extension/flexion between females and males, but no sex differences were found in Pan or Homo, supporting our predictions. Inter- and intra-specific variation in trabecular architecture of distal femur provides a comparative context to interpret knee postures and, in turn, locomotor behaviours in fossil hominins.

The deep trabecular structure of first metacarpals in extant hominids.

OBJECTIVES: Recent studies have associated subarticular trabecular bone distribution in the extant hominid first metacarpal (Mc1) with observed thumb use, to infer fossil hominin thumb use. Here, we analyze the entire Mc1 to test for interspecific differences in: (1) the absolute volume of trabecular volume fraction, (2) the distribution of the deeper trabecular network, and (3) the distribution of trabeculae in the medullary cavity, especially beneath the Mc1 disto-radial flange. MATERIALS AND METHODS: Trabecular bone was imaged using micro-computed tomography in a sample of Homo sapiens (n = 11), Pan paniscus (n = 10), Pan troglodytes (n = 11), Gorilla gorilla (n = 10) and Pongo sp., (n = 7). Using Canonical Holistic Morphometric Analysis (cHMA), we tested for interspecific differences in the trabecular bone volume fraction (BV/TV) and its relative distribution (rBV/TV) throughout the Mc1, including within the head, medullary cavity, and base. RESULTS: P. paniscus had the highest, and H. sapiens the lowest, BV/TV relative to other species. rBV/TV distribution statistically distinguished the radial concentrations and lack of medullary trabecular bone in the H. sapiens Mc1 from all other hominids. H. sapiens and, to a lesser extent, G. gorilla also had a significantly higher trabecular volume beneath the disto-radial flange relative to other hominids. DISCUSSION: These results are consistent with differences in observed thumb use in these species and may also reflect systemic differences in bone volume fraction. The trabecular bone extension into the medullary cavity and concentrations beneath the disto-radial flange may represent crucial biomechanical signals that will aid in the inference of fossil hominin thumb use.

Morphological integration and shape covariation between the trapezium and first metacarpal among extant hominids.

OBJECTIVES: The shape of the trapezium and first metacarpal (Mc1) markedly influence thumb mobility, strength, and the manual abilities of extant hominids. Previous research has typically focused solely on trapezium-Mc1 joint shape. Here we investigate how morphological integration and shape covariation between the entire trapezium (articular and non-articular surfaces) and the entire Mc1 reflect known differences in thumb use in extant hominids. MATERIALS AND METHODS: We analyzed shape covariation in associated trapezia and Mc1s across a large, diverse sample of Homo sapiens (n = 40 individuals) and other extant hominids (Pan troglodytes, n = 16; Pan paniscus, n = 13; Gorilla gorilla gorilla, n = 27; Gorilla beringei, n = 6; Pongo pygmaeus, n = 14; Pongo abelii, n = 9) using a 3D geometric morphometric approach. We tested for interspecific significant differences in degree of morphological integration and patterns of shape covariation between the entire trapezium and Mc1, as well as within the trapezium-Mc1 joint specifically. RESULTS: Significant morphological integration was only found in the trapezium-Mc1 joint of H. sapiens and G. g. gorilla. Each genus showed a specific pattern of shape covariation between the entire trapezium and Mc1 that was consistent with different intercarpal and carpometacarpal joint postures. DISCUSSION: Our results are consistent with known differences in habitual thumb use, including a more abducted thumb during forceful precision grips in H. sapiens and a more adducted thumb in other hominids used for diverse grips. These results will help to infer thumb use in fossil hominins.

Variation and covariation of external shape and cross-sectional geometry in the human metacarpus.

OBJECTIVES: Analyses of external bone shape using geometric morphometrics (GM) and cross-sectional geometry (CSG) are frequently employed to investigate bone structural variation and reconstruct activity in the past. However, the association between these methods has not been thoroughly investigated. Here, we analyze whole bone shape and CSG variation of metacarpals 1-5 and test covariation between them. MATERIALS AND METHODS: We analyzed external metacarpal shape using GM and CSG of the diaphysis at three locations in metacarpals 1-5. The study sample includes three modern human groups: crew from the shipwrecked Mary Rose (n = 35 metacarpals), a Pre-industrial group (n = 50), and a Post-industrial group (n = 31). We tested group differences in metacarpal shape and CSG, as well as correlations between these two aspects of metacarpal bone structure. RESULTS: GM analysis demonstrated metacarpus external shape variation is predominately related to changes in diaphyseal width and articular surface size. Differences in external shape were found between the non-pollical metacarpals of the Mary Rose and Pre-industrial groups and between the third metacarpals of the Pre- and Post-industrial groups. CSG results suggest the Mary Rose and Post-industrial groups have stronger metacarpals than the Pre-industrial group. Correlating CSG and external shape showed significant relationships between increasing external robusticity and biomechanical strength across non-pollical metacarpals (r: 0.815-0.535; p ≤ 0.05). DISCUSSION: Differences in metacarpal cortical structure and external shape between human groups suggest differences in the type and frequency of manual activities. Combining these results with studies of entheses and kinematics of the hand will improve reconstructions of manual behavior in the past.

Trabecular bone structure of the proximal capitate in extant hominids and fossil hominins with implications for midcarpal joint loading and the dart-thrower's motion.

OBJECTIVES: This research examines whether the distribution of trabecular bone in the proximal capitates of extant hominids, as well as several fossil hominin taxa, is associated with the oblique path of the midcarpal joint known as the dart-thrower's motion (DTM). MATERIALS AND METHODS: We analyzed proximal capitates from extant (Pongo n = 12; Gorilla n = 11; Pan n = 10; fossil and recent Homo sapiens n = 29) and extinct (Australopithecus sediba n = 2; Homo naledi n = 1; Homo floresiensis n = 2; Neandertals n = 3) hominids using a new canonical holistic morphometric analysis, which quantifies and visualizes the distribution of trabecular bone using relative bone volume as a fraction of total volume (rBV/TV). RESULTS: Homo sapiens and Neandertals had a continuous band of high rBV/TV that extended across the scaphoid, lunate, and hamate subarticular regions, but other fossil hominins and extant great apes did not. A. sediba expressed a distinct combination of human-like and Pan-like rBV/TV distribution. Both H. floresiensis and H. naledi had high rBV/TV on the ulnar-side of the capitate but low rBV/TV on the radial-side. CONCLUSION: The proximal capitates of H. sapiens and Neandertals share a distinctive distribution of trabecular bone that suggests that these two species of Homo regularly load(ed) their midcarpal joints along the full extent of the oblique path of the DTM. The observed pattern in A. sediba suggests that human-like stress at the capito-scaphoid articular surface was combined with Pan-like wrist postures, whereas the patterns in H. floresiensis and H. naledi suggest their midcarpal joints were loaded differently from that of H. sapiens and Neandertals.

A computational framework for canonical holistic morphometric analysis of trabecular bone.

Bone is a remarkable, living tissue that functionally adapts to external loading. Therefore, bone shape and internal structure carry information relevant to many disciplines, including medicine, forensic science, and anthropology. However, morphometric comparisons of homologous regions across different individuals or groups are still challenging. In this study, two methods were combined to quantify such differences: (1) Holistic morphometric analysis (HMA) was used to quantify morphometric values in each bone, (2) which could then be mapped to a volumetric mesh of a canonical bone created by a statistical free-form deformation model (SDM). Required parameters for this canonical holistic morphometric analysis (cHMA) method were identified and the robustness of the method was evaluated. The robustness studies showed that the SDM converged after one to two iterations, had only a marginal bias towards the chosen starting image, and could handle large shape differences seen in bones of different species. Case studies were performed on metacarpal bones and proximal femora of different primate species to confirm prior study results. The differences between species could be visualised and statistically analysed in both case studies. cHMA provides a framework for performing quantitative comparisons of different morphometric quantities across individuals or groups. These comparisons facilitate investigation of the relationship between spatial morphometric variations and function or pathology, or both.

Kinetics of stone tool production among novice and expert tool makers.

OBJECTIVES: As is the case among many complex motor tasks that require prolonged practice before achieving expertise, aspects of the biomechanics of knapping vary according to the relative experience/skill level of the practitioner. In archaeological experiments focused on the production of Plio-Pleistocene stone tools, these skill-mediated biomechanical differences have bearings on experimental design, the interpretation of results, and lithic assemblage analysis. A robust body of work exists on variation in kinematic patterns across skill levels but less is known about potential kinetic differences. The current study was undertaken to better understand kinetic patterns observed across skill levels during "Oldowan," freehand stone tool production. MATERIALS AND METHODS: Manual pressure data were collected from 23 novice and 9 expert stone tool makers during the production of simple stone flakes using direct hard hammer percussion. RESULTS: Results show that expert tool makers experienced significantly lower cumulative pressure magnitudes and pressure-time integral magnitudes compared with novices. In expert knappers, digits I and II experienced similarly high pressures (both peak pressure and pressure-time integrals) and low variability in pressure relative to digits III-V. Novices, in contrast, tended to hold hammerstones such that pressure patterns were similar across digits II-V, and they showed low variability on digit I only. DISCUSSION: The similar and consistent emphasis of the thumb by both skill groups indicates the importance of this digit in stabilizing the hammerstone. The emphasis placed on digit II is exclusive to expert knappers, and so this digit may offer osteological signals diagnostic of habitual expert tool production.

The implications of thumb movements for Neanderthal and modern human manipulation.

Much research has debated the technological abilities of Neanderthals relative to those of early modern humans, with a particular focus on subtle differences in thumb morphology and how this may reflect differences in manipulative behaviors in these two species. Here, we provide a novel perspective on this debate through a 3D geometric morphometric analysis of shape covariation between the trapezial and proximal first metacarpal articular surfaces of Neanderthals (Homo neanderthalensis) in comparison to early and recent humans (Homo sapiens). Results show a distinct pattern of shape covariation in Neanderthals, consistent with more extended and adducted thumb postures that may reflect habitual use of grips commonly used for hafted tools. Both Neanderthals and recent humans demonstrate high intraspecific variation in shape covariation. This intraspecific variation is likely the result of genetic and/or developmental differences, but may also reflect, in part, differing functional requirements imposed by the use of varied tool-kits. These results underscore the importance of holistic joint shape analysis for understanding the functional capabilities and evolution of the modern human thumb.

The position of Australopithecus sediba within fossil hominin hand use diversity.

The human lineage is marked by a transition in hand use, from locomotion towards increasingly dexterous manipulation, concomitant with bipedalism. The forceful precision grips used by modern humans probably evolved in the context of tool manufacture and use, but when and how many times hominin hands became principally manipulative remains unresolved. We analyse metacarpal trabecular and cortical bone, which provide insight into behaviour during an individual's life, to demonstrate previously unrecognized diversity in hominin hand use. The metacarpals of the palm in Australopithecus sediba have trabecular morphology most like orangutans and consistent with locomotor power-grasping with the fingers, while that of the thumb is consistent with human-like manipulation. This internal morphology is the first record of behaviour consistent with a hominin that used its hand for both arboreal locomotion and human-like manipulation. This hand use is distinct from other fossil hominins in this study, including A. afarensis and A. africanus.

Evidence for habitual climbing in a Pleistocene hominin in South Africa.

Bipedalism is a defining trait of the hominin lineage, associated with a transition from a more arboreal to a more terrestrial environment. While there is debate about when modern human-like bipedalism first appeared in hominins, all known South African hominins show morphological adaptations to bipedalism, suggesting that this was their predominant mode of locomotion. Here we present evidence that hominins preserved in the Sterkfontein Caves practiced two different locomotor repertoires. The trabecular structure of a proximal femur (StW 522) attributed to Australopithecus africanus exhibits a modern human-like bipedal locomotor pattern, while that of a geologically younger specimen (StW 311) attributed to either Homo sp. or Paranthropus robustus exhibits a pattern more similar to nonhuman apes, potentially suggesting regular bouts of both climbing and terrestrial bipedalism. Our results demonstrate distinct morphological differences, linked to behavioral differences between Australopithecus and later hominins in South Africa and contribute to the increasing evidence of locomotor diversity within the hominin clade.

Trabecular variation in the first metacarpal and manipulation in hominids.

OBJECTIVES: The dexterity of fossil hominins is often inferred by assessing the comparative manual anatomy and behaviors of extant hominids, with a focus on the thumb. The aim of this study is to test whether trabecular structure is consistent with what is currently known about habitually loaded thumb postures across extant hominids. MATERIALS AND METHODS: We analyze first metacarpal (Mc1) subarticular trabecular architecture in humans (Homo sapiens, n = 10), bonobos (Pan paniscus, n = 10), chimpanzees (Pan troglodytes, n = 11), as well as for the first time, gorillas (Gorilla gorilla gorilla, n = 10) and orangutans (Pongo sp., n = 1, Pongo abelii, n = 3 and Pongo pygmaeus, n = 5). Using a combination of subarticular and whole-epiphysis approaches, we test for significant differences in relative trabecular bone volume (RBV/TV) and degree of anisotropy (DA) between species. RESULTS: Humans have significantly greater RBV/TV on the radiopalmar aspects of both the proximal and distal Mc1 subarticular surfaces and greater DA throughout the Mc1 head than other hominids. Nonhuman great apes have greatest RBV/TV on the ulnar aspect of the Mc1 head and the palmar aspect of the Mc1 base. Gorillas possessed significantly lower DA in the Mc1 head than any other taxon in our sample. DISCUSSION: These results are consistent with abduction of the thumb during forceful "pad-to-pad" precision grips in humans and, in nonhuman great apes, a habitually adducted thumb that is typically used in precision and power grips. This comparative context will help infer habitual manipulative and locomotor grips in fossil hominins.

The unexpected importance of the fifth digit during stone tool production.

Unique anatomical features of the human hand facilitate our ability to proficiently and forcefully perform precision grips and in-hand manipulation of objects. Extensive research has been conducted into the role of digits one to three during these manual behaviours, and the origin of the highly derived first digit anatomy that facilitates these capabilities. Stone tool production has long been thought a key influence in this regard. Despite previous research stressing the unique derived morphology of the human fifth digit little work has investigated why humans alone display these features. Here we examine the recruitment frequency, loading magnitude, and loading distribution of all digits on the non-dominant hand of skilled flintknappers during four technologically distinct types of Lower Palaeolithic stone tool production. Our data reveal the fifth digit to be heavily and frequently recruited during all studied behaviours. It occasionally incurred pressures, and was used in frequencies, greater or equal to those of the thumb, and frequently the same or greater than those of the index finger. The fifth digit therefore appears key to >2 million years of stone tool production activities, a behaviour that likely contributed to the derived anatomy observed in the modern human fifth ray.

Metacarpal trabecular bone varies with distinct hand-positions used in hominid locomotion.

Trabecular bone remodels during life in response to loading and thus should, at least in part, reflect potential variation in the magnitude, frequency and direction of joint loading across different hominid species. Here we analyse the trabecular structure across all non-pollical metacarpal distal heads (Mc2-5) in extant great apes, expanding on previous volume of interest and whole-epiphysis analyses that have largely focused on only the first or third metacarpal. Specifically, we employ both a univariate statistical mapping and a multivariate approach to test for both inter-ray and interspecific differences in relative trabecular bone volume fraction (RBV/TV) and degree of anisotropy (DA) in Mc2-5 subchondral trabecular bone. Results demonstrate that whereas DA values only separate Pongo from African apes (Pan troglodytes, Pan paniscus, Gorilla gorilla), RBV/TV distribution varies with the predicted loading of the metacarpophalangeal (McP) joints during locomotor behaviours in each species. Gorilla exhibits a relatively dorsal distribution of RBV/TV consistent with habitual hyper-extension of the McP joints during knuckle-walking, whereas Pongo has a palmar distribution consistent with flexed McP joints used to grasp arboreal substrates. Both Pan species possess a disto-dorsal distribution of RBV/TV, compatible with multiple hand postures associated with a more varied locomotor regime. Further inter-ray comparisons reveal RBV/TV patterns consistent with varied knuckle-walking postures in Pan species in contrast to higher RBV/TV values toward the midline of the hand in Mc2 and Mc5 of Gorilla, consistent with habitual palm-back knuckle-walking. These patterns of trabecular bone distribution and structure reflect different behavioural signals that could be useful for determining the behaviours of fossil hominins.

Inverse remodelling algorithm identifies habitual manual activities of primates based on metacarpal bone architecture.

Previously, a micro-finite element (micro-FE)-based inverse remodelling method was presented in the literature that reconstructs the loading history of a bone based on its architecture alone. Despite promising preliminary results, it remains unclear whether this method is sensitive enough to detect differences of bone loading related to pathologies or habitual activities. The goal of this study was to test the sensitivity of the inverse remodelling method by predicting joint loading histories of metacarpal bones of species with similar anatomy but clearly distinct habitual hand use. Three groups of habitual hand use were defined using the most representative primate species: manipulation (human), suspensory locomotion (orangutan), and knuckle-walking locomotion (bonobo, chimpanzee, gorilla). Nine to ten micro-computed tomography scans of each species ([Formula: see text] in total) were used to create micro-FE models of the metacarpal head region. The most probable joint loading history was predicted by optimally scaling six load cases representing joint postures ranging from [Formula: see text] (extension) to [Formula: see text] (flexion). Predicted mean joint load directions were significantly different between knuckle-walking and non-knuckle-walking groups ([Formula: see text]) and in line with expected primary hand postures. Mean joint load magnitudes tended to be larger in species using their hands for locomotion compared to species using them for manipulation. In conclusion, this study shows that the micro-FE-based inverse remodelling method is sensitive enough to detect differences of joint loading related to habitual manual activities of primates and might, therefore, be useful for palaeoanthropologists to reconstruct the behaviour of extinct species and for biomedical applications such as detecting pathological joint loading.

Manual restrictions on Palaeolithic technological behaviours.

The causes of technological innovation in the Palaeolithic archaeological record are central to understanding Plio-Pleistocene hominin behaviour and temporal trends in artefact variation. Palaeolithic archaeologists frequently investigate the Oldowan-Acheulean transition and technological developments during the subsequent million years of the Acheulean technocomplex. Here, we approach the question of why innovative stone tool production techniques occur in the Lower Palaeolithic archaeological record from an experimental biomechanical and evolutionary perspective. Nine experienced flintknappers reproduced Oldowan flake tools, 'early Acheulean' handaxes, and 'late Acheulean' handaxes while pressure data were collected from their non-dominant (core-holding) hands. For each flake removal or platform preparation event performed, the percussor used, the stage of reduction, the core securing technique utilised, and the relative success of flake removals were recorded. Results indicate that more heavily reduced, intensively shaped handaxes with greater volumetric controls do not necessarily require significantly greater manual pressure than Oldowan flake tools or earlier 'rougher' handaxe forms. Platform preparation events do, however, require significantly greater pressure relative to either soft or hard hammer flake detachments. No significant relationships were identified between flaking success and pressure variation. Our results suggest that the preparation of flake platforms, a technological behaviour associated with the production of late Acheulean handaxes, could plausibly have been restricted prior to the emergence of more forceful precision-manipulative capabilities than those required for earlier lithic technologies.

MIA-Clustering: a novel method for segmentation of paleontological material.

Paleontological research increasingly uses high-resolution micro-computed tomography (µCT) to study the inner architecture of modern and fossil bone material to answer important questions regarding vertebrate evolution. This non-destructive method allows for the measurement of otherwise inaccessible morphology. Digital measurement is predicated on the accurate segmentation of modern or fossilized bone from other structures imaged in µCT scans, as errors in segmentation can result in inaccurate calculations of structural parameters. Several approaches to image segmentation have been proposed with varying degrees of automation, ranging from completely manual segmentation, to the selection of input parameters required for computational algorithms. Many of these segmentation algorithms provide speed and reproducibility at the cost of flexibility that manual segmentation provides. In particular, the segmentation of modern and fossil bone in the presence of materials such as desiccated soft tissue, soil matrix or precipitated crystalline material can be difficult. Here we present a free open-source segmentation algorithm application capable of segmenting modern and fossil bone, which also reduces subjective user decisions to a minimum. We compare the effectiveness of this algorithm with another leading method by using both to measure the parameters of a known dimension reference object, as well as to segment an example problematic fossil scan. The results demonstrate that the medical image analysis-clustering method produces accurate segmentations and offers more flexibility than those of equivalent precision. Its free availability, flexibility to deal with non-bone inclusions and limited need for user input give it broad applicability in anthropological, anatomical, and paleontological contexts.

The evolution of the hominin thumb and the influence exerted by the non-dominant hand during stone tool production.

Modern humans possess a highly derived thumb that is substantially stronger and more robust than the fingers. Previous hypotheses concerning the evolution of such traits have focused upon the manipulation of hammerstones during stone tool production and of stone tools during their use. To date there has been no research on the manipulative pressures exerted by the non-dominant (core-holding) hand during stone tool production and its potential influence on the evolutionary history of the thumb. Here we provide the first investigation into the frequencies of digit recruitment and the relative manipulative forces experienced in the non-dominant hand during stone tool production. Eight experienced knappers produced flake cutting tools under four distinct conditions while pressure sensors, secured to the volar pads of the thumb, index and middle fingers of the non-dominant hand, recorded manipulative forces. Results indicate that relative to the fingers, the thumb was recruited significantly more frequently and experienced significantly greater manipulative forces during core repositioning events and the securing of the core during flake detachments. Our results support the hypothesis that the robust thumb anatomy observed in the hominin lineage was selected for, at least in part, as a result of more frequent and greater manipulative pressures acting upon the thumb relative to the fingers on the non-dominant hand during stone tool production.