Technical note: Does scan resolution or downsampling impact the analysis of trabecular bone architecture?

The “gold standard” for the assessment of trabecular bone structure is high-resolution micro-CT. In this technical note, we test the influence of initial scan resolution and post hoc downsampling on the quantitative and qualitative analysis of trabecular bone in a Gorilla tibia. We analyzed trabecular morphology in the right distal tibia of one Gorilla gorilla individual to investigate the impact of variation in voxel size on measured trabecular variables. For each version of the micro-CT volume, trabecular bone was segmented using the medical image analysis method. Holistic morphometric analysis was then used to analyze bone volume (BV/TV), anisotropy (DA), trabecular thickness (Tb.Th), spacing (Tb.Sp), and number (Tb.N). Increasing voxel size during initial scanning was found to have a strong impact on DA and Tb.Th measures, while BV/TV, Tb.Sp, and Tb.N were found to be less sensitive to variations in initial scan resolution. All tested parameters were not substantially influenced by downsampling up to 90 μm resolution. Color maps of BV/TV and DA also retained their distribution up to 90 μm. This study is the first to examine the effect of variation in micro-CT voxel size on the analysis of trabecular bone structure using whole epiphysis approaches. Our results indicate that microstructural variables may be measured for most trabecular parameters up to a voxel size of 90 μm for both scan and downsampled resolutions. Moreover, if only BV/TV, Tb.Sp or Tb.N is measured, even larger voxel sizes might be used without substantially affecting the results

Trabecular bone structure correlates with hand posture and use in hominoids

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

Cortical bone mapping: An application to hand and foot bones in hominoids

Bone form reflects both the genetic profile and behavioural history of an individual. As cortical bone is able to remodel in response to mechanical stimuli, interspecific differences in cortical bone thickness may relate to loading during locomotion or manual behaviours during object manipulation. Here, we test the application of a novel method of cortical bone mapping to the third metacarpal (Mc3) and talus of Pan, Pongo, and Homo. This method of analysis allows measurement of cortical thickness throughout the bone, and as such is applicable to elements with complex morphology. In addition, it allows for registration of each specimen to a canonical surface, and identifies regions where cortical thickness differs significantly between groups. Cortical bone mapping has potential for application to palaeoanthropological studies; however, due to the complexity of correctly registering homologous regions across varied morphology, further methodological development would be advantageous

Locomotion in Homo floresiensis: reconstructing foot use from the internal bone structure of the metatarsals of LB1

The enigmatic Homo floresiensis displays a unique combination of cranial and post-cranial morphology [1-3], distinguishing it from other species of the genus Homo. Although its skeletal anatomy shows clear adaptations for terrestrial bipedalism, it also retains a suite of features conducive to arboreal behaviours. Thus, exactly how the locomotor behaviours of H. floresiensis compare with those of other hominins remains an important research question. The foot of the holotype (LB1) is long relative to its femoral length, has a longer forefoot than hindfoot, long phalanges relative to the non-hallucial metatarsals (Mts), and a short Mt1 relative to the other Mts [3]. However, it also possesses a human-like Mt head morphology and relative robusticity pattern [2-3]. Here, we assess the internal morphology of the Mts of LB1 to further assess foot functional morphology and locomotor kinematics in H. floresiensis. Using high resolution micro-CT scans of the Mts of LB1 and a comparative sample of Homo sapiens (N=10), Pan troglodytes (N=15), Pan paniscus (N=15), Gorilla spp. (N=10) and Pongo spp. (N=9), we conducted a cross-sectional geometric analysis at mid-shaft and analysis of trabecular bone distribution in the Mt head. As the head was only fully preserved for the right Mt5 of LB1, trabecular analysis was limited to this element.Cross-sectional geometry of the Mts at mid-shaft distinguishes between ape-like and human-like biomechanics, with greater loading of the Mt2 and Mt3 in apes compared with more lateral loading in humans [4]. The Mts of LB1 are internally robust, having a high cross-sectional area relative to bone length. Results show that the relative strength of the Mts, based on the internal structure, differs from the previously reported human-like pattern, which was based on external measurements of midshaft circumference [2-3]. We find that, after scaling by total bone length, the robusticity pattern for the left Mts of LB1 is 1>2>5>3>4 for CSA and Z, and 1>5>2>4>3 for J. Although there is some variation among humans, in general the Mt3 and Mt2 have lower measures of robusticity than the Mt4 and Mt5 [4]. In LB1, the Mt2 is consistently more robust than is expected in humans, with the pattern being 1>2/5>3/4 compared to 1>4/5>2/3 in humans. The distribution of trabecular bone in the Mt5 head distinguishes between locomotor groups. In H. sapiens, where the foot is loaded in dorsiflexion there is a dorsal concentration of bone, which is asymmetric in extending dorsomedially. In African apes, where the toes are positioned dorsally during knuckle-walking and disto-plantarly during climbing (depending on substrate size) the distribution of trabecular bone extends dorsally to plantarly on the metatarsal head. In Pongo, trabecular bone is distributed distally and plantarly reflecting a grasping foot. The distribution of trabecular bone in the Mt5 of LB1 is located dorsally and distally but does not extend plantarly. This distribution pattern differs from humans in being centrally located, rather than medially, and in extending further distally. This suggests that the metatarsophalangeal joint in LB1 was loaded in a more a neutral position than in humans.Together, the results suggest that loading of the foot of H. floresiensis differed from modern humans. First, the distribution of load across the foot was likely higher in the Mt2, a feature that could relate to higher loading of the second ray in a foot with a relatively short first ray. Secondly, the trabecular pattern suggests loading of the Mt5 head more distally than in humans, and with less asymmetric loading. This differing position of the metatarsophalangeal joint could be related to the long, curved phalanges of LB1. Future research exploring whole-bone cortical and trabecular structure of the metatarsals will shed new light on the kinematics of locomotion in H. floresiensis

Structural organization of the cranial vault in Neanderthals and present-day humans: Can endocranial shape characteristics be explained by vault thickness?

In studies of hominin brain evolution the shape of the interior braincase (or endocranium) is often used to infer cortical organization. However, the braincase is not only shaped by brain, but also by the interplay of evolutionary and developmental changes of facial size and shape, the development of soft tissues, and neurocranial bone thickness. It therefore remains unclear to what extent the well-documented endocranial shape differences between the more globular present-day humans and the ..

Covariation of endocranial shape and cranial vault thickness in present-day humans and Neandertals

A better understanding of the patterns of brain growth and development in extinct but also in extant great apes informs discussions about the evolution of cognitive abilities and behaviors in the human lineage. In fossils, brain shape and its cortical organization can usually only be inferred from the shape of the endocranial cavity and from the brain imprints in the cranial bone. However, the shape of the braincase results from different mechanisms: the patterns of brain growth and development [1], the evolutionary and developmental changes affecting facial size and shape [2], the development of soft tissues [3] and the pattern of growth and development of the entire neurocranium [4]. It has been shown that present-day humans and Neandertals achieved similar endocranial capacities via different developmental pathways, suggesting underlying differences in the tempo and mode of brain growth and development [5].Here, we assess the influence of bone thickness on endocranial shape. Specifically, we examined to what extent differences in bone thickness of the cranial vault can explain the endocranial shape differences between present-day humans and Neanderthals. Our sample comprises 75 computed tomographic scans of adult present-day humans and 6 Neandertals. Endocranial shape was measured using 935 landmarks and semilandmarks and analyzed after a Procrustes registration. Cranial vault thickness (CVT) was computed from 472 landmarks and semilandmarks as the distance between the endocranial and the ectocranial surfaces. We first quantified CVT standardized for the size. Second, we explored the covariation between endocranial shape and the cranial vaultthickness using a two-blocks partial least-squares analysis (PLS). Last, we established a predictive regression model of endocranial shape using cranial thickness as an input variable and endocranial shape as an output. We built this model from the present-day human sample only, and measured the fitness of the model in explaining the endocranial shape that characterizes the Neandertal individuals.Our results demonstrate that even though Neandertals tend to have a thicker cranial vault, these values are still comprised within the range of variation of present-day humans. The first dimension of covariation in the PLS analysis was driven by variation within present-day humans. Individuals displaying elongated shapes showed an overall thinner CVT, while those with rounded vaults had a thicker cranial vault. Scores along the second axis of covariation displayed a shift between present-day humans and Neandertals. Along this axis, present-day humans were characterized by bulged, vertically stretched and thin parietal bones, while Neandertals displayed vertically shorter, wider and thicker parietal bones. Finally, our regression model failed to predict the Neandertal endocranial shape from their CVT values. Altogether, our results suggest that endocranial shape differences between present-day humans and Neandertals are not likely to be explained by their CVT, and strengthen the hypothesis of different brain shapes between these two human groups

Cortical bone architecture of hominid intermediate phalanges reveals functional signals of locomotion and manipulation

Objectives: Reconstruction of fossil hominin manual behaviors often relies on comparative analyses of extant hominid hands to understand the relationship between hand use and skeletal morphology. In this context, the intermediate phalanges remain understudied. Thus, here we investigate cortical bone morphology of the intermediate phalanges of extant hominids and compare it to the cortical structure of the proximal phalanges, to investigate the relationship between cortical bone structure and inferred loading during manual behaviors. Materials and Methods: Using micro‐CT data, we analyze cortical bone structure of the intermediate phalangeal shaft of digits 2–5 in Pongo pygmaeus (n = 6 individuals), Gorilla gorilla (n = 22), Pan spp. (n = 23), and Homo sapiens (n = 23). The R package morphomap is used to study cortical bone distribution, cortical thickness and cross‐sectional properties within and across taxa. Results: Non‐human great apes generally have thick cortical bone on the palmar shaft, with Pongo only having thick cortex on the peaks of the flexor sheath ridges, while African apes have thick cortex along the entire flexor sheath ridge and proximal to the trochlea. Humans are distinct in having thicker dorsal shaft cortex as well as thick cortex at the disto‐palmar region of the shaft. Discussion: Variation in cortical bone distribution and properties of the intermediate phalanges is consistent with differences in locomotor and manipulative behaviors in extant great apes. Comparisons between the intermediate and proximal phalanges reveals similar patterns of cortical bone distribution within each taxon but with potentially greater load experienced by the proximal phalanges, even in knuckle‐walking African apes. This study provides a comparative context for the reconstruction of habitual hand use in fossil hominins and hominids

Cortical bone distribution of the proximal phalanges in great apes : implications for reconstructing manual behaviours

DATA AVAILABILITY STATEMENT : Copies of all scans are curated by the relevant curatorial institutions that are responsible for the original specimens and access can be requested through each institution. The authors confirm that the data supporting the findings of this study are available from the corresponding author upon reasonable request.Primate fingers are typically in direct contact with the environment during both locomotion and manipulation, and aspects of external phalangeal morphology are known to reflect differences in hand use. Since bone is a living tissue that can adapt in response to loading through life, the internal bone architecture of the manual phalanges should also reflect differences in manual behaviours. Here, we use the R package Morphomap to analyse high-resolution microCT scans of hominid proximal phalanges of digits 2–5 to determine whether cortical bone structure reflects variation in manual behaviours between bipedal (Homo), knuckle-walking (Gorilla, Pan) and suspensory (Pongo) taxa. We test the hypothesis that relative cortical bone distribution patterns and cross-sectional geometric properties will differ both among extant great apes and across the four digits due to locomotor and postural differences. Results indicate that cortical bone structure reflects the varied hand postures employed by each taxon. The phalangeal cortices of Pongo are significantly thinner and have weaker cross-sectional properties relative to the African apes, yet thick cortical bone under their flexor sheath ridges corresponds with predicted loading during flexed finger grips. Knuckle-walking African apes have even thicker cortical bone under the flexor sheath ridges, as well as in the region proximal to the trochlea, but Pan also has thicker diaphyseal cortices than Gorilla. Humans display a distinct pattern of distodorsal thickening, as well as relatively thin cortices, which may reflect the lack of phalangeal curvature combined with frequent use of flexed fingered hand grips during manipulation. Within each taxon, digits 2–5 have a similar cortical distribution in Pongo, Gorilla and, unexpectedly, Homo, which suggest similar loading of all fingers during habitual locomotion or hand use. In Pan, however, cortical thickness differs between the fingers, potentially reflecting differential loading during knuckle-walking. Inter- and intra-generic variation in phalangeal cortical bone structure reflects differences in manual behaviours, offering a comparative framework for reconstructing hand use in fossil hominins.H2020 European Research Council.https://onlinelibrary.wiley.com/journal/14697580Anatom

Cortical bone architecture of hominid intermediate phalanges reveals functional signals of locomotion and manipulation

DATA AVAILABILITY STATEMENT : Copies of all scans are curated by the relevant curatorial institutions that are responsible for the original specimens and access can be requested through each institution. The authors confirm that the data supporting the findings of this study are available from the corresponding author upon reasonable request.OBJECTIVES : Reconstruction of fossil hominin manual behaviors often relies on comparative analyses of extant hominid hands to understand the relationship between hand use and skeletal morphology. In this context, the intermediate phalanges remain understudied. Thus, here we investigate cortical bone morphology of the intermediate phalanges of extant hominids and compare it to the cortical structure of the proximal phalanges, to investigate the relationship between cortical bone structure and inferred loading during manual behaviors. MATERIALS AND METHODS : Using micro-CT data, we analyze cortical bone structure of the intermediate phalangeal shaft of digits 2–5 in Pongo pygmaeus (n = 6 individuals), Gorilla gorilla (n = 22), Pan spp. (n = 23), and Homo sapiens (n = 23). The R package morphomap is used to study cortical bone distribution, cortical thickness and cross-sectional properties within and across taxa. RESULTS : Non-human great apes generally have thick cortical bone on the palmar shaft, with Pongo only having thick cortex on the peaks of the flexor sheath ridges, while African apes have thick cortex along the entire flexor sheath ridge and proximal to the trochlea. Humans are distinct in having thicker dorsal shaft cortex as well as thick cortex at the disto-palmar region of the shaft. DISCUSSION : Variation in cortical bone distribution and properties of the intermediate phalanges is consistent with differences in locomotor and manipulative behaviors in extant great apes. Comparisons between the intermediate and proximal phalanges reveals similar patterns of cortical bone distribution within each taxon but with potentially greater load experienced by the proximal phalanges, even in knuckle-walking African apes. This study provides a comparative context for the reconstruction of habitual hand use in fossil hominins and hominids.H2020 European Research Council; HORIZON EUROPE Marie Sklodowska-Curie Actions.http://wileyonlinelibrary.com/journal/ajpahj2024AnatomySDG-03:Good heatlh and well-bein

Cortical bone distribution of the proximal phalanges in great apes: implications for reconstructing manual behaviours

Primate fingers are typically in direct contact with the environment during both locomotion and manipulation, and aspects of external phalangeal morphology are known to reflect differences in hand use. Since bone is a living tissue that can adapt in response to loading through life, the internal bone architecture of the manual phalanges should also reflect differences in manual behaviours. Here, we use the R package Morphomap to analyse high‐resolution microCT scans of hominid proximal phalanges of digits 2–5 to determine whether cortical bone structure reflects variation in manual behaviours between bipedal (Homo), knuckle‐walking (Gorilla, Pan) and suspensory (Pongo) taxa. We test the hypothesis that relative cortical bone distribution patterns and cross‐sectional geometric properties will differ both among extant great apes and across the four digits due to locomotor and postural differences. Results indicate that cortical bone structure reflects the varied hand postures employed by each taxon. The phalangeal cortices of Pongo are significantly thinner and have weaker cross‐sectional properties relative to the African apes, yet thick cortical bone under their flexor sheath ridges corresponds with predicted loading during flexed finger grips. Knuckle‐walking African apes have even thicker cortical bone under the flexor sheath ridges, as well as in the region proximal to the trochlea, but Pan also has thicker diaphyseal cortices than Gorilla. Humans display a distinct pattern of distodorsal thickening, as well as relatively thin cortices, which may reflect the lack of phalangeal curvature combined with frequent use of flexed fingered hand grips during manipulation. Within each taxon, digits 2–5 have a similar cortical distribution in Pongo, Gorilla and, unexpectedly, Homo, which suggest similar loading of all fingers during habitual locomotion or hand use. In Pan, however, cortical thickness differs between the fingers, potentially reflecting differential loading during knuckle‐walking. Inter‐ and intra‐generic variation in phalangeal cortical bone structure reflects differences in manual behaviours, offering a comparative framework for reconstructing hand use in fossil hominins