Recent origin of low trabecular bone density in modern humans

Humans are unique, compared with our closest living relatives (chimpanzees) and early fossil hominins, in having an enlarged body size and lower limb joint surfaces in combination with a relatively gracile skeleton (i.e., lower bone mass for our body size). Some analyses have observed that in at least a few anatomical regions modern humans today appear to have relatively low trabecular density, but little is known about how that density varies throughout the human skeleton and across species or how and when the present trabecular patterns emerged over the course of human evolution. Here, we test the hypotheses that (i) recent modern humans have low trabecular density throughout the upper and lower limbs compared with other primate taxa and (ii) the reduction in trabecular density first occurred in early Homo erectus, consistent with the shift toward a modern human locomotor anatomy, or more recently in concert with diaphyseal gracilization in Holocene humans. We used peripheral quantitative CT and microtomography to measure trabecular bone of limb epiphyses (long bone articular ends) in modern humans and chimpanzees and in fossil hominins attributed to Australopithecus africanus, Paranthropus robustus/early Homo from Swartkrans, Homo neanderthalensis, and early Homo sapiens. Results show that only recent modern humans have low trabecular density throughout the limb joints. Extinct hominins, including pre-Holocene Homo sapiens, retain the high levels seen in nonhuman primates. Thus, the low trabecular density of the recent modern human skeleton evolved late in our evolutionary history, potentially resulting from increased sedentism and reliance on technological and cultural innovations

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 focussed 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 while 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

Track D Social Science, Human Rights and Political Science

Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/138414/1/jia218442.pd

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 ( n=48 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 −75∘ (extension) to +75∘ (flexion). Predicted mean joint load directions were significantly different between knuckle-walking and non-knuckle-walking groups ( p<0.05 ) 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

Relative fibular strength and locomotor behavior in OH 35 and KNM-WT 15000

Relative fibular/tibial strength has been demonstrated to be related to the degree of arboreality/ terrestriality in anthropoid primates. In this study fibular/tibial strength was determined in OH 35, a Homo habilis (or possibly Paranthropus boisei), (1.8 myr) and KNM-WT 15000, a juvenile Homo erectus, (1.5 myr), and was compared to modern humans (n=79), chimpanzees (n=16), gorillas (n=16) and orangutans (n=11). Ontogenetic changes in fibular/tibial strength were also analyzed due to KNM-WT 15000’s juvenile status. Cross-sectional properties were derived from multi-plane radiography and either CT sections of casts (fossils) or external molds (extant). RMA regressions were run on polar second moment of area (J), a measure of torsional and average bending rigidity, of the fibula against that of the tibia for all extant species. Fossils were analyzed using their relative deviations from each regression line, expressed in SEE units. Great apes differed significantly from humans in regression line elevation, with relatively stronger fibulae. OH 35 fell in the center of the great ape distribution, within 1 SEE of each great ape taxon, but 1.9 SEE from humans. KNM-WT 15000 was more than 2 SEE from all great apes and within 0.6 SEE of humans. This was not a result of his age, as fibular/tibial strength slightly decreases with age in humans. OH 35 has some human-like features; however, the relative strength of the two bones aligns the specimen with great apes, suggesting a significant degree of arboreality. KNM-WT 15000 is demonstrated to be fully modern, complimenting other evidence for complete terrestrial bipedality

Relative fibular strength and locomotor behavior in KNM-WT 15000 and OH 35

Relative fibular/tibial strength has been demonstrated to vary with locomotor behavior among anthropoid primates. In this study fibular/tibial strength was determined in KNM-WT 15000, a juvenile Homo erectus individual (1.5 Ma), and in OH 35, a Homo habilis (or possibly Paranthropus boisei) individual (1.8 Ma), and compared to that of adult modern humans (n ¼ 79), chimpanzees (n ¼ 16), gorillas (n ¼ 16) and orangutans (n ¼ 11). Ontogenetic changes in fibular/tibial strength were also analyzed due to KNMWT 15000's juvenile status. Cross-sectional properties at midshaft were derived from multi-plane radiography and external contours, or CT scanning. Comparisons of log-transformed fibular/tibial polar second moment of area and anteroposterior (A-P) and mediolateral (M-L) second moments of area were carried out between extant species. Fossil deviations from each extant taxon's mean proportion were calculated in standard deviation (SD) units for that taxon. Great apes differ significantly from modern humans, with relatively stronger fibulae, particularly in the M-L plane. KNM-WT 15000 is more than 2 SD from all great apes (3 SD in the M-L plane) and within 1 SD of modern humans for almost all variables. This is not a result of its age, as fibular/tibial strength slightly decreases with age (i.e., becomes less like that of great apes) in humans. OH 35 falls within 1 SD of chimpanzees and orangutans for the majority of cross-sectional proportions, but more than 1 SD from humans. KNM-WT 15000 is demonstrated to be fully modern, complimenting other indications of complete terrestrial bipedality and possibly showing adaptations for endurance running. OH 35 has some human-like features; however, the relative strength of the two bones aligns the specimen with great apes, consistent with a significant degree of arboreality, in particular, vertical climbing

Recent origin of low trabecular bone density in modern humans

Humans are unique, compared with our closest living relatives (chimpanzees) and early fossil hominins, in having an enlarged body size and lower limb joint surfaces in combination with a relatively gracile skeleton (i.e., lower bone mass for our body size). Some analyses have observed that in at least a few anatomical regions modern humans today appear to have relatively low trabecular density, but little is known about how that density varies throughout the human skeleton and across species or how and when the present trabecular patterns emerged over the course of human evolution. Here, we test the hypotheses that (i) recent modern humans have low trabecular density throughout the upper and lower limbs compared with other primate taxa and (ii) the reduction in trabecular density first occurred in early Homo erectus, consistent with the shift toward a modern human locomotor anatomy, or more recently in concert with diaphyseal gracilization in Holocene humans. We used peripheral quantitative CT and microtomography to measure trabecular bone of limb epiphyses (long bone articular ends) in modern humans and chimpanzees and in fossil hominins attributed to Australopithecus africanus, Paranthropus robustus/early Homo from Swartkrans, Homo neanderthalensis, and early Homo sapiens. Results show that only recent modern humans have low trabecular density throughout the limb joints. Extinct hominins, including pre-Holocene Homo sapiens, retain the high levels seen in nonhuman primates. Thus, the low trabecular density of the recent modern human skeleton evolved late in our evolutionary history, potentially resulting from increased sedentism and reliance on technological and cultural innovations

Cross-sectional properties of the humeral diaphysis of Paranthropus boisei: Implications for upper limb function

A ∼1.52 Ma adult upper limb skeleton of Paranthropus boisei (KNM-ER 47000) recovered from the Koobi Fora Formation, Kenya (FwJj14E, Area 1A) includes most of the distal half of a right humerus (designated KNM-ER 47000B). Natural transverse fractures through the diaphysis of KNM-ER 470000B provide unobstructed views of cortical bone at two sections typically used for analyzing cross-sectional properties of hominids (i.e., 35% and 50% of humerus length from the distal end). Here we assess cross-sectional properties of KNM-ER 47000B and two other P. boisei humeri (OH 80-10, KNM-ER 739). Cross-sectional properties for P. boisei associated with bending/torsional strength (section moduli) and relative cortical thickness (%CA; percent cortical area) are compared to those reported for nonhuman hominids, AL 288-1 (Australopithecus afarensis), and multiple species of fossil and modern Homo. Polar section moduli (Zp) are assessed relative to a mechanically relevant measure of body size (i.e., the product of mass [M] and humerus length [HL]). At both diaphyseal sections, P. boisei exhibits %CA that is high among extant hominids (both human and nonhuman) and similar to that observed among specimens of Pleistocene Homo. High values for Zp relative to size (M × HL) indicate that P. boisei had humeral bending strength greater than that of modern humans and Neanderthals and similar to that of great apes, A. afarensis, and Homo habilis. Such high humeral strength is consistent with other skeletal features of P. boisei (reviewed here) that suggest routine use of powerful upper limbs for arboreal climbing

Humeral anatomy of the KNM-ER 47000 upper limb skeleton from Ileret, Kenya: Implications for taxonomic identification

KNM-ER 47000 is a fossil hominin upper limb skeleton from the Koobi Fora Formation, Kenya (FwJj14E, Area 1A) that includes portions of the scapula, humerus, ulna, and hand. Dated to ∼1.52 Ma, the skeleton could potentially belong to one of multiple hominin species that have been documented in the Turkana Basin during this time, including Homo habilis, Homo erectus, and Paranthropus boisei. Although the skeleton lacks associated craniodental material, the partial humerus (described here) preserves anatomical regions (i.e., distal diaphysis, elbow joint) that are informative for taxonomic identification among early Pleistocene hominins. In this study, we analyze distal diaphyseal morphology and the shape of the elbow region to determine whether KNM-ER 47000 can be confidently attributed to a particular species. The morphology of the KNM-ER 47000 humerus (designated KNM-ER 47000B) is compared to that of other early Pleistocene hominin fossil humeri via the application of multivariate ordination techniques to both two-dimensional landmark data (diaphysis) and scale-free linear shape data (elbow). Distance metrics reflecting shape dissimilarity between KNM-ER 47000B and other fossils (and species average shapes) are assessed in the context of intraspecific variation within modern hominid species (Homo sapiens, Pan troglodytes, Gorilla gorilla, Pongo pygmaeus). Our comparative analyses strongly support attribution of KNM-ER 47000 to P. boisei. Compared to four other partial skeletons that have (justifiably or not) been attributed to P. boisei, KNM-ER 47000 provides the most complete picture of upper limb anatomy in a single individual. The taxonomic identification of KNM-ER 47000 makes the skeleton an important resource for testing future hypotheses related to P. boisei upper limb function and the taxonomy of isolated early Pleistocene hominin remains

Scapular anatomy of Paranthropus boisei from Ileret, Kenya

KNM-ER 47000A is a new 1.52 Ma hominin scapular fossil belonging to an associated partial skeleton from the Koobi Fora Formation, Kenya (FwJj14E, Area 1A). This fossil effectively doubles the record of Early Pleistocene scapulae from East Africa, with KNM-WT 15000 (early African Homo erectus) preserving the only other known scapula to date. KNM-ER 47000A consists of a complete glenoid cavity preserving a portion of the scapular spine and neck, the proximal half of the acromion, and a majority of the axillary border. A sufficient amount of anatomy is preserved to compare KNM-ER 47000A with scapulae of several Australopithecus species, extinct Homo, and living hominoids. The glenohumeral joint of KNM-ER 47000A is more laterally oriented than those of great apes and Australopithecus, aligning it closely with KNM-WT 15000 and modern humans. While this morphology does not imply a strong commitment to arboreality, its scapular spine is obliquely oriented—as in gorillas and some Australopithecus fossils—particularly when compared to the more horizontal orientation seen in KNM-WT 15000 and modern humans. Such a spine orientation suggests a narrow yet long infraspinous region, a feature that has been attributed to suspensory taxa. Accordingly, the morphology of KNM-ER 47000A presents conflicting behavioral implications. Nonetheless, a multivariate consideration of the available scapular traits aligns KNM-ER 47000A and Australopithecus with great apes, whereas KNM-WT 15000 resembles modern humans. The scapular morphology of KNM-ER 47000A is unique among fossil and extant hominoids and its morphological differences from KNM-WT 15000 strengthen the attribution of KNM-ER 47000 to Paranthropus boisei as opposed to early Homo. As the first evidence of scapular morphology in P. boisei, KNM-ER 47000A provides important new information on variation in hominin shoulder and upper limb anatomy from this critical period of hominin evolutionary history