The effects of the industrial transition on lower limb bone structure: A comparison of the inhabitants of Pecos Pueblo and present-day Indigenous peoples of New Mexico.

OBJECTIVES: Comparisons between Indigenous peoples over time and within a particular geographic region can shed light on the impact of environmental transitions on the skeleton, including relative bone strength, sexual dimorphism, and age-related changes. Here we compare long bone structural properties of the inhabitants of the late prehistoric-early historic Pecos Pueblo with those of present-day Indigenous individuals from New Mexico. MATERIALS AND METHODS: Femora and tibiae of 126 adults from Pecos Pueblo and 226 present-day adults were included in the study. Cross-sectional diaphyseal properties-areas and second moments of area-were obtained from past studies of the Pecos Pueblo skeletal sample, and from computed tomography scans of recently deceased individuals in the present-day sample. RESULTS: Femora and tibiae from Pecos individuals are stronger relative to body size than those of present-day Indigenous individuals. Present-day individuals are taller but not wider, and this body shape difference affects cross-sectional shape, more strongly proximally. The tibia shows anteroposterior strengthening among Pecos individuals, especially among males. Sexual dimorphism in midshaft bone shape is stronger within the Pecos Pueblo sample. With aging, Pecos individuals show more medullary expansion but also more subperiosteal expansion than present-day individuals, maintaining bone strength despite cortical thinning. DISCUSSION: Higher activity levels, carried out over rough terrain and throughout adult life, likely explain the relatively stronger lower limb bones of the Pecos individuals, as well as their greater subperiosteal expansion with aging. Greater sexual dimorphism in bone structure among Pecos individuals potentially reflects greater gender-based differences in behavioral patterns.

Changes in diaphyseal cross-sectional properties with age in macaques.

OBJECTIVES: The present study seeks to quantify changes in long bone cross-sectional properties in a colony of semi-free-ranging rhesus macaques and compare observed aging patterns to those of other primates, including humans. METHODS: Peripheral quantitative computed tomography was used to obtain midshaft cross sections of the femora, tibiae, humeri, and radii of 115 macaque specimens ranging from 7 to 31 years of age. Linear regressions of cross-sectional properties on age were analyzed. An analysis of covariance was conducted to quantify differences in rates of change between males and females. RESULTS: Results show that medullary area increases while cortical area decreases with age in both sexes. The polar section modulus and the polar strain-strength index, measuring torsional and bending strength, show no decline in most sections but decrease significantly with age in the hindlimb elements of female macaques. Volumetric bone mineral density (vBMD) also decreases with age in both male and female macaques; however, the cumulative change in vBMD over the adult lifespan is relatively small, equivalent to a less than 10% decrease in material strength. An analysis of covariance shows no differences between males and females in the rate of change of properties with age. DISCUSSION: Overall, this study shows that there are some similarities in the skeletal aging patterns of macaques and those of other primates, including humans, but also some differences, with greater losses of bone found in human females as a result of an extended post-reproductive period that is generally not found among wild or semi-wild macaques.

Effects of the energy balance transition on bone mass and strength.

Chronic positive energy balance has surged among societies worldwide due to increasing dietary energy intake and decreasing physical activity, a phenomenon called the energy balance transition. Here, we investigate the effects of this transition on bone mass and strength. We focus on the Indigenous peoples of New Mexico in the United States, a rare case of a group for which data can be compared between individuals living before and after the start of the transition. We show that since the transition began, bone strength in the leg has markedly decreased, even though bone mass has apparently increased. Decreased bone strength, coupled with a high prevalence of obesity, has resulted in many people today having weaker bones that must sustain excessively heavy loads, potentially heightening their risk of a bone fracture. These findings may provide insight into more widespread upward trends in bone fragility and fracture risk among societies undergoing the energy balance transition.

The estimation and evolution of hominin body mass.

Body mass is a critical variable in many hominin evolutionary studies, with implications for reconstructing relative brain size, diet, locomotion, subsistence strategy, and social organization. We review methods that have been proposed for estimating body mass from true and trace fossils, consider their applicability in different contexts, and the appropriateness of different modern reference samples. Recently developed techniques based on a wider range of modern populations hold promise for providing more accurate estimates in earlier hominins, although uncertainties remain, particularly in non-Homo taxa. When these methods are applied to almost 300 Late Miocene through Late Pleistocene specimens, the resulting body mass estimates fall within a 25-60 kg range for early non-Homo taxa, increase in early Homo to about 50-90 kg, then remain constant until the Terminal Pleistocene, when they decline.

Adapting in the Arctic II: Upper limb diaphyseal robusticity and habitual activity in Late Holocene hunter-gatherers from Alaska.

OBJECTIVES: This study compares humeral diaphyseal robusticity and asymmetry between Late Holocene hunter-gatherers from Alaska with the goal of reconstructing habitual activity in relation to culture and environment. MATERIALS AND METHODS: Ancestral remains from four geographic regions of Alaska were divided into five site groups defined by subsistence strategies and technology: Aleutian Islands, Coastal Bay, Far North Coastal, Inland/Riverine, and Tikeraq. Mid-distal humeral diaphyseal robusticity was quantified using cross-sectional geometric properties standardized by estimated body mass and bone length. RESULTS: Humeral strength and bilateral asymmetry were greatest in Aleutian Island males, moderate in Far North Coastal and Tikeraq males, and reduced in Inland/Riverine males. Left-biased directional asymmetry and reduced humeral strength were found in Coastal Bay males. Aleutian Island males had relatively mediolaterally strengthened humeri compared with other groups. Aleutian Island females had elevated humeral strength, while humeral asymmetry among females was moderate and did not vary between groups. Humeri were relatively round among Aleutian Island and Tikeraq females and anteroposteriorly (A-P) strengthened among Coastal Bay, Far North Coastal, and Inland/Riverine females. CONCLUSIONS: These results suggest elevated humeral strength and asymmetry in males that engaged in rowing and unimanual projectile hunting, while reduced humeral strength and asymmetry may reflect bow-and-arrow or ensnarement technologies. Left-biased humeral asymmetry may be associated with net-fishing. Humeral strength and asymmetry are consistent with select instances of unimanual projectile hunting in females, while differences in humeral A-P/mediolateral strength may reflect variation in butchery and processing of prey versus rowing and throwing behaviors.

Long-term trends in human body size track regional variation in subsistence transitions and growth acceleration linked to dairying.

Evidence for a reduction in stature between Mesolithic foragers and Neolithic farmers has been interpreted as reflective of declines in health, however, our current understanding of this trend fails to account for the complexity of cultural and dietary transitions or the possible causes of phenotypic change. The agricultural transition was extended in primary centers of domestication and abrupt in regions characterized by demic diffusion. In regions such as Northern Europe where foreign domesticates were difficult to establish, there is strong evidence for natural selection for lactase persistence in relation to dairying. We employ broad-scale analyses of diachronic variation in stature and body mass in the Levant, Europe, the Nile Valley, South Asia, and China, to test three hypotheses about the timing of subsistence shifts and human body size, that: 1) the adoption of agriculture led to a decrease in stature, 2) there were different trajectories in regions of in situ domestication or cultural diffusion of agriculture; and 3) increases in stature and body mass are observed in regions with evidence for selection for lactase persistence. Our results demonstrate that 1) decreases in stature preceded the origins of agriculture in some regions; 2) the Levant and China, regions of in situ domestication of species and an extended period of mixed foraging and agricultural subsistence, had stable stature and body mass over time; and 3) stature and body mass increases in Central and Northern Europe coincide with the timing of selective sweeps for lactase persistence, providing support for the "Lactase Growth Hypothesis."

Two Late Pleistocene human femora from Trinil, Indonesia: Implications for body size and behavior in Southeast Asia.

Late Pleistocene hominin postcranial specimens from Southeast Asia are relatively rare. Here we describe and place into temporal and geographic context two partial femora from the site of Trinil, Indonesia, which are dated stratigraphically and via Uranium-series direct dating to ca. 37-32 ka. The specimens, designated Trinil 9 and 10, include most of the diaphysis, with Trinil 9 being much better preserved. Microcomputed tomography is used to determine cross-sectional diaphyseal properties, with an emphasis on midshaft anteroposterior to mediolateral bending rigidity (Ix/Iy), which has been shown to relate to both body shape and activity level in modern humans. The body mass of Trinil 9 is estimated from cortical area and reconstructed length using new equations based on a Pleistocene reference sample. Comparisons are carried out with a large sample of Pleistocene and Holocene East Asian, African, and European/West Asian femora. Our results show that Trinil 9 has a high Ix/Iy ratio, most consistent with a relatively narrow-bodied male from a mobile hunting-gathering population. It has an estimated body mass of 55.4 kg and a stature of 156 cm, which are small relative to Late Pleistocene males worldwide, but larger than the penecontemporaneous Deep Skull femur from Niah Cave, Malaysia, which is very likely female. This suggests the presence of small-bodied active hunter-gatherers in Southeast Asia during the later Late Pleistocene. Trinil 9 also contrasts strongly in morphology with earlier partial femora from Trinil dating to the late Early-early Middle Pleistocene (Femora II-V), and to a lesser extent with the well-known complete Femur I, most likely dating to the terminal Middle-early Late Pleistocene. Temporal changes in morphology among femoral specimens from Trinil parallel those observed in Homo throughout the Old World during the Pleistocene and document these differences within a single site.

Body proportions and environmental adaptation in gorillas.

OBJECTIVES: Limb length and trunk proportions are determined in a large, taxonomically and environmentally diverse sample of gorillas and related to variation in locomotion, climate, altitude, and diet. MATERIALS AND METHODS: The sample includes 299 gorilla skeletons, 115 of which are infants and juveniles, distributed between western lowland (G. gorilla gorilla), low and high elevation grauer (G. beringei graueri), and Virunga mountain gorillas (G. b. beringei). Limb bone and vertebral column lengths scaled to body mass are compared between subgroups by age group. RESULTS: All G. beringei have relatively short 3rd metapodials and manual proximal phalanges compared to G. gorilla, and this difference is apparent in infancy. All G. beringei also have shortened total limb lengths relative to either body mass or vertebral column length, although patterns of variation in individual skeletal elements are more complex, and infants do not display the same patterns as adults. Mountain gorillas have relatively long clavicles, present in infancy, and a relatively long thoracic (but not lumbosacral) vertebral column. DISCUSSION: A variety of environmental factors likely contributed to observed patterns of morphological variation among extant gorillas. We interpret the short hand and foot bones of all G. beringei as genetic adaptations to greater terrestriality in the last common ancestor of G. beringei; variation in other limb lengths to climatic adaptation, both genetic and developmental; and the larger thorax of G. b. beringei to adaptation to reduced oxygen pressure at high altitudes, again as a product of both genetic differences and environmental influences during development.

Scaling and relative size of the human, nonhuman ape, and baboon calcaneus.

Among human and nonhuman apes, calcaneal morphology exhibits significant variation that has been related to locomotor behavior. Due to its role in weight-bearing, however, both body size and locomotion may impact calcaneal morphology. Determining how calcaneal morphologies vary as a function of body size is thus vital to understanding calcaneal functional adaptation. Here, we study calcaneus allometry and relative size in humans (n = 120) and nonhuman primates (n = 278), analyzing these relationships in light of known locomotor behaviors. Twelve linear measures and three articular facet surface areas were collected on calcaneus surface models. Body mass was estimated using femoral head superoinferior breadth. Relationships between calcaneal dimensions and estimated body mass were analyzed across the sample using phylogenetic least squares regression analyses (PGLS). Differences between humans and pooled nonhuman primates were tested using RMA ANCOVAs. Among (and within) genera residual differences from both PGLS regressions and isometry were analyzed using ANOVAs with post hoc multiple comparison tests. The relationships between all but two calcaneus dimensions and estimated body mass exhibit phylogenetic signal at the smallest taxonomic scale. This signal disappears when reanalyzed at the genus level. Calcaneal morphology varies relative to both body size and locomotor behavior. Humans have larger calcanei for estimated body mass relative to nonhuman primates as a potential adaptation for bipedalism. More terrestrial taxa exhibit longer calcaneal tubers for body mass, increasing the triceps surae lever arm. Among nonhuman great apes, more arboreal taxa have larger cuboid facet surface areas for body mass, increasing calcaneocuboid mobility.

Calcaneal shape variation in humans, nonhuman primates, and early hominins.

The foot has played a prominent role in evaluating early hominin locomotion. The calcaneus, in particular, plays an important role in weight-bearing. Although the calcanei of early hominins have been previously scrutinized, a three-dimensional analysis of the entire calcaneal shape has not been conducted. Here, we investigate the relationship between external calcaneal shape and locomotion in modern Homo sapiens (n = 130), Gorilla (n = 86), Pan (n = 112), Pongo (n = 31), Papio (n = 28), and hylobatids (Hylobates, Symphalangus; n = 32). We use these results to place the calcanei attributed to Australopithecus sediba, A. africanus, A. afarensis, H. naledi, and Homo habilis/Paranthropus boisei into a locomotor context. Calcanei were scanned using either surface scanning or micro-CT and their external shape analyzed using a three-dimensional geometric morphometric sliding semilandmark analysis. Blomberg's K statistic was used to estimate phylogenetic signal in the shape data. Shape variation was summarized using a principal components analysis. Procrustes distances between all taxa as well as distances between each fossil and the average of each taxon were calculated. Blomberg's K statistic was small (K = 0.1651), indicating weak phylogenetic effects, suggesting variation is driven by factors other than phylogeny (e.g., locomotion or body size). Modern humans have a large calcaneus relative to body size and display a uniquely convex cuboid facet, facilitating a rigid midfoot for bipedalism. More arboreal great apes display relatively deeper cuboid facet pivot regions for increased midfoot mobility. Australopithecus afarensis demonstrates the most human-like calcaneus, consistent with obligate bipedalism. Homo naledi is primarily modern human-like, but with some intermediate traits, suggesting a different form of bipedalism than modern humans. Australopithecus africanus, A. sediba, and H. habilis/P. boisei calcanei all possess unique combinations of human and nonhuman ape-like morphologies, suggesting a combination of bipedal and arboreal behaviors.

Body mass estimation from footprint size in hominins.

Although many studies relating stature to foot length have been carried out, the relationship between foot size and body mass remains poorly understood. Here we investigate this relationship in 193 adult and 50 juvenile habitually unshod/minimally shod individuals from five different populations-Machiguenga, Daasanach, Pumé, Hadzabe, and Samoans-varying greatly in body size and shape. Body mass is highly correlated with foot size, and can be predicted from foot area (maximum length × breadth) in the combined sample with an average error of about 10%. However, comparisons among populations indicate that body shape, as represented by the body mass index (BMI), has a significant effect on foot size proportions, with higher BMI samples exhibiting relatively smaller feet. Thus, we also derive equations for estimating body mass from both foot size and BMI, with BMI in footprint samples taken as an average value for a taxon or population, estimated independently from skeletal remains. Techniques are also developed for estimating body mass in juveniles, who have relatively larger feet than adults, and for converting between foot and footprint size. Sample applications are given for five Pliocene through Holocene hominin footprint samples from Laetoli (Australopithecus afarensis), Ileret (probable Homo erectus), Happisburgh (possible Homo antecessor), Le Rozel (archaic Homo sapiens), and Barcin Höyük (H. sapiens). Body mass estimates for Homo footprint samples appear reasonable when compared to skeletal estimates for related samples. However, estimates for the Laetoli footprint sample using the new formulae appear to be too high when compared to skeletal estimates for A. afarensis. Based on the proportions of A.L. 288-1, this is apparently a result of relatively large feet in this taxon. A different method using a ratio between body mass and foot area in A.L. 288-1 provides estimates more concordant with skeletal estimates and should be used for A. afarensis.

Adapting in the Arctic: Habitual activity and landscape interaction in Late Holocene hunter-gatherers from Alaska.

OBJECTIVES: This study compares lower limb diaphyseal robusticity between Native Alaskan hunter-gatherers to reconstruct patterns of mobility and engagement with terrain. MATERIALS AND METHODS: Ancestral remains included in this study date between 600 and 1800 C.E. and were divided into three regions: Coastal Bay, Far North Coastal, and Inland/Riverine. Cross-sectional properties were determined at femoral and tibial midshafts and standardized by powers of body mass and bone length. RESULTS: Consistently elaevated areas and second moments of area were found in ancestral remains from the Far North Coastal, while the Coastal Bay remains had reduced diaphyseal robusticity. Individuals from the Inland/Riverine region were intermediate in robusticity for male femora, but similar to the Coastal Bay group for females. Sexual dimorphism was greatest in the Inland/Riverine ancestral remains and comparable between Coastal Bay and Far North Coastal regions. CONCLUSIONS: Ancestral remains from the Far North Coastal region have the greatest diaphyseal robusticity in response to intensive hunting and travel over rugged terrain. Reduced sexual dimorphism in the Far North Coastal region suggest female participation in hunting activities. Intermediate diaphyseal robusticity among Inland/Riverine males and increased sexual dimorphism reflects diverse patterns of mobility in relation to the hunting cycle between males and females. Reduced diaphyseal robusticity and sexual dimorphism among the Coastal Bay group is associated with sedentary villages established around net fishing in regions with low relief. Such findings argue against technocentric views of sedentism in hunter-gatherer lifeways and generally reflect diverse adaptive strategies and interaction with local terrain among Indigenous Late Holocene hunter-gatherers of Alaska.

Bilateral asymmetry and developmental plasticity of the humerus in modern humans.

OBJECTIVE: This study investigates bilateral asymmetry in the humerus of modern human populations with differing activity patterns to assess the relative plasticity of different bone regions in response to environmental influences, particularly the biomechanical demands of handedness. METHODS: External breadths, cross-sectional properties, and centroid sizes were used to quantify directional and absolute asymmetry of humeral diaphyseal, distal periarticular, and articular regions in six populations with differing subsistence strategies (total n = 244). Geometric section properties were measured using computed tomography at six locations along the distal humerus, while centroid sizes of the distal articular and periarticular regions, as well as eight segments of the diaphysis, were extracted from external landmark data. Bilateral asymmetries were compared between populations and sexes. Each property was also tested for correlation with bilateral asymmetry at 40% of bone length, which has been shown to correlate with handedness. RESULTS: Asymmetry is highest in the diaphysis, but significant through all distal bone regions. Asymmetry increases in the region of the deltoid tuberosity, and progressively declines distally through the shaft and distal periarticular region. Articular asymmetry is higher than periarticular asymmetry, approaching levels seen just proximal to the olecranon fossa, and is weakly but significantly correlated with diaphyseal asymmetry. Hunter-gatherers from Indian Knoll have significantly higher levels of asymmetry than other groups and are more sexually dimorphic, particularly in cross-sectional properties of the diaphysis. CONCLUSIONS: Humeral dimensions throughout the diaphysis, including regions currently used in taxonomic assignments of fossil hominins, likely respond to in vivo use, including population and sex-specific behaviors.

Gorilla calcaneal morphological variation and ecological divergence.

OBJECTIVES: The primate foot has been extensively investigated because of its role in weight-bearing; however, the calcaneus has been relatively understudied. Here we examine entire gorilla calcaneal external shape to understand its relationship with locomotor behavior. MATERIALS AND METHODS: Calcanei of Gorilla gorilla gorilla (n = 43), Gorilla beringei graueri (n = 20), and Gorilla beringei beringei (n = 15) were surface or micro-CT scanned. External shape was analyzed through a three-dimensional geometric morphometric sliding semilandmark analysis. Semilandmarks were slid relative to an updated Procrustes average in order to minimize the bending energy of the thin plate spline interpolation function. Shape variation was summarized using principal components analysis of shape coordinates. Procrustes distances between taxa averages were calculated and resampling statistics run to test pairwise differences. Linear measures were collected and regressed against estimated body mass. RESULTS: All three taxa exhibit statistically different morphologies (p < .001 for pairwise comparisons). G. g. gorilla demonstrates an anteroposteriorly elongated calcaneus with a deeper cuboid pivot region and mediolaterally flatter posterior talar facet. G. b. beringei possesses the flattest cuboid and most medially-angled posterior talar facets. G. b. graueri demonstrates intermediate articular facet morphology, a medially-angled tuberosity, and an elongated peroneal trochlea. DISCUSSION: Articular facet differences separate gorillas along a locomotor gradient. G. g. gorilla is adapted for arboreality with greater joint mobility, while G. b. beringei is adapted for more stereotypical loads associated with terrestriality. G. b. graueri's unique posterolateral morphology may be due to a secondary transition to greater arboreality from a more terrestrial ancestor.

Locomotion on the edge: Structural properties of the third metacarpal in Thoroughbred and Quarter Horse racehorses and feral Assateague Island ponies.

The elongated, distally tapered limbs of horses are adapted for high-speed locomotion. Because these traits are artificially selected for in modern racehorses, they operate at a morphological extreme with a high risk of fracture. Racehorses are subject to different training and racing regimes depending on their breed and gait, and are therefore an interesting model to examine bone functional adaptation under variable biomechanically intense conditions. This study compares bone structural properties in the third metacarpal (MCIII) of Thoroughbred (n = 9) and Quarter Horse (n = 11) racehorses, using feral Assateague Island ponies (n = 6) as an untrained/unraced outgroup, to determine whether structural properties reflect variable racing and training regimes. Geometric section properties and bone mineral densities were determined using peripheral quantitative CT at two diaphyseal sites and through the distal epiphysis. Diaphyseal strength of the MCIII in all three breeds does not differ relative to body size, but in the mid-diaphyseal region Thoroughbreds have higher antero-posterior relative to medio-lateral bending strength than Quarter Horses, as well as higher bone mineral densities in left MCIII epiphyses (particularly in the lateral condyle). Interestingly, all breeds have lower bone mineral densities in the lateral versus medial condyle, an inherent structural feature that may influence predisposition to fracture when running around turns. Our results suggest that despite subtle differences in bone structure between different racehorse breeds, basic morphology of the third metacarpus is relatively similar among racing and non-racing horses, possibly reflecting intense selection (natural and artificial) across domestic equids for similar structural features within distal limb elements.

Skeletal ageing in Virunga mountain gorillas.

Bone loss and heightened fracture risk are common conditions associated with ageing in modern human populations and have been attributed to both hormonal and other metabolic and behavioural changes. To what extent these age-related trends are specific to modern humans or generally characteristic of natural populations of other taxa is not clear. In this study, we use computed tomography to examine age changes in long bone and vertebral structural properties of 34 wild-adult Virunga mountain gorillas (Gorilla beringei beringei) whose skeletons were recovered from natural accumulations. Chronological ages were known or estimated from sample-specific dental wear formulae and ranged between 11 and 43 years. Gorillas show some of the same characteristics of skeletal ageing as modern humans, including endosteal and some periosteal expansion. However, unlike in humans, there is no decline in cortical or trabecular bone density, or in combined geometric-density measures of strength, nor do females show accelerated bone loss later in life. We attribute these differences to the lack of an extended post-reproductive period in gorillas, which provides protection against bone resorption. Increases in age-related fractures (osteoporosis) in modern humans may be a combined effect of an extended lifespan and lower activity levels earlier in life. This article is part of the theme issue 'Evolution of the primate ageing process'.