Limb bone bilateral asymmetry: variability and commonality among modern humans

Humans demonstrate species-wide bilateral asymmetry in long bone dimensions. Previous studies have documented greater right-biases in upper limb bone dimensions--especially in length and diaphyseal breadth--as well as more asymmetry in the upper limb when compared with the lower limb. Some studies have reported left-bias in lower limb bone dimensions, which, combined with the contralateral asymmetry in upper limbs, has been termed "crossed symmetry." The examination of sexual dimorphism and population variation in asymmetry has been limited. This study re-examines these topics in a large, geographically and temporally diverse sample of 780 Holocene adult humans. Fourteen bilateral measures were taken, including maximum lengths, articular and peri-articular breadths, and diaphyseal breadths of the femur, tibia, humerus, and radius. Dimensions were converted into percentage directional (%DA) and absolute (%AA) asymmetries. Results reveal that average diaphyseal breadths in both the upper and lower limbs have the greatest absolute and directional asymmetry among all populations, with lower asymmetry evident in maximum lengths or articular dimensions. Upper limb bones demonstrate a systematic right-bias in all dimensions, while lower limb elements have biases closer to zero %DA, but with slight left-bias in diaphyseal breadths and femoral length. Crossed symmetry exists within individuals between similar dimensions of the upper and lower limbs. Females have more asymmetric and right-biased upper limb maximum lengths, while males have greater humeral diaphyseal and head breadth %DAs. The lower limb demonstrates little sexual dimorphism in asymmetry. Industrial groups exhibit relatively less asymmetry than pre-industrial humans and less dimorphism in asymmetry. A mixture of influences from both genetic and behavioral factors is implicated as the source of these patterns.     

Postcranial variations in late Epigravettian and Neolithic human remains from Arene Candide cave (Liguria,Italy)

Late Epigravettian postcranial human remains from the Arene Candide cave (Finale Ligure, Savona, Italy) were compared with the Neolithic sample found in the upper levels of the same site. Data on length, diaphyseal circumference and diameter of clavicle, humerus, radius, femur and tibia were collected from male specimens having all these bones. The Epigravettian sample is characterized by significantly greater tibial length, robustness and platycnemia, significantly lower circumferences in the upper limb bones and the clavicle, and a high degree of asymmetry. Variations observed in lower limb bones are those expected on the basis of the different functional requirements of a hunting and gathering economy compared to a more sedentary, food producing economy. Differences in the upper limb bones and the clavicle are less explicable. However, considering that in spite of a more slender structure, the Epigravettian bones show evidence of vigorous use, variation in upper limb could result from qualitatively different involvements.     

Habitual throwing and swimming correspond with upper limb diaphyseal strength and shape in modern human athletes

Variation in upper limb long bone cross‐sectional properties may reflect a phenotypically plastic response to habitual loading patterns. Structural differences between limb bones have often been used to infer past behavior from hominin remains; however, few studies have examined direct relationships between behavioral differences and bone structure in humans. To help address this, cross‐sectional images (50% length) of the humeri and ulnae of university varsity‐level swimmers, cricketers, and controls were captured using peripheral quantitative computed tomography. High levels of humeral robusticity were found in the dominant arms of cricketers, and bilaterally among swimmers, whereas the most gracile humeri were found in both arms of controls, and the nondominant arms of cricketers. In addition, the dominant humeri of cricketers were more circular than controls. The highest levels of ulnar robusticity were also found in the dominant arm of cricketers, and bilaterally amongst swimmers. Bilateral asymmetry in humeral rigidity among cricketers was greater than swimmers and controls, while asymmetry for ulnar rigidity was greater in cricketers than controls. The results suggest that more mechanically loaded upper limb elements––unilaterally or bilaterally––are strengthened relative to less mechanically loaded elements, and that differences in mechanical loading may have a more significant effect on proximal compared to distal limb segments. The more circular humerus in the dominant arm in cricketers may be an adaptation to torsional strain associated with throwing activities. The reported correspondence between habitual activity patterns and upper limb diaphyseal properties may inform future behavioral interpretations involving hominin skeletal remains. Am J Phys Anthropol 2009. © 2009 Wiley‐Liss, Inc.     

Bilateral asymmetry of the humerus during growth and development

The development of handedness throughout growth can be investigated by using bilateral asymmetry of the humerus as a proxy for this trait. A large skeletal sample of nonadults from English archaeological sites was examined using standard metric techniques to assess when right-sided asymmetry first appears in the human skeleton. Results of this work indicate a change in directional asymmetry during growth and development, with infants and young children exhibiting no significant asymmetry and older children and adolescents demonstrating right-sidedness. This trend is consistent with what has been observed in previous studies of upper limb asymmetry in skeletal material and behaviorally in living children, adding further strength to the premise that biomechanical forces strongly influence bilateral asymmetry in the upper limb bones. Variability in the magnitude of asymmetry between different features of the humerus was also noted. This characteristic can be explained by differing degrees of genetic canalization, with length and articular dimensions being more strongly canalized than diaphyseal properties.     

Bilateral asymmetry in the limb bones of the chimpanzee (Pan troglodytes)

There is much debate in behavioral primatology on the existence of population-level handedness in chimpanzees. The presence or absence of functional laterality in great apes may shed light on the origins of human handedness and on the evolution of cerebral asymmetry. The plasticity of long bone diaphyses in response to mechanical loading allows the functional interpretation of differences in cross-sectional geometric. While left-right asymmetry in upper limb diaphyseal morphology is a known property in human populations, it remains relatively unexplored in apes. We studied bilateral asymmetry in 64 skeletons of wild-caught chimpanzee using the humerus, second metacarpal, and femur. The total subperiosteal area (TA) of the diaphyses was measured at 40% of maximum humeral length and at the midshaft of the metacarpals and femora using external silicone molds. Overall, the TA values of the left humeri were significantly greater than the right, indicating directional asymmetry. This effect was even greater when the magnitude of difference in TA between each pair of humeri was compared. The right second metacarpals showed a tendency toward greater area than did the left, but this did not reach statistical significance. The lack of asymmetry in the femur serves as a lower limb control, and suggests that the upper limb results are not a product of fluctuating asymmetry. These findings imply behavioral laterality in upper limb function in chimpanzees, and suggest a complementary relationship between precision and power.     

Postcranial robusticity in Homo. II: Humeral bilateral asymmetry and bone plasticity

The analysis of humeral asymmetry in Recent human skeletal samples and an extant tennis-player sample documents minimal asymmetry in bone length, little asymmetry in distal humeral articular breadth, but pronounced and variable asymmetry in mid- and distal diaphyseal crosssectional geometric parameters. More specifically, skeletal samples of normal modern Euroamericans, prehistoric and early historic Amerindians, and prehistoric Japanese show moderate (ca. 5–14%) median asymmetry in diaphyseal cross-sectional areas and polar second moments of area, whereas the tennis-player sample, with pronounced unilateral physical activity, exhibits median asymmetries of 28–57% in the same parameters. A sample of Neandertals with nonpathological upper limbs exhibits similarly low articular asymmetry but pronounced diaphyseal asymmetries, averaging 24–57%. In addition, three Neandertals with actual or possible post-traumatic upper limb alterations have the same low articular asymmetry but extremely high diaphyseal asymmetries, averaging 112–215%. These data support those from experimental work on animals, exercise programs of humans, and human clinical contexts in establishing the high degree of diaphyseal plasticity possible for humans, past and present, under changing biomechanical loading conditions. This lends support to activity-related functional interpretations of changing human diaphyseal morphology and robusticity during the Pleistocene. © 1994 Wiley-Liss, Inc.     

Postcranial adaptations for climbing in Loridae (Primates)

The Loridae are an arboreal family of small primates that are specialized for slow and quiet climbing. This paper examines the relationship between lorid locomotory behaviour and postcranial skeletal morphology. Lorid humeral and femoral diaphyseal geometric cross-sectional properties, articular surface areas, and lengths are compared to those properties in other small primates with less specialized locomotory behaviour. The comparative sample includes both closely related prosimians and more distantly related platyrrhines.
Results indicate that lorids have greater humeral and femoral diaphyseal rigidity than other quadrupedal primates of similar body size, suggesting that lorid limbs are subjected to greater forces. Lorids also have relatively larger humeral and femoral articulations, corresponding to field and laboratory observations which indicate that lorid joints are highly mobilc. In addition, lorids have long humeri relative to femoral length, and compared to humeral length in less specialized prosimians of similar body mass. Long humeral length relative to femoral length is interpreted as a climbing adaptation because similar limb proportions are also seen in many non-primate climbers. Altogether, humeral and femoral diaphyseal cross-sectional properties, articular surface areas, and lengths comprise a suite of characters which have potential for identifying climbing specialists in the fossil record.     

Is the Clavicle of Apes Long? An Investigation of Clavicular Length in Relation to Body Mass and Upper Thoracic Width

An elongated clavicle is one of the distinct features of apes and humans. It plays an important role in providing mobility as well as stability for the shoulder joints. The relative length of the clavicle is an especially important factor in limiting the range of shoulder joint excursion. It is said that among primates, Asian apes, i.e., gibbons and orang-utans, have very long clavicles. At the same time, they also have a wide upper thoracic cage, which may diminish the effective length of the clavicle. To clarify the length of the clavicle in apes, from the standpoint of the functional anatomy of the shoulder girdle, we examined clavicular length in 15 anthropoid species exhibiting various positional behaviors. The results confirm that clavicle length in Asian apes is long, and chimpanzees have a short clavicle like that of Old and New World monkeys, when scaled to body mass. The clavicular length of chimpanzees, however, is intermediate between Old World monkeys and Asian apes when scaled against thoracic width. Therefore, living apes can be grouped together, albeit just barely, by possession of a relatively long clavicle for their thoracic cage size. Interestingly, New World monkeys tend to exhibit a longer clavicle than Old World monkeys of equivalent body mass or thoracic cage width. Although it is unclear whether the ancestral condition of clavicular length in anthropoids was similar to that of living Old or New World monkeys, an elongation of clavicle was an important step toward evolution of the modern body plan of hominoids.     

A comparison of primate, carnivoran and rodent limb bone cross-sectional properties: are primates really unique?

The cross-sectional properties of mammalian limb bones provide an important source of information about their loading history and locomotor adaptations. It has been suggested, for instance, that the cross-sectional strength of primate limb bones differs from that of other mammals as a consequence of living in a complex arboreal environment (Kimura, 1991, 1995). In order to test this hypothesis more rigorously, we have investigated cross-sectional properties in samples of humeri and femora of 71 primate species, 30 carnivorans and 59 rodents. Primates differ from carnivorans and rodents in having limb bones with greater cross-sectional strength than mammals of similar mass. This might imply that primates have stronger bones than carnivorans and rodents. However, primates also have longer proximal limb bones than other mammals. When cross-sectional dimensions are regressed against bone length, primates appear to have more gracile bones than other mammals. These two seemingly contradictory findings can be reconciled by recognizing that most limb bones experience bending as a predominant loading regime. After regressing cross-sectional strength against the product of body mass and bone length, a product which should be proportional to the bending moments applied to the limb, primates are found to overlap considerably with carnivorans and rodents. Consequently, primate humeri and femora are similar to those of nonprimates in their resistance to bending. Comparisons between arboreal and terrestrial species within the orders show that the bones of arboreal carnivorans have greater cross-sectional properties than those of terrestrial carnivorans, thus supporting Kimura's general notion. However, no differences were found between arboreal and terrestrial rodents. Among primates, the only significant difference was in humeral bending rigidity, which is higher in the terrestrial species. In summary, arboreal and terrestrial species do not show consistent differences in long bone reinforcement, and Kimura's conclusions must be modified to take into account the interaction of bone length and cross-sectional geometry.     

Role of Nonbehavioral Factors in Adjusting Long Bone Diaphyseal Structure in Free-ranging <Emphasis Type="Italic">Pan troglodytes</Emphasis>

Limb bones deform during locomotion and can resist the deformations by adjusting their shapes. For example, a tubular-shaped diaphysis best resists variably-oriented deformations. As behavioral profiles change during adulthood, patterns of bone deformation may exhibit age trends. Habitat characteristics, e.g., annual rainfall, tree density, and elevation changes, may influence bone deformations by eliciting individual components of behavioral repertoires and suppressing others, or by influencing movements during particular components. Habituated chimpanzee communities provide a unique opportunity to examine these factors because of the availability of morphological data and behavioral observations from known-age individuals inhabiting natural habitats. We evaluated adult femora and humeri of 18 female and 10 male free-ranging chimpanzees (Pan troglodytes) from communities in Gombe (Tanzania), Mahale Mountains (Tanzania), and Taï Forest (Côte d’Ivoire) National Parks. We compare cross sections at several locations (35%, 50%, 65% diaphyseal lengths). Community comparisons highlight different diaphyseal shapes of Taï females relative to Mahale and Gombe females, particularly in humeral diaphyses. Age trends in diaphyseal shapes are consistent with reduced activity levels in general, not only reduced arboreal activity. Age-related bone loss is apparent among community females, but is less striking among males. Community trends in diaphyseal shape are qualitatively consistent with ranked annual rainfall at localities, tree density, and elevation change or ruggedness of terrain. Habitat characteristics may contribute to variation in diaphyseal shape among chimpanzee communities, much like among modern human groups, but verification awaits further rigorous experimental and comparative analyses.     

Brief communication: histological age estimation using rib and clavicle.

Histological methods for estimating age at death using osteon population densities for the rib, clavicle, and rib and clavicle combined are presented. Predicting formulas were generated from a sample of 40 individuals of known age, sex, and race. Independent samples of 12 ribs and 7 clavicles were used to test the formulas. Mean differences between known and predicted ages were 1.1 years, 2.6 years, and 3.4 years for the clavicle, rib and clavicle combined, and rib formulas respectively. An analysis of variance found no significant differences among the means for predicted and known ages. Since the formula based upon rib and clavicle combined has the higher standard error and r2, and includes data from different bones, it should provide better overall accuracy and reliability, and is recommended whenever both bones are available.     

Epipaleolithic human appendicular remains from Ein Gev I,Israel

The Upper Paleolithic (Early Epipaleolithic/Kebaran; ∼ 19,000 cal BP) human skeleton, from Layer 3 of Ein Gev I on the western flanks of the Golan Heights adjacent to the Sea of Galilee, retains sufficient limb remains to permit assessment of its body size and proportions, as well as diaphyseal reflections of skeletal hypertrophy. The individual was of modest stature but average mass for a later Upper Paleolithic individual, providing it with the body mass-to-stature body proportions characteristic of later Upper Paleolithic and more recent circum-Mediterranean humans. The humeri exhibit unexceptional diaphyseal asymmetry and robustness for an Upper Paleolithic human, and the femur exhibits similar relative diaphyseal hypertrophy. The humeral midshafts are relatively round, but the femoral and tibial midshafts are pronounced anteroposteriorly. As such, Ein Gev 1 provides additional paleobiological data on the appendicular remains of these Southwest Asian humans prior to the increasing sedentism of the terminal Pleistocene.     

A three‐dimensional analysis of bilateral directional asymmetry in the human clavicle

This study presents a novel three‐dimensional analysis using statistical atlases and automated measurements to assess diaphyseal morphology of the clavicle and its relationship to muscle asymmetry. A sample of 505 individuals (285 males, 220 females) from the William McCormick Clavicle Collection was CT scanned, segmented, and added to a statistical bone atlas that captures correspondence between homologous points on the bone surfaces. Muscle attachment sites were localized on the atlas and then propagated across the entire population. Cross‐sectional contours were extracted at 5% increments along the entire bone, as well as at muscle attachment sites and the clavicle waist; maximum and minimum dimensions of each cross‐sectional contour were calculated. In addition, the entire three‐dimensional surface was examined for asymmetry by analyzing the magnitude and directional differences between homologous points across all bone surfaces in the dataset. The results confirm the existing studies on clavicle asymmetry, namely that the left clavicle is longer than the right, but the right is more robust than the left. However, the patterns of asymmetry are sexually dimorphic. Males are significantly asymmetric in all dimensions and at muscle and ligament attachment sites (P < 0.05), whereas female asymmetry is more variable. We hypothesize that this is related to absolute and relative differences in male muscle strength compared to females. However, an area with no muscle attachments on the posterior midshaft was significantly asymmetric in both sexes. We suggest that this is a curvature difference caused by opposing muscle actions at the medial and lateral ends of the bone. Am J Phys Anthropol 2012. © 2012 Wiley Periodicals, Inc.     

Weight of the skeleton during postnatal development

The weight of all bones and the length of humeri, radii, femora and tibiae have been determined in a series of 150 dry, fat-free skeletons from American Whites and Negroes of both sexes, ranging in age from 23 days to 22 years. Six skeletons were eliminated from the series because of evidence of previous illness. A comparison of the lengths of femur plus tibia of this series with the mean statures of a large series of living children at given ages indicates similarity in the growth patterns. Statistical analyses of the data show that the skeletal weight cannot be estimated reliably from age by cither an exponential growth equation or by a logistic function. The weight of the skeleton, however, is related to the lengths of the measured limb bones by allometric equations, and such equations involving each of the four bones are presented for estimation of skeletal weight in the living. Although the standard errors of estimate of the equations based on lengths of each of these four bones differ very little, the radius is recommended over the other three because it is more readily accessible in the living for a roentgenogram and its shadow on the film shows least distortion.     

A genome-wide scan for quantitative trait loci affecting limb bone lengths and areal bone mineral density of the distal femur in a White Duroc × Erhualian F<Subscript>2</Subscript> population

Background

Limb bone lengths and bone mineral density (BMD) have been used to assess the bone growth and the risk of bone fractures in pigs, respectively. It has been suggested that limb bone lengths and BMD are under genetic control. However, the knowledge about the genetic basis of the limb bone lengths and mineralisatinon is limited in pigs. The aim of this study was to identify quantitative trait loci (QTL) affecting limb bone lengths and BMD of the distal femur in a White Duroc × Erhualian resource population.

Results

Limb bone lengths and femoral bone mineral density (fBMD) were measured in a total of 1021 and 116 F₂ animals, respectively. There were strong positive correlations among the lengths of limb bones and medium positive correlations between the lengths of limb bones and fBMD. A whole-genome scan involving 183 microsatellite markers across the pig genome revealed 35 QTL for the limb bone lengths and 2 for femoral BMD. The most significant QTL for the lengths of five limb bones were mapped on two chromosomes affecting all 5 limb bones traits. One was detected around 57 cM on pig chromosome (SSC) 7 with the largest F-value of more than 26 and 95% confidence intervals of less than 5 cM, providing a crucial start point to identify the causal genes for these traits. The Erhualian alleles were associated with longer limb bones. The other was located on SSCX with a peak at 50–53 cM, whereas alleles from the White Duroc breed increased the bone length. Many QTL identified are homologous to the human genomic regions containing QTL for bone-related traits and a list of interesting candidate genes.

Conclusion

This study detected the QTL for the lengths of scapula, ulna, humerus and tibia and fBMD in the pig for the first time. Moreover, several new QTL for the pig femoral length were found. As correlated traits, QTL for the lengths of five limb bones were mainly located in the same genomic regions. The most promising QTL for the lengths of five limb bones on SSC7 merits further investigation.

     

The Shanidar 3 Neandertal

The Shanidar 3 Neandertal partial skeleton preserves four teeth, major portions of the thoracic and lumbar vertebrae, sacrum, ribs, clavicles, scapulae, humeri, hand bones, innominate bones, and foot bones, plus fragments of the ulnae, radii, femora, tibiae, and fibulae. Their morphology aligns Shanidar 3 closely with the other Shanidar Neandertals and the European and Near Eastern Neandertals. This is apparent especially in the dentition, scapulae, hand bones, and pubic bones.     

Severe short-limb dwarfism resembling Grebe chondrodysplasia

Summary A severe, nonlethal short-limb bone dysplasia is described in two unrelated patients. The disorder is characterized by a peculiar facial appearance, rib anomalies and severe shortness and distortion of individual long bones, notably the humeri, tibiae, fibulae, metapodia and phalanges with marked irregularity and asymmetry of bone changes. The condition is differentiated from other bone dysplasias with extreme limb shortness, in particular Grebe chondrodysplasia.     

Skeletal differences between pygmy (Pan paniscus) and common chimpanzees (Pan troglodytes)

Skeletal dimensions of pygmy (Pan paniscus) and common (Pan troglodytes) chimpanzees were compared. Significant differences were found in the clavicles, scapulae, pelvises, and in the humerus/femur and femur head/length ratios. No significant differences were observed in long bone lengths or talar breadths. There is extensive overlap in body weights, so that the observed differences cannot be accounted for by body size alone. We conclude that pygmy and common chimpanzees are morphologically distinct. Implications for hominoid evolution are discussed.     

Comparative limb bone scaling in turtles: Phylogenetic transitions with changes in functional demands?

Several terrestrial vertebrate clades include lineages that have evolved nearly exclusive use of aquatic habitats. In many cases, such transitions are associated with the evolution of flattened limbs that are used to swim via dorsoventral flapping. Such changes in shape may have been facilitated by changes in limb bone loading in novel aquatic environments. Studies on limb bone loading in turtles found that torsion is high relative to bending loads on land, but reduced compared to bending during aquatic rowing. Release from torsion among rowers could have facilitated the evolution of hydrodynamically advantageous flattened limbs among aquatic species. Because rowing is regarded as an intermediate locomotor stage between walking and flapping, rowing species might show limb bone flattening intermediate between the tubular shapes of walkers and the flattened shapes of flappers. We collected measurements of humeri and femora from specimens representing four functionally divergent turtle clades: sea turtles (marine flappers), softshells (specialized freshwater rowers), emydids (generalist semiaquatic rowers), and tortoises (terrestrial walkers). Patterns of limb bone scaling with size were compared across lineages using phylogenetic comparative methods. Although rowing taxa did not show the intermediate scaling patterns we predicted, our data provide other functional insights. For example, flattening of sea turtle humeri was associated with positive allometry (relative to body mass) for the limb bone diameter perpendicular to the flexion-extension plane of the elbow. Moreover, softshell limb bones exhibit positive allometry of femoral diameters relative to body mass, potentially helping them maintain their typical benthic position in water by providing additional weight to compensate for shell reduction. Tortoise limb bones showed positive allometry of diameters, as well as long humeri, relative to body mass, potentially reflecting specializations for resisting loads associated with digging. Overall, scaling patterns of many turtle lineages appear to correlate with distinctive behaviors or locomotor habits.     

Longitudinal and lateral variations in the aluminum concentration of selected caprine, bovine, and human bone samples

Longitudinal and lateral variations in Al concentration in several large animal (bovine and caprine) long bones (tibia and femur) and several human clavicle bones were examined using a sensitive analytical method based on electrothermal atomization atomic absorption spectrometry with Zeeman background correction. Bone segments were carefully removed using special tools free of significant Al contamination, freeze-dried, and digested overnight at room temperature in concentrated HNO₃. Bone digestates were analyzed for Al using simple aqueous calibration standards with a Ca(NO₃)₂ modifier. Mean bone Al concentrations were relatively low (<1 Μg/g, dry weight) in bovine and caprine long bones compared to literature values for human bone samples. Longitudinal variations of Al in the animal bones examined appeared relatively uniform compared to the human clavicle bones, where, in three of five cases, Al appeared enriched at the epiphyses (joints). The Al “enrichment” was symmetrical with respect to both left and right clavicle bones. Aluminum concentrations at the mid-shaft of the clavicle bone show less variation compared to whole bone studies, but considerable scatter is evident along the bone length. The mean bone aluminum concentration in the five human subjects varied from 1 to 6 Μ/g dry weight.