Enthesis bilateral asymmetry in humans and African apes

Entheses (skeletal muscle and tendon attachment sites) have often been used to infer handedness and activity variability among human populations. However, the specific roles that intensity vs. frequency of muscle contractions play in modifying entheses are not well understood and the assumption that entheses reflect muscle activity levels has been challenged. This study explores the effect of habitual muscular activity on enthesis morphology in humans and African apes by investigating bilateral asymmetry in the forelimbs and hindlimbs of these taxa. Humans have generally more developed entheses in the lower limb while African apes have generally more developed entheses in the forelimbs. All species studied have more asymmetric forelimbs than hindlimbs except humans that show more asymmetrical expression of bony spurs in the lower limbs than in the upper limbs. When comparing species, humans are always more asymmetric in ethesis development than apes for both the forelimbs and hindlimbs, which reflects the relatively greater asymmetry in limb use in humans and the more symmetric use in apes. Enthesis development may reflect cross-symmetry patterns in humans and, more subtly, a moderate handedness in apes during manipulative activities. This study suggests that enthesis morphology provides information on muscle activity levels, with greater development of entheses associated with more habitual or powerful muscle use. The general similarity of ape and human responses to muscle activity suggests that muscle activity influenced enthesis development in Plio-Pleistocene hominins and that interpretation of muscle markings in these fossils can provide data for functional inferences in these extinct species.     

Patterns of clavicular bilateral asymmetry in relation to the humerus: variation among humans

Studies of directional asymmetry in the human upper limb have extensively examined bones of the arm, forearm, and hand, but have rarely considered the clavicle. Physiologically, the clavicle is an integrated element of the upper limb, transmitting loads to the axial skeleton and supporting the distal bones. However, clavicles develop in a manner that is unique among the bones of the upper limb. Previous studies have indicated that the clavicle has a right-biased asymmetry in diaphyseal breadth, as in humeri, radii, ulnae, and metacarpals, but unlike these other elements, a left-biased length asymmetry. Few studies have assessed how clavicular asymmetry relates to these other bones of the upper limb. Bilateral directional asymmetry of the clavicle is examined in relation to the humerus in a large, geographically diverse human sample, comparing lengths and diaphyseal breadths. Dimensions were converted into percentage directional (%DA) and absolute (%AA) asymmetries. Results indicate that humans have same-side %DA bias in the clavicles and humeri, and contralateral length %DA between these elements. Diaphyseal breadths in both clavicles and humeri are more asymmetric-both in direction and amount-than lengths. Differences in diaphyseal asymmetry are shown to relate to variation in physical activities among groups, but a relationship between activity and length asymmetry is not supported. This further supports previous research, which suggests different degrees of sensitivity to loading between diaphyseal breadths and maximum lengths of long bones. Differences in lateralized behavior and the potential effects of different bone development are examined as possible influences on the patterns observed among human groups.     

Laterality in spontaneous motor activity of chimpanzees and squirrel monkeys

Varieties of nonmanipulative motor responses were observed in chimpanzees and squirrel monkeys. Chimpanzees displayed a right hand preference for touching their inanimate environments but used their right and left hands equally for touching their faces and their bodies. The latter result was not consistent with previous reports of a left hand preference for face touching in apes. The right hand preference for environmental touching was stronger in male than in female chimpanzees. Squirrel monkeys had a right preference for combined hand and foot responses directed to their bodies, but expressed no handedness for environmentally directed touching. These limb preferences in chimpanzees and squirrel monkeys indicate that neither precise, complex manipulation nor postural instability are necessary conditions for population level hand preferences. Factor analysis of the chimpanzee manual responses showed distinct self and environmentally directed factors. Analysis of the squirrel monkey data also showed self and environmental factors, except that body scratching had a negative loading on the environmental factor. This latter result suggests that self-scratching by squirrel monkeys is a displacement activity that suppresses manual exploration of the environment. © 1992 Wiley-Liss, Inc.     

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.     

Muscle architecture of the common chimpanzee (Pan troglodytes): perspectives for investigating chimpanzee behavior

Thorpe et al. (Am J Phys Anthropol 110:179–199, 1999) quantified chimpanzee (Pan troglodytes) muscle architecture and joint moment arms to determine whether they functionally compensated for structural differences between chimpanzees and humans. They observed enough distinction to conclude that musculoskeletal properties were not compensatory and suggested that chimpanzees and humans do not exhibit dynamically similar movements. These investigators based their assessment on unilateral limb musculatures from three male chimpanzees, of which they called one non-adult representative. Factors such as age, sex, and behavioral lateralization may be responsible for variation in chimpanzee muscle architecture, but this is presently unknown. While the full extent of variation in chimpanzee muscle architecture due to such factors cannot be evaluated with data presently available, the present study expands the chimpanzee dataset and provides a preliminary glimpse of the potential relevance of these factors. Thirty-seven forelimb and 36 hind limb muscles were assessed in two chimpanzee cadavers: one unilaterally (right limbs), and one bilaterally. Mass, fiber length, and physiological cross-sectional area (PCSA) are reported for individual muscles and muscle groups. The musculature of an adult female is more similar in architectural patterns to a young male chimpanzee than to humans, particularly when comparing muscle groups. Age- and sex-related intraspecific differences do not obscure chimpanzee-human interspecific differences. Side asymmetry in one chimpanzee, despite consistent forelimb directional asymmetry, also does not exceed the magnitude of chimpanzee-human differences. Left forelimb muscles, on average, usually had higher masses and longer fiber lengths than right, while right forelimb muscles, on average, usually had greater PCSAs than left. Most muscle groups from the left forelimb exhibited greater masses than right groups, but group asymmetry was significant only for the manual digital muscles. The hind limb exhibited less asymmetry than the forelimb in most comparisons. Examination of additional chimpanzees would clarify the full range of inter- and intra-individual variation.     

Handed foraging behavior in scale-eating cichlid fish: its potential role in shaping morphological asymmetry

Scale-eating cichlid fish, Perissodus microlepis, from Lake Tanganyika display handed (lateralized) foraging behavior, where an asymmetric 'left' mouth morph preferentially feeds on the scales of the right side of its victim fish and a 'right' morph bites the scales of the left side. This species has therefore become a textbook example of the astonishing degree of ecological specialization and negative frequency-dependent selection. We investigated the strength of handedness of foraging behavior as well as its interaction with morphological mouth laterality in P. microlepis. In wild-caught adult fish we found that mouth laterality is, as expected, a strong predictor of their preferred attack orientation. Also laboratory-reared juvenile fish exhibited a strong laterality in behavioral preference to feed on scales, even at an early age, although the initial level of mouth asymmetry appeared to be small. This suggests that pronounced mouth asymmetry is not a prerequisite for handed foraging behavior in juvenile scale-eating cichlid fish and might suggest that behavioral preference to attack a particular side of the prey plays a role in facilitating morphological asymmetry of this species.     

Jaw laterality and related handedness in the hunting behavior of a scale-eating characin, Exodon paradoxus

Background

Asymmetry in animal bodies and behavior has evolved several times, but our knowledge of their linkage is limited. Tanganyikan scale-eating cichlids have well-known antisymmetry in their bodies and behavior; individuals open their mouths leftward (righty) or rightward (lefty), and righties always attack the right flank of the prey, whereas lefties attack the left. This study analyzed the morphological asymmetry in a scale-eating characiform, Exodon paradoxus, and its behavioral handedness.

Methodology/Principal Findings

Each eight E. paradoxus was observed for 1-h with a prey goldfish in an aquarium to detect the behavioral handedness. Following the experiment, the lateral differences in the mandibles and head-inclination of these eight and ten additional specimens were analyzed. Both measurements on the morphology showed a bimodal distribution, and the laterality identified by these two methods was always consistent within a given individual, indicating that the characin has morphological antisymmetry. Furthermore, this laterality significantly corresponded to behavioral handedness; that is, lefties more often rasped scales from the right flank of the prey and vice versa. However, the correlation between laterality and handedness is the opposite of that in the cichlids. This is due to differences in the feeding apparatus and technique. The characin has cuspids pointing forward on the external side of the premaxilla, and it thrusts its dominant body side outward from its body axis on the flank of the prey to tear off scales. By contrast, the cichlids draw their dominant body side inward toward the axis or rotate it to scrape or wrench off scales with the teeth lined in the opened mouth.

Conclusions/Significance

This study demonstrated that the antisymmetry in external morphology and the corresponding behavioral handedness have evolved in two lineages of scale-eating fishes independently, and these fishes adopt different utilization of their body asymmetry to tear off scales.     

Genetic basis in motor skill and hand preference for tool use in chimpanzees (Pan troglodytes)

Chimpanzees are well known for their tool using abilities. Numerous studies have documented variability in tool use among chimpanzees and the role that social learning and other factors play in their development. There are also findings on hand use in both captive and wild chimpanzees; however, less understood are the potential roles of genetic and non-genetic mechanisms in determining individual differences in tool use skill and laterality. Here, we examined heritability in tool use skill and handedness for a probing task in a sample of 243 captive chimpanzees. Quantitative genetic analysis, based on the extant pedigrees, showed that overall both tool use skill and handedness were significantly heritable. Significant heritability in motor skill was evident in two genetically distinct populations of apes, and between two cohorts that received different early social rearing experiences. We further found that motor skill decreased with age and that males were more commonly left-handed than females. Collectively, these data suggest that though non-genetic factors do influence tool use performance and handedness in chimpanzees, genetic factors also play a significant role, as has been reported in humans.     

Hand preferences for coordinated bimanual actions in 777 great apes: implications for the evolution of handedness in hominins

Whether or not nonhuman primates exhibit population-level handedness remains a topic of considerable scientific debate. Here, we examined handedness for coordinated bimanual actions in a sample of 777 great apes including chimpanzees, bonobos, gorillas, and orangutans. We found population-level right-handedness in chimpanzees, bonobos and gorillas, but left-handedness in orangutans. Directional biases in handedness were consistent across independent samples of apes within each genus. We suggest that, contrary to previous claims, population-level handedness is evident in great apes but differs among species as a result of ecological adaptations associated with posture and locomotion. We further suggest that historical views of nonhuman primate handedness have been too anthropocentric, and we advocate for a larger evolutionary framework for the consideration of handedness and other aspects of hemispheric specialization among primates.     

Directional asymmetry in the forelimb of Macaca mulatta

Asymmetry was investigated in the forelimbs of 150 rhesus monkey (Macaca mulatta) skeletons using measurements of right and left humerii, radii, ulnae, second metacarpals, and femora. Seven of the ten forelimb dimensions were larger on the right than on the left side. Paired t-tests revealed that the mean of the right side was significantly larger than that for the left for two measurements of the ulna and two of the humerus. No measurement was significantly larger on the left than on the right side. These results indicate a small but significant asymmetry in the forelimb bones of rhesus monkeys and, as is the case for humans, the direction of asymmetry favors the right side. Our findings are consistent with an interpretation of hypertrophy of certain muscles and opens the question of whether rhesus monkeys preferentially use their right forelimbs for manipulative tasks that require manual dexterity, as is the case for humans. These forelimb skeletal asymmetries are discussed in light of the recent literature on cortical asymmetry and handedness in nonhuman primates.     

Articular constraint, handedness, and directional asymmetry in the human second metacarpal

The hypothesis that functional adaptation of joint surfaces to mechanical loading occurs primarily through change in mass, density, and structure of subarticular trabeculae (the "articular constraint" model) is investigated through an analysis of directional asymmetry among three separate bone compartments in the human second metacarpal. Measures of midshaft cross-sectional geometry, osteometry of the distal epiphysis, and subarticular trabecular microarchitecture of the distal epiphysis (assessed by high-resolution microcomputed tomography) were determined for 29 paired male and female metacarpals from a well-preserved nineteenth-century Euro-Canadian historic cemetery sample. For each measure, asymmetry was quantified using both mean-difference and confidence-interval methods. Both methods found a significant right-hand bias for measures of structural strength in midshaft geometry, as has been previously noted for this sample. Articular size, however, exhibits a right-hand bias only with regard to mediolateral, and not dorsopalmar, dimensions, a result that may reflect directional asymmetry in hand breadth at the distal palmar arch. The most striking asymmetries occur for subarticular trabecular microarchitecture. The right metacarpal head exhibits greater bone volume fraction, bone surface density, trabecular number, connectivity, and a more platelike rather than rodlike structure. These outcomes confer greater resistance to both axial compressive and shear strains for the metacarpal head at the metacarpophalangeal arthrosis. In all, these results confirm and extend previous research documenting structural asymmetries and limb dominance and are consistent with the concept of articular constraint. They also suggest a morphological signal through which functional asymmetry associated with handedness in fossil hominins may be investigated.     

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.     

Front Cover

This review highlights the scientific advances concerning the origins of human right‐handedness and language (speech and gestures). The comparative approach we adopted provides evidence that research on human and non‐human animals’ behavioural asymmetries helps understand the processes that lead to the strong human left‐hemisphere specialisation. We review four major non‐mutually exclusive environmental factors that are likely to have shaped the evolution of human and non‐human primates’ manual asymmetry: socioecological lifestyle, postural characteristics, task‐level complexity and tool use. We hypothesise the following scenario for the evolutionary origins of human right‐handedness: the right‐direction of modern humans’ manual laterality would have emerged from our ecological (terrestrial) and social (multilevel system) lifestyle; then, it would have been strengthened by the gradual adoption of the bipedal stance associated with bipedal locomotion, and the increasing level of complexity of our daily tasks including bimanual coordinated actions and tool use. Although hemispheric functional lateralisation has been shaped through evolution, reports indicate that many factors and their mutual intertwinement can modulate human and non‐human primates’ manual laterality throughout their life cycle: genetic and environmental factors, mainly individual sociodemographic characteristics (e.g., age, sex and rank), behavioural characteristics (e.g., gesture per se and gestural sensory modality) and context‐related characteristics (e.g., emotional context and position of target). These environmental (evolutionary and life cycle) factors could also have influenced primates’ manual asymmetry indirectly through epigenetic modifications. All these findings led us to propose the hypothesis of a multicausal origin of human right‐handedness.     

下肢长骨骨重的非对称性

本文测量82副中国成年下股长骨即股骨,胫骨和腓骨的重量,在两侧骨重相差>1％时,则股骨、胫骨和腓骨及其三骨总重均以非对称性为多,均具有非常显著性差异(P<0.001)。除腓骨重具有明显侧别差异外,其余无显著性侧别差异,对腓骨侧差解释为:①腓骨主要机能是肌的附着,而下肢对踢和足趾取物具有明显的侧别差异;②以两侧骨重相差>1％时为非对称性的标准,由于腓骨绝对重量较小,在两侧相差<0.5克时即多属非对称性。     

Associated cranial and forelimb remains attributed to Australopithecus afarensis from Hadar, Ethiopia

A partial skeleton from Hadar, Ethiopia (A.L. 438-1) attributed to Australopithecus afarensis is comprised of part of the mandible, a frontal bone fragment, a complete left ulna, two second metacarpals, one third metacarpal, plus parts of the clavicle, humerus, radius, and right ulna. It is one of only a few early hominin specimens to preserve both cranial and postcranial elements. It also includes the first complete ulna from a large A. afarensis individual, and the first associated metacarpal and forelimb remains. This specimen, dated to approximately 3Ma, is among the geologically youngest A. afarensis fossils and is also one of the largest individuals known. Its ulnar to mandibular proportions are similar to those of the geologically older and much smaller A.L. 288-1, suggesting that body size increased without disproportional enlargement of the mandible. Overall, however, analysis of this large specimen and of the diminutive A.L. 288-1 demonstrates that the functional morphology of the A. afarensis upper limb was similar at all body sizes; there is no evidence to support the hypothesis that more than one hominin species is present at Hadar. Morphologically, all apparent apomorphic traits of the elbow, forearm, wrist, and hand of A.L. 438-1 are shared uniquely with humans. Compared to humans, A.L. 438-1 does have a more curved ulna, although A.L. 288-1 does not, and it appears to have had slightly less well-developed manipulatory capabilities of its hands, although still more derived than in apes. We conclude that selection for effective arboreality in the upper limb of Australopithecus afarensis was weaker than in non-hominins, and that manipulative ability was of greater selective advantage than in extant great apes.     

Chimpanzee (Pan troglodytes) Precentral Corticospinal System Asymmetry and Handedness: A Diffusion Magnetic Resonance Imaging Study

Background

Most humans are right handed, and most humans exhibit left-right asymmetries of the precentral corticospinal system. Recent studies indicate that chimpanzees also show a population-level right-handed bias, although it is less strong than in humans.

Methodology/Principal Findings

We used in vivo diffusion-weighted and T1-weighted magnetic resonance imaging (MRI) to study the relationship between the corticospinal tract (CST) and handedness in 36 adult female chimpanzees. Chimpanzees exhibited a hemispheric bias in fractional anisotropy (FA, left>right) and mean diffusivity (MD, right>left) of the CST, and the left CST was centered more posteriorly than the right. Handedness correlated with central sulcus depth, but not with FA or MD.

Conclusions/Significance

These anatomical results are qualitatively similar to those reported in humans, despite the differences in handedness. The existence of a left>right FA, right>left MD bias in the corticospinal tract that does not correlate with handedness, a result also reported in some human studies, suggests that at least some of the structural asymmetries of the corticospinal system are not exclusively related to laterality of hand preference.     

Poliomyelitis and skeletal asymmetry in Gombe chimpanzees

Skeletons of free-ranging chimpanzees from Gombe National Park, Tanzania allow assessment of the effects of long-term, unilateral upper limb paralysis due to the infectious viral disease, poliomyelitis. Comparison of left and right upper limb bone weights, lengths, joint areas, and diaphysial diameters between two adult females with long-term, partial paralysis and a group of unaffected adult Gombe chimpanzees show that the disease caused considerable asymmetries in the skeleton. Detailed analyses of mineral content and diaphysial cross-sectional geometry of the humerus in the affected females show individual differences. The analysis extends to consideration of bone-muscle relationships and peripheral and central nervous system involvement. For each individual, sex, estimated age at death, and behavioral information during life are known from field studies. The impact of the disease on survival and reproductive outcome of the affected individuals is discussed.     

Linking structural variability in long bone diaphyses to habitual behaviors: foragers from the southern African Later Stone Age and the Andaman Islands

The cross-sectional distribution of cortical bone in long bone diaphyses is highly responsive to mechanical loading during life, yet the relationship between systemic and localized influences on skeletal structure remains unclear. This study investigates postcranial robustness throughout the body among adults from two groups of foragers with different patterns and modes of mobility, to determine whether there is evidence for upper vs. lower body localization of skeletal robustness. The samples used for this comparison are from the southern African Later Stone Age (LSA; n = 65, male = 33, female = 28) dating from ca. 10,000 to 2,000 B.P., and 19th century indigenous Andaman Islanders (AI; n = 36, male = 17, female = 16). The LSA were highly mobile foragers who did not exploit offshore marine resources. In contrast, the AI had tightly constrained terrestrial, but significant marine, mobility. Geometric properties of cortical bone distribution in the diaphyses of the clavicle, humerus, femur, tibia, and first metatarsal are compared between the samples, providing a representation of skeletal robustness throughout the body. Multivariate ANOVA shows the AI to have significantly stronger clavicles and humeri, while the LSA femora, tibiae, and first metatarsals are stronger than those of the AI. These patterns, in which upper and lower limbs show biomechanical properties that are consistent with habitual behaviors, suggest localized osteogenic response. Although postcranial robustness appears to be correlated with overall limb function, the results suggest that more proximal elements within the limb may be more responsive to mechanical loading.     

Behavioral laterality and morphological asymmetry in the cuttlefish, Sepia lycidas

Behavioral laterality is widely found among vertebrates, but has been little studied in aquatic invertebrates. We examined behavioral laterality in attacks on prey shrimp by the cuttlefish, Sepia lycidas, and correlated this to their morphological asymmetry. Behavioral tests in the laboratory revealed significant individual bias for turning either clockwise or counterclockwise toward prey, suggesting behavioral dimorphism in foraging behavior. Morphological bias was examined by measuring the curvature of the cuttlebone; in some the cuttlebone was convex to the right (righty), while in others, the cuttlebone was convex to the left (lefty). The frequency distributions of an index of cuttlebone asymmetry were bimodal, indicating that populations were composed of two types of individuals: "righty" and "lefty." Moreover, an individual's laterality in foraging behavior corresponded with the asymmetry of its cuttlebone, with righty individuals tending to turn counterclockwise and lefty ones in the opposite direction. These results indicate that cuttlefish exhibit behavioral dimorphism and morphological antisymmetry in natural populations. The presence of two types of lateral morph in cuttlefish provides new information on the relationship between antisymmetric morphologies and the evolution of individual laterality in behavioral responses in cephalopods. The implications of these findings for the interpretation of ecological meaning and maintenance mechanisms of laterality in cuttlefish are also discussed.