Advanced computer graphics technology reveals cortical asymmetry in endocasts of rhesus monkeys

Lengths of cortical sulci were measured on ten endocranial casts (endocasts) from skulls of rhesus monkeys, using advanced computer technology that permits analysis and imaging of surface morphology in three dimensions. Sulcal lengths were compared in left and right hemispheres and, contrary to earlier reports, the length of the left Sylvian fissure was found to be significantly longer than its right counterpart, as is the case for chimpanzees and humans. This asymmetry in humans is thought to be associated with asymmetrical representation of language functions in the left hemisphere and, although this report is the first to demonstrate a significantly longer left Sylvian fissure in rhesus monkeys, our results are in keeping with psychophysical evidence that suggests that Macaca is left hemisphere dominant for perception of meaningful vocalizations. We attribute the difference between our findings and previous reports to the sensitivity of the new computer technology used to collect data from endocasts.     

Fluctuating asymmetry in fetuses of diabetic rhesus macaques

This study examines dental fluctuating asymmetry (FA) in two samples of fetal rhesus monkeys, one composed of 19 fetuses from diabetic mothers (FDM) and the other of 20 fetuses from nondiabetic mothers. Seventeen measurements were taken on the deciduous dentition of right and left mandibles. The degree of FA was assessed by comparing FDM to fetuses of normal mothers by correlation between right and left sides, and analysis of variation differences between right and left sides. Significant FA was found for three traits based on the correlation between right and left sides and for seven traits by the between-treatment ratio of variance between sides. Distal teeth, both within and outside of a morphologic field, exhibit significantly greater FA than mesial teeth. Our results support the hypothesis that developmental instability is detectable by dental FA.     

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.     

中国现生六种非人灵长类和树鼩大脑两半球不对称性的比较研究

对中国现生六种灵长类动物：懒猴、猕猴、灰叶猴、川金丝猴、滇金丝猴、长臂猿以及与灵长类关系密切的树鼩的大脑两半球形态,功能的不对称性以及由此引起的行为不对称性进行了研究。结果表明：大脑两半球不对称现象均存在于上述几种动物中。因而,这种不对称性可能经历了一个长期演化历程。     

Endocranial suture closure in rhesus macaques (Macaca mulatta)

Endocasts from skulls of 330 rhesus monkeys (Macaca mulatta) of known age are scored for closure of nine bilateral and three unilateral sutures or segments of sutures. A variety of tests reveals a strong relationship between age and stages of suture closure, although increasingly broad confidence intervals prevent sutures from being very useful for precisely aging older macaques. The order in which endosutures begin to close, as well as that in which closure is finally achieved, is determined for macaques, and these sequences compared to those for endosutures of humans (Todd and Lyon, 1924). The basilar suture is the earliest to close, while the masto-occipital and rostral and caudal squamosal sutures achieve closure quite late in both species. On the other hand, humans and macaques differ in their schedules for the sphenofrontal suture and in the initiation of closure for the rostral portion of the squamosal suture. Two sutures close significantly sooner on the right than on the left side (the rostral squamosal and masto-occipital) and asymmetry favoring closure of the right lateral lambdoid suture also approaches significance at the 0.05 level. No sutures close significantly sooner on the left side. It is suggested that macaque sutures may close from the inside out, that endosutures are more sensitive than ectosutures for detecting sequences in which cranial sutures begin to close, and that directional asymmetries in suture closure of macaques may be related to minor asymmetries in brain/skull shape (petalias).     

Morphological asymmetry and behavioral laterality in the crayfish, Procambarus clarkii

Lateral asymmetry is found widely among vertebrates, but is scarcely observed in invertebrates. Here, morphological asymmetry and behavioral laterality of a wild crayfish, Procambarus clarkii, was investigated. The carapace morphology of crayfish showed left–right differences; in some, the right side of the carapace was larger than the left side, while in others, the left side was larger. A bimodal distribution in the direction of escape behaviors induced by a tactile stimulus was also observed. Experimental crayfish were definitively divided into two groups: individuals that frequently jumped leftward (right type) and those that jumped rightward (left type). Moreover, carapace asymmetry and lateralized escape responses were significantly correlated. These results suggest that crayfish exhibit left–right dimorphism in natural populations. The ecological advantages and maintenance mechanisms underlying these behaviors are also discussed.     

Dimensions and moment arms of the hind- and forelimb muscles of common chimpanzees (Pan troglodytes).

This paper supplies quantitative data on the hind- and forelimb musculature of common chimpanzees (Pan troglodytes) and calculates maximum joint moments of force as a contribution to a better understanding of the differences between chimpanzee and human locomotion. We dissected three chimpanzees, and recorded muscle mass, fascicle length, and physiological cross-sectional area (PCSA). We also obtained flexion/extension moment arms of the major muscles about the limb joints. We find that in the hindlimb, chimpanzees possess longer fascicles in most muscles but smaller PCSAs than are predicted for humans of equal body mass, suggesting that the adaptive emphasis in chimpanzees is on joint mobility at the expense of tension production. In common chimpanzee bipedalism, both hips and knees are significantly more flexed than in humans, necessitating muscles capable of exerting larger moments at the joints for the same ground force. However, we find that when subject to the same stresses, chimpanzee hindlimb muscles provide far smaller moments at the joints than humans, particularly the quadriceps and plantar flexors. In contrast, all forelimb muscle masses, fascicle lengths, and PCSAs are smaller in humans than in chimpanzees, reflecting the use of the forelimbs in chimpanzee, but not human, locomotion. When subject to the same stresses, chimpanzee forelimb muscles provide larger moments at the joints than humans, presumably because of the demands on the forelimbs during locomotion. These differences in muscle architecture and function help to explain why chimpanzees are restricted in their ability to walk, and particularly to run bipedally.     

Age- and sex-associated variations in the directional asymmetry of rhesus macaque forelimb bones

Several investigators have questioned the significance of handedness as an explanation of directional forelimb asymmetries, yet little has been done to isolate other explanatory factors. In this investigation, we analyze 61 female and 76 male rhesus macaque skeletons for evidence of age- and/or sex-associated variations in ten forelimb bone measurements. All significant directional asymmetries are found to favor the right side. Although some of these asymmetries are found to favor the right side. Although some of these asymmetries are compatible with the interpretation of muscle hypertrophy associated with preferential use of the right forelimb, the overall pattern suggests that age- and sex-related ontogenetic factors deserve equal consideration. Significant sex differences in asymmetry means are present within and across age groups (juveniles, subadults, and adults), and numerous changes in asymmetry with age are also found. A pattern of decreasing asymmetry with age was found in males, with 40% of the ten measures being asymmetrical in juveniles, 30% in subadults, and 20% in adults. Among females, this pattern is reversed. No significant asymmetries were found for juvenile or subadult females, whereas 40% of the measures were asymmetrical in adult females. We conclude that greater consideration of age- and sex-related factors is necessary when drawing samples for the purpose of investigating asymmetries, and an awareness of trait-specific age and sex patterns of variation is necessary when citing forelimb asymmetries in demographically nonrepresentative populations as evidence of handedness or other behavioral asymmetries.     

Histological changes induced in developing limb buds of C57BL mouse embryos submitted in utero to the combined influence of acetazolamide and cadmium sulphate

Microscopic defects in limb buds of C57BL mouse embryos after the combined teratogenic action of acetazolamide plus cadmium sulphate administered on day 9 of gestation were studied in serial sections. Postaxial deficiencies observed in 12-15-day embryos and affecting preferentially the right forelimbs were classified in nine morphological types according to increasing amounts of missing parts. Type X defect consists of a nearly complete amelia in which all four limbs are represented only by the girdle and proximal end of the stylopod. Type XI abnormality appears as an intermediate reduction affecting the area of digit IV. In addition to modifications of the forelimb bud shape detected from the 10-day stage onwards, observations made 24 and 48 hr after treatment confirmed that the postaxial defects result from an absolute lack of postaxial mesoderm occurring without cell necrosis as a consequence of a postaxial shortening of the apical ectodermal ridge (aer). In 10-day embryos, the latter appears shortened and hypertrophied; it is later fragmented into alternate thick and thin portions in 11-day affected limb buds. These ectodermal changes might account for the genesis of all types of defects observed. Untreated 9-day embryos with 12-25 pairs of somites display a number of asymmetries between their right and left forelimb territories: Until the 19-somite stage, the vascular supply to that area is provided exclusively by the umbilical vein, which is larger on the right side; the initial amount of somatopleural limb mesoderm is greater in the right rudiment and the genesis of its aer is slightly protracted as compared to the left one. These asymmetries might contribute to the right side predominance of the forelimb defects induced by acetazolamide and cadmium.     

Directional asymmetry in the limbs,skull and pelvis of the silver fox (V. vulpes)

Directional asymmetry (DA) is a characteristic of most vertebrates, most strikingly exhibited by the placement of various organs (heart, lungs, liver, etc.) but also noted in small differences in the metrics of skeletal structures such as the pelvis of certain fish or sauropsids. We have analyzed DA in the skeleton of the fox (V. vulpes), using ～1,000 radiographs of foxes from populations used in the genetic analysis of behavior and morphology. Careful measurements from this robust data base demonstrate that: 1) DA occurs in the limb bones, the ileum, and ischium and in the mandible; 2) regardless of the direction of the length asymmetry vector of a particular skeletal unit, the vectorial direction of length is always opposite to that of width; 3) with the exception of the humerus and radius, there is no correlation or inverse correlation between vectorial amplitudes or magnitudes of bone asymmetries. 4) Postnatal measurements on foxes demonstrate that the asymmetry increases after birth and continues to change (increasing or decreasing) during postnatal growth. 5) A behavior test for preferential use of a specific forelimb exhibited fluctuating asymmetry but not DA. None of the skeletal asymmetries were significantly correlated with a preferential use of a specific forelimb. We suggest that for the majority of fox skeletal parameters, growth on the right and left side of the fox are differentially biased resulting in fixed differences between the two sides in either the rate of growth or the length of the period during which growth occurs. Random effects around these fixed differences perturb the magnitude of the effects such that the magnitudes of length and width asymmetries are not inversely correlated at the level of individual animals. J. Morphol., 2010. © 2010 Wiley‐Liss, Inc.     

Patterns of asymmetry in the twining vine Dalechampia scandens (Euphorbiaceae): ontogenetic and hierarchical perspectives

We studied patterns of fluctuating asymmetry (FA) in leaves of four populations of the neotropical vine Dalechampia scandens to obtain insight into the origin of leaf FA and the level at which it is controlled. We analysed correlations in signed and unsigned asymmetry at different organizational levels. We also analysed the ontogeny of FA during leaf expansion to test whether asymmetry is regulated during cell expansion, and whether fast-expanding leaves are more or less asymmetrical. Signed asymmetry was negatively correlated between successive leaves, that is, when the right side of a leaf was larger than the left side, the next leaf on the shoot tended to show the opposite pattern. The magnitude of FA, however, was very weakly correlated among successive leaves or among leaves measured on different shoots. The direction of asymmetry did not change during leaf expansion, but the relative asymmetry, that is, asymmetry corrected for difference in trait size, decreased during expansion. We found a weak negative relationship between leaf expansion rate and relative asymmetry on the fully expanded leaves. These results suggest that leaf asymmetry in Dalechampia originates from perturbations in cell proliferation in the stem, creating asymmetries in opposite directions in successive leaves. These asymmetries persist during leaf expansion, but tend to be reduced by unknown mechanisms.     

Directional asymmetry of body dimensions among white adolescents

Asymmetry of paired dimensions has been recognized as a methodological problem in anthropometry and more recently as an indicator of environmental stress. This study seeks to determine the extent of directional asymmetry for some of the measurements commonly made in anthropometry. Upper arm circumference, biepicondylar breadth, triceps and subscapular skinfolds, bicondylar breadth of the femur, and calf circumference were measured on right and left sides among 135 white adolescents from suburban Philadelphia. Handedness (right or nonright) was subject-assessed. Body composition was estimated through underwater weighing. Asymmetry was evaluated using a paired t test. Arm measurements are significantly asymmetric in favor of the right side; subscapular skinfolds and leg measurements are not significantly asymmetric. Among the sample of right-handed subjects (n = 116), upper arm circumference and biepicondylar breadth were significantly larger on the right side, and, among the males of this subsample, triceps was as well. The nonright-handed subjects (n = 19) did not show statistically significant asymmetry. Asymmetry was negatively but weakly related to body composition. These results are consistent with an explanation in terms of preferred use of one side of the body and consequent muscle hypertrophy, but an adequate test of this explanation requires hypothesis testing in larger samples of nonright-handed subjects.     

Video-task acquisition in rhesus monkeys (Macaca mulatta) and chimpanzees (Pan troglodytes): A comparative analysis

This study describes video-task acquisition in two nonhuman primate species. The subjects were seven rhesus monkeys (Macaca mulatta) and seven chimpanzees (Pan troglodytes). All subjects were trained to manipulate a joystick which controlled a cursor displayed on a computer monitor. Two criterion levels were used: one based on conceptual knowledge of the task and one based on motor performance. Chimpanzees and rhesus monkeys attained criterion in a comparable number of trials using a conceptually based criterion. However, using a criterion based on motor performance, chimpanzees reached criterion significantly faster than rhesus monkeys. Analysis of error patterns and latency indicated that the rhesus monkeys had a larger asymmetry in response bias and were significantly slower in responding than the chimpanzees. The results are discussed in terms of the relation between object manipulation skills and video-task acquisition.     

Paradoxical bilateral asymmetry in bone size and bone mass in the hand

Among 227 chronic renal disease patients, micrometer caliper radiogrammetric measurements of the second metacarpal at midshaft showed the right metacarpal to be larger (with greater bone area) and with a greater cortical area than the left second metacarpal, both in 208 right-handed individuals and in 19 left-handed individuals. This direction of asymmetry was individually characteristic of the majority of individuals, whether right-handed, left-handed or ambidextrous.     

Anatomical brain asymmetry in monkeys: frontal, temporoparietal, and limbic cortex in Macaca

Measurements evaluating possible cerebral hemispheric asymmetries were taken by hand on frontal, parietal, and temporal cortex on 60 formalin-fixed Macaca mulatta and Macaca fascicularis brain specimens. No statistically significant (P less than 0.05) right/left side differences in the mean length of four sulci in visual-processing areas of the cortex were found. The sulcus adjacent to the region cytoarchitecturally homologous to the motor speech area in the human brain did not show pronounced asymmetry. In both species, however, a small parietal lobe sulcus showed greater development on the left hemisphere than in the right. In measurements made using digital planimetry, right/left side differences in the area of the dorsal cingulate gyrus were not found. Behavioral evidence suggests that monkeys do not exhibit a consistent pattern of cerebral dominance for functions associated with most of these regions of the brain.     

Hand dominance and bilateral asymmetry in the structure of the second metacarpal

Bilateral asymmetry in the structure of the second metacarpal was examined in relation to functional hand dominance in a large, clinically nonselected, healthy population sample from the Baltimore Longitudinal Study of Aging. Bilateral bone measurements were made from anteroposterior hand radiographs of a total of 992 individuals, 609 males and 383 females, with an age range of 19–94 years. Hand dominance was determined on the basis of personal impression. Total width and medullary width at the midshaft of the second metacarpal were measured to 0.05 mm using a Helios caliper. These two measurements were used to derive cortical thickness, cortical bone area, periosteal (total) area, medullary area, percent cortical area, and the second moment of area in the mediolateral plane. In both right and left-handed individuals, statistically significant side differences were found in the calculated bone areas and the second moment of area, with the dominant hand being larger. Cortical thickness did not show significant side-related differences for either handedness. These results show that functional handedness leads to periosteal and endosteal expansion of the second metacarpal cortex on the dominant side, increasing bone strength without increasing cortical thickness. This is the first time this pattern of asymmetry has been reported in left-handers as well as right-handers. Our results argue for the primacy of environmental (mechanical) effects in determining bilateral asymmetry of limb bone structural properties. © 1994 Wiley-Liss, Inc.     

Age changes in the external dimensions of adult bone

Humeri from a large, ossuary-derived sample are used to demonstrate that considerable size variability is introduced to transverse skeletal measurements when young adults and older adults are pooled. Humeri from young adults (epiphyseal lines still visible, N ≈? 25) are smaller in transverse dimensions than those of older adults (N ≈? 300). Among left humeri, only shaft diameters demonstrate statistically significant differences. The right humeri, however, show statistically significant differences for six of the eight measurements. The increased size of the older adult humeri reflects the fact that appositional growth continues throughout adulthood. The more pronounced differences seen on the right side probably reflect developing dominance asymmetry. Recognition of this source of intrasample variability will influence the choice of skeletal measurements used for population comparisons and/or indicators of robusticity.     

BILATERAL DIRECTIONAL ASYMMETRY OF THE APPENDICULAR SKELETON OF THE HARBOR PORPOISE (PHOCOENA PHOCOENA)

Directional asymmetry ( DA ) of the lengths, diameters, and masses of the scapula, humerus, radius, and ulna were analyzed on a sample of 213 harbor porpoises from Denmark and West Greenland. The levels of DA were consistent across yearlings and older animals, mature and immature animals, sexes, and populations. All investigated variables showed significant DA favoring the right side. For the pooled sample, DA of lengths ranged from 0.2% SE 0.1 (ulna) to 1.2% SE 0.1 (scapula). DA s of diameters were 1.5% SE 0.2 for the humerus, 0.6% SE 0.1 for the radius, and 1.3% SE 0.2 for the ulna. DA of mass ranged from 2.8% SE 0.5 (humerus) to 4.3% SE 0.7 (ulna). The humerus and ulna had significantly larger mean diameter/ length ratios on the right side than the left, making them more robust. The large DA of scapula length indicates larger muscle mass associated with the right flipper, while the generally more robust right humerii and ulnae may be designed for higher levels of mechanical stress. These DA s and the examples of lateralized behavior recorded in cetaceans, point to the existence of lateralized use of the flippers at the population level in harbor porpoises and possibly other cetacean species.     

Quadrupedal locomotion in squirrel monkeys (Cebidae: Saimiri sciureus): a cineradiographic study of limb kinematics and related substrate reaction forces

Quadrupedal locomotion of squirrel monkeys on small-diameter support was analyzed kinematically and kinetically to specify the timing between limb movements and substrate reaction forces. Limb kinematics was studied cineradiographically, and substrate reaction forces were synchronously recorded. Squirrel monkeys resemble most other quadrupedal primates in that they utilize a diagonal sequence/diagonal couplets gait when walking on small branches. This gait pattern and the ratio between limb length and trunk length influence limb kinematics. Proximal pivots of forelimbs and hindlimbs are on the same horizontal plane, thus giving both limbs the same functional length. However, the hindlimbs are anatomically longer than the forelimbs. Therefore, hindlimb joints must be more strongly flexed during the step cycle compared to the forelimb joints. Because the timing of ipsilateral limb movements prevents an increasing amount of forelimb retraction, the forelimb must be more protracted during the initial stance phase. At this posture, gravity acts with long moment arms at proximal forelimb joints. Squirrel monkeys support most of their weight on their hindlimbs. The timing of limb movements and substrate reaction forces shows that the shift of support to the hindlimbs is mainly done to reduce the compressive load on the forelimb. The hypothesis of the posterior weight shift as a dynamic strategy to reduce load on forelimbs, proposed by Reynolds ([1985]) Am. J. Phys. Anthropol. 67:335-349; [1985] Am. J. Phys. Anthropol. 67:351-362), is supported by the high correlation of ratios between forelimb and hindlimb peak vertical forces and the range of motion of shoulder joint and scapula in primates.     

Suspensory locomotion of Lagothrix lagothricha and Ateles belzebuth in Yasuní National Park,Ecuador

A comparative field study of the locomotion of woolly monkeys (Lagothrix lagothricha) and spider monkeys (Ateles belzebuth) in undisturbed rainforest of northeastern Ecuador reveals substantial differences in their use of suspensory modes. Ateles performed both more brachiation (by forelimbs and tail, with trunk rotation), and forelimb swing (similar to brachiation, but without trunk rotation) than Lagothrix. In contrast, in Lagothrix 20% of suspensory movement was by pronograde forelimb swing, which resembles forelimb swing except that the body is held in a pronograde orientation due to the tail and/or feet intermittently grasping behind the trailing forelimb. Ateles never exhibited this mode. Both brachiation and forelimb swing by Ateles were more dynamic than in Lagothrix, consisting of higher proportions of full-stride bouts (versus single-step). Both species used smaller supports for suspensory than for quadrupedal locomotion, and Ateles used both smaller and larger supports for suspension than did Lagothrix. Analysis of support inclination shows that both species tended to perform more above-support movement on horizontal supports and more below-support (suspensory) movement from oblique supports. Our attempt to elucidate the aspects of canopy structure that favor suspension suggests the need for additional kinds of observational data, focusing on the "immediate structural context" of positional events.