The architecture of the shoulder in some mammals

A series of nine features of the shoulder girdle, chosen as having functional significance in relation to the movements of the shoulder in arboreal locomotion, have been studied in 1188 specimens of 194 genera of mammals. The features were defined metrically and examined by means of a multivariate statistical technique: viz. canonical analysis. The study has shown that those mammals which are nonarboreal differ considerably among themselves and form the arboreal forms. But the myriad shapes of the shoulder girdle in a wide range of mammals (e.g. some marsupials, edentates, rodents, carnivores and primates) which climb or forage in trees, can be summarized mathematically by a very small number of similar canonical variates. This information correlates well with that of a previous series of studies carried out on the primates alone. The biological information that was postulated as being reflected by the individual canonical variates for the primates is also apparent for the arboreal mammals. The different variates separate the forms in ways which are consonant with what is known about the function of the shoulder in locomotion. Aspects of the shape of the shoulder defined by the analysis appear to be discernible from an examination of the contribution of the original variables to each individual canonical variate. This seems to confirm that the shape of the shoulder girdle within a very wide range of mammals is limited by a very small number of underlying factors of biological significance. One interpretation of the results suggests that the genetic model of the mammalian shoulder may have been sufficiently fixed at an early stage in the evolution of the class as to place considerable constraints upon the subsequent evolution of the shoulder in the different Orders.     

Shoulder movements during quadrupedal locomotion in arboreal primates

The kinematics of scapula and shoulder joint movements were analyzed in three species of arboreal quadrupedal primates using cineradiography. Our findings indicate that scapular movement is highly important for forelimb movement in primates with this ancestral mode of locomotion. Retroversion of the scapula (syn. caudal rotation or extension) during the stance phase contributes more than 40% to the stride length of the forelimb. Lateral forelimb excursions, a general feature for arboreal primates, are based on complex three-dimensional scapular movements guided by the clavicle. Humeral abduction is achieved by scapular abduction and transversal rotation of the scapula about its longitudinal axis, and is therefore strikingly different from humeral abduction in humans. At the same time, the movements of the shoulder joint are limited to flexion and extension only.     

Glenohumeral mobility in primates

This study refutes the traditional idea that the glenohumeral joint of hominoids is more mobile than that of other primates, a belief that forms a basis for the two prominent theories of hominoid evolution. According to the brachiation theory, many anatomical features of the hominoid shoulder (including those of the glenohumeral joint) increase shoulder mobility and are interpreted as adaptations for brachiation. The slow climbing theory explains the same set of features as adaptations for slow climbing. The slow-climbing primates should therefore also possess these features, and their glenohumeral mobility should be the same as that of hominoids and be higher than that of other primates. This study presents three-dimensional glenohumeral mobility data, measured using a single video camera method on fresh specimens. The results show that the hominoid glenohumeral joint is actually less mobile than those of non-hominoid primates, including the habitually slow-climbing lorines, but it is characterized by a smooth excursion in the scapulocranial direction.     

Kinematic and EMG analysis of horizontal bimanual climbing in humans

Climbing is an increasingly popular recreational and competitive behavior, engaged in a variety of environments and styles. However, injury rates are high in climbing populations, especially in the upper extremity and shoulder. Despite likely arising from an arboreal, climbing ancestor and being closely related to primates that are highly proficient climbers, the modern human shoulder has devolved a capacity for climbing. Limited biomechanical research exists on manual climbing performance. This study assessed kinematic and muscular demands during a bimanual climbing task that mimicked previous work on climbing primates. Thirty participants were recruited – 15 experienced and 15 inexperienced climbers. Motion capture and electromyography (EMG) measured elbow, thoracohumeral and trunk angles, and activity of twelve shoulder muscles, respectively, of the right-side while participants traversed across a horizontal climbing apparatus. Statistical parametric mapping was used to detect differences between groups in kinematics and muscle activity. Experienced climbers presented different joint motions that more closely mimicked the kinematics of climbing primates, including more elbow flexion (p = 0.0045) and internal rotation (p = 0.021), and less thoracohumeral elevation (p = 0.046). Similarly, like climbing primates, experienced climbers generally activated the shoulder musculature at a lower percentage of maximum, particularly during the exchange from support to swing and swing to support phase. However, high muscle activity was recorded in all muscles in both participant groups. Climbing experience coincided with a positive training effect, but not enough to overcome the high muscular workload of bimanual climbing. Owing to the evolved primary usage of the upper extremity for low-force, below shoulder-height tasks, bimanual climbing may induce high risk of fatigue-related musculoskeletal disorders.     

The functional morphology of the primate shoulder as revealed by comparative anatomical,osteometric and discriminant function techniques

A background to assessments of the ecological adaptations of fossil primates is the relationship of the detailed shape of bones in living forms to their known locomotor patterns, and this has been here attempted for the shoulder. Within the locomotion of the primates the function of the shoulder varies according to the extent to which the trunk is suspended by the arms. An analysis of the differences in the shoulder muscles has shown that much of their quantitative variation is mechanically in phase with these functional differences. A series of features of the shoulder bones, chosen because of their association with the mechanically meaningful features of the musculature, have been found to vary (a) in association with the known contrasts in locomotion and (b) in such a way as to render more efficient mechanically the associated muscular structure. Investigation of bony dimensions “residual” to such a study has shown that they are not highly correlated with primate locomotion but are, in contrast, associated with the commonly accepted taxonomic grouping of the order. The combination by discriminant functions of such sets of “locomotor” and “residual” dimensions reveals unsuspected information for living primates and might well allow more precise definition of the functional and taxonomic status of a fossil. The experimental testing of functional inferences from morphology is a necessary part of such studies, and preliminary reports of experimental stress analysis utilising the photoelastic technique confirm and reinforce their validity.     

Scapular position in primates

Scapular position affects shoulder mobility, which plays an important role in the upper limb adaptations in primates. However, currently available data on scapular position are unsatisfactory because of the failure to simultaneously consider the relative dimensions of all the three skeletal elements of the shoulder girdle, i.e. the clavicle, the scapula and the thorax. In the present study, the clavicular length and the scapular spine length were measured on preserved cadavers, and the dorsoventral thoracic diameter was measured on scaled radiographs of a wide range of primates, permitting a quantitative comparison of scapular position among primates. It was found that arboreal monkeys have a more dorsally situated scapula than terrestrial ones, but the same difference was not found between terrestrial and arboreal prosimians. Hominoids were found to have the most dorsally situated scapula. Contrary to the slow climbing theory of hominoid evolution, which tries to explain most postcranial specializations of hominoids as adaptations for slow climbing, the scapulae of slow-climbing lorines and Alouatta are much less dorsal than those of the hominoids.     

Foraging patterns of nonhuman primates and the nature of food preferences in man.

1) There are a variety of foraging and dietary patterns among primates; different species have generally obligate food habits. 2) There are a number of convergent dietary patterns among primates that are not taxonomically dependent; closely related species may have very different food habits, while the diets of unrelated forms may be quite similar. 3) At least at a general level, relationships exist between dietary patterns and alimentary tract adaptations. Further comparative studies of the histology of the gut tract of primates in conjunction with detailed and quantitative studies of the food habits of natural populations are needed to determine if more precise dietary/digestive tract relationships exist. Studies of this type should lead to a better understanding of digestive physiology. However, whether we can ever determine the "natural diet" of man by such comparisons, of course, still remains an unanswered question.     

Effects of activity pattern on eye size and orbital aperture size in primates

Among primates, nocturnal species exhibit relatively larger orbital apertures than diurnal species. Most researchers have considered this disparity in orbital aperture size to reflect differences in eye size, with nocturnal primates having relatively large eyes in order to maximize visual sensitivity. Presumed changes in eye size due to shifts in activity pattern are an integral part of theoretical explanations for many derived features of anthropoids, including highly convergent orbits and a postorbital septum. Here I show that despite clear differences in relative orbital aperture size, many diurnal and nocturnal primates do not differ in relative eye size. Among nocturnal primates, relative eye size is influenced by diet. Nocturnal visual predators (e.g., Tarsius, Loris, and Galago moholi) tend to have larger relative eye sizes than diurnal primates. By contrast, nocturnal frugivores (e.g., Perodicticus, Nycticebus, and Cheirogaleus) have relative eye sizes that are comparable to those of diurnal primates. Although some variation in orbital aperture size can be attributed to variation in eye size, both cornea size and orbit orientation also exert a strong influence on orbital aperture size. These findings argue for caution in the use of relative orbital aperture size as an indicator of activity pattern in fossil primates. These findings further suggest that existing scenarios for the evolution of unique orbital morphologies in anthropoids must be modified to reflect the importance of ecological variables other than activity pattern.     

Air trapping and arboreal locomotor adaptation in primates: a review of experiments on humans

A review was made of experiments on humans in which air trapping by glottis closure during three-dimensional movements were examined in four subjects including former Olympic gymnasts. In brachiation and horizontal bar exercises, the behaviour of the larynx was monitored with a fiberoptic endoscope, and EMG-data were recorded from shoulder muscles. The results revealed that immobilization of the polyaxial connection between the shoulder girdle and the thorax by air trapping occurs in phases of extreme loading of the upper limbs. The closure of the airway by the larynx in humans serves three functions: first, the prevention of errors in deglutition; second, the production of vocal sounds; third, the retention of air inside the thoracic cavity. The latter function, air trapping, allows the immobilization of the rib cage for the muscular fixation of the shoulder blade on the trunk in movements that imply unusually high external forces acting on the upper limbs. This morphological-functional innovation probably has been made when early mammals invaded the three dimensional arboreal habitat, because it gave the tree-dwelling early primates the device to anchor themselves by the arms alone and to avoid falling out of trees. The specific functional characteristic of primates is the hermetic closure of the vocal and vestibular folds by rapidly contracting muscles in the folds. So the closure of the glottis, which in humans seems primarily an adaptation to the production of vocal tones, seems to go back to the adaptation of Tertiary arboreal primates to movements in a three-dimensional environment. Our conclusions are in agreement with the results of other contributions to this volume.     

Expression of Myosin Heavy Chain Isoforms in the Supraspinatus Muscle of Different Primate Species: Implications for the Study of the Adaptation of Primate Shoulder Muscles to Different Locomotor Modes

The supraspinatus muscle is a key component of the soft tissues of the shoulder. In pronograde primates, its main function, in combination with the other rotator cuff muscles (subscapularis, infraspinatus, and teres minor), is to stabilize the glenohumeral joint, whereas in orthograde primates it functions together with the deltoid, to elevate the upper extremity in the scapular plane. To determine whether these functional differences are also reflected in the molecular biochemistry of the supraspinatus muscles involved in these different locomotor modes, we used real-time polymerase chain reaction (RT-PCR) to analyze the expression of the myosin heavy chain (MHC) isoforms in supraspinatus muscles from modern humans and 12 species of pronograde and orthograde primates. The MHC expression pattern in the supraspinatus muscle of pronograde primates was consistent with its function as a tonic and postural muscle, whereas the MHC expression pattern observed in the supraspinatus muscle of nonhuman orthograde primates was that of a muscle that emphasizes speed, strength, and less resistance to fatigue. These findings are consistent with the role of the supraspinatus in the posture and locomotor modes of these groups of nonhuman primates. The humans included in the study had an expression pattern similar to that of the nonhuman orthograde primates. In conclusion, molecular analysis of skeletal muscles via RT-PCR can contribute to a better understanding of the morphological and functional characteristics of the primate musculoskeletal system.     

懒猴肩关节的多变量分析

在懒猴与其它灵长类肩关节局部解剖的基础上,对肩关节有关指数的多变量分析结果表明,与骨骼相比,肩关节肌的种间差别明显较大。肩胛盂宽指数、肩胛骨指数和锁肱指数对种的区分有重要意义。懒猴具有类似于叶猴三角肌、大圆肌和喙肱中肌较远的止点及发达的背阔肌和斜方肌颅侧部,增强了肩关节的运动,表现出适应树栖四足运动的特征。而懒猴粗壮的肱骨、较长的锁骨和较长的肱骨,是攀爬型和四足倒挂运动的适应结果。     

Conflict Among Individual Mitochondrial Proteins in Resolving the Phylogeny of Eutherian Orders

The phylogenetic relationship among primates, ferungulates (artiodactyls + cetaceans + perissodactyls + carnivores), and rodents was examined using proteins encoded by the H strand of mtDNA, with marsupials and monotremes as the outgroup. Trees estimated from individual proteins were compared in detail with the tree estimated from all 12 proteins (either concatenated or summing up log-likelihood scores for each gene). Although the overall evidence strongly suggests ((primates, ferungulates), rodents), the ND1 data clearly support another tree, ((primates, rodents), ferungulates). To clarify whether this contradiction is due to (1) a stochastic (sampling) error; (2) minor model-based errors (e.g., ignoring site rate variability), or (3) convergent and parallel evolution (specifically between either primates and rodents or ferungulates and the outgroup), the ND1 genes from many additional species of primates, rodents, other eutherian orders, and the outgroup (marsupials + monotremes) were sequenced. The phylogenetic analyses were extensive and aimed to eliminate the following artifacts as possible causes of the aberrant result: base composition biases, unequal site substitution rates, or the cumulative effects of both. Neither more sophisticated evolutionary analyses nor the addition of species changed the previous conclusion. That is, the statistical support for grouping rodents and primates to the exclusion of all other taxa fluctuates upward or downward in quite a tight range centered near 95% confidence. These results and a site-by-site examination of the sequences clearly suggest that convergent or parallel evolution has occurred in ND1 between primates and rodents and/or between ferungulates and the outgroup. While the primate/rodent grouping is strange, ND1 also throws some interesting light on the relationships of some eutherian orders, marsupials, and montremes. In these parts of the tree, ND1 shows no apparent tendency for unexplained convergences. Received: 5 December 1997 / Accepted: 24 February 1998     

Origins of primate locomotion: gait mechanics of the woolly opossum

The locomotion of primates differs from that of other mammals in three fundamental ways. During quadrupedal walking, primates use diagonal sequence gaits, protract their arms more at forelimb touchdown, and experience lower vertical substrate reaction forces on their forelimbs relative to their hindlimbs. It is widely held that the unusual walking gaits of primates represent a basal adaptation for movement on thin, flexible branches and reflect a major change in the functional role of the forelimb. However, little data on nonprimate arboreal mammals exist to test this notion. To that end, we examined the gait mechanics of the woolly opossum (Caluromys philander), a marsupial convergent with small-bodied prosimians in ecology, behavior, and morphology. Data on the footfall sequence, relative arm protraction, and peak vertical substrate reaction forces were obtained from videotapes and force records for three adult woolly opossums walking quadrupedally on a wooden runway and a thin pole. For all steps recorded on both substrates, woolly opossums always used diagonal sequence walking gaits, protracted their arms beyond 90 degrees relative to horizontal body axis, and experienced peak vertical substrate reaction forces on forelimbs that were significantly lower than on hindlimbs. The woolly opossum is the first nonprimate mammal to show locomotor mechanics that are identical to those of primates. This case of convergence between primates and a committed fine-branch, arboreal marsupial strongly implies that the earliest primates evolved gait specializations for fine-branch locomotion, which reflect important changes in forelimb function.     

Morphometric affinities of the human shoulder

To analyze differences between apes and monkeys and the affinities of man, we have studied the shoulder girdle of 327 specimens of anthropoid primates. The scapula, clavicle and humerus are viewed as an integrated functional complex on the basis of 18 measurements. Several varieties of multivariate analysis show that man is clearly closer to other hominoids than to the included monkey taxa (whether terrestrial or arboreal, Old World or New World). The marked shoulder differences between apes and monkeys and similarities between apes and man correlate with the muscular anatomy, which in hominoids allows the motions involved in their locomotion and feeding behavior. As the hominid-pongid correspondence in shoulder morphology is especially detailed regarding the functionally important joint surfaces, it is consistent with a fairly recent period of common ancestry and behavior. No hypothetical evolutionary pathway or ancestral form of the human shoulder need look far beyond the model afforded by extant pongids. In contrast with previous studies on the primate shoulder, these results agree with information accumulating from other systems—comparative anatomy, primate behavior, and molecular biology — in suggesting very close relationship between man and extant African pongids.     

The range of passive arm circumduction in primates: Do hominoids really have more mobile shoulders?

Hominoids and lorines are assumed to possess greater shoulder mobility than other primates. This assumption is based on morphological characteristics of the shoulder, rather than on empirical data. However, recent studies have shown that the glenohumeral joint of hominoids is not more mobile than that of other primates (Chan LK. 2007. Glenohumeral mobility in primates. Folia Primatol (Basel) 78(1):1–18), and the thoracic shape of hominoids does not necessarily promote shoulder mobility (Chan LK. 2007. Scapular position in primates. Folia Primatol (Basel) 78(1):19–35). Moreover, lorines differ significantly from hominoids in both these features, thus challenging the assumption that both hominoids and lorines have greater shoulder mobility. The present study aims to test this assumption by collecting empirical data on shoulder mobility in 17 primate species. Passive arm circumduction (a combination of glenohumeral and pectoral girdle movement) was performed on sedated subjects (except humans), and the range measured on the video images of the circumduction. The motion differed among primate species mostly in the craniodorsal directions, the directions most relevant to the animal's ability to brachiate and slow climb. Hylobatids possessed the highest craniodorsal mobility among all primate species studied. However, nonhylobatid hominoids did not have greater craniodorsal mobility than arboreal quadrupedal monkeys, and lorines did not have greater craniodorsal mobility than arboreal quadrupedal prosimians. Nonhylobatid hominoids and lorines had similar craniodorsal mobility, but this was due to a longer clavicle, more dorsal scapula, and lower glenohumeral mobility in the former, and a shorter clavicle, less dorsal scapula, and greater glenohumeral mobility in the latter. This study provides evidence for the reexamination of the brachiation, slow climbing, and vertical climbing hypotheses. Am J Phys Anthropol, 2008. © 2008 Wiley‐Liss, Inc.     

Septa and processes: convergent evolution of the orbit in haplorhine primates and strigiform birds

According to the “nocturnal visual predation hypothesis” (NVPH), the convergent eyes and orbits of primates result from selection for improved stereoscopic depth perception to facilitate manual capture of prey at night. Within primates, haplorhines share additional derived orbital morphologies, including a postorbital septum and greater orbital convergence than any other mammalian clade. While the homology and function of the haplorhine septum remain controversial, experimental data suggest that septa evolved to inhibit mechanical disturbance of the orbital contents by the anterior temporalis muscle during mastication. According to this “insulation hypothesis,” haplorhines are particularly susceptible to disruption of the orbital contents because they have large and highly convergent eyes and orbits. However, comparative tests of the insulation hypothesis have been hindered by the morphological uniqueness of the haplorhine septum among mammals. Among birds, owls (Strigiformes) exhibit an expanded postorbital process that may be functionally analogous to the haplorhine septum. Here we present a comparative analysis of orbital morphology in 103 avian species that tests two hypotheses: (1) large, convergent orbits are associated with nocturnal visual predation, and (2) the strigiform postorbital process and haplorhine postorbital septum similarly function to insulate the eyes from contractions of mandibular adductors. Strigiforms, as nocturnal visual predators, possess relatively large orbits and exhibit the highest degree of orbital convergence in our sample. Notably, orbital convergence does not scale with orbit size in birds as in mammals. Owls are also unique among the birds examined in possessing extensive, plate-like postorbital processes that largely isolate the orbits from the temporal fossae. Furthermore, dissections of four owl species demonstrate that the expanded strigiform postorbital process deflects the path of mandibular adductors around the eye's inferolateral margin. These findings provide further comparative support for both the NVPH and the insulation hypothesis.     

Convergent evolution of escape from hepaciviral antagonism in primates

The ability to mount an interferon response on sensing viral infection is a critical component of mammalian innate immunity. Several viruses directly antagonize viral sensing pathways to block activation of the host immune response. Here, we show that recurrent viral antagonism has shaped the evolution of the host protein MAVS--a crucial component of the viral-sensing pathway in primates. From sequencing and phylogenetic analyses of MAVS from 21 simian primates, we found that MAVS has evolved under strong positive selection. We focused on how this positive selection has shaped MAVS' susceptibility to Hepatitis C virus (HCV). We functionally tested MAVS proteins from diverse primate species for their ability to resist antagonism by HCV, which uses its protease NS3/4A to cleave human MAVS. We found that MAVS from multiple primates are resistant to inhibition by the HCV protease. This resistance maps to single changes within the protease cleavage site in MAVS, which protect MAVS from getting cleaved by the HCV protease. Remarkably, most of these changes have been independently acquired at a single residue 506 that evolved under positive selection. We show that "escape" mutations lower affinity of the NS3 protease for MAVS and allow it to better restrict HCV replication. We further show that NS3 proteases from all other primate hepaciviruses, including the highly divergent GBV-A and GBV-C viruses, are functionally similar to HCV. We conclude that convergent evolution at residue 506 in multiple primates has resulted in escape from antagonism by hepaciviruses. Our study provides a model whereby insights into the ancient history of viral infections in primates can be gained using extant host and virus genes. Our analyses also provide a means by which primates might clear infections by extant hepaciviruses like HCV.     

Mapping bone cell distributions to assess ontogenetic origin of primate midfacial form

Midfacial reduction in primates has been explained as a byproduct of other growth patterns, especially the convergent orbits. This is at once an evolutionary and developmental explanation for relatively short snouts in most modern primates. Here, we use histological sections of perinatal nonhuman primates (tamarin, tarsier, loris) to investigate how orbital morphology emerges during ontogeny in selected primates compared to another euarchontan (Tupaia glis). We annotated serial histological sections for location of osteoclasts or osteoblasts, and used these to create three‐dimensional “modeling maps” showing perinatal growth patterns of the facial skeleton. In addition, in one specimen we transferred annotations from histological sections to CT slices, to create a rotatable 3D volume that shows orbital modeling. Our findings suggest that growth in the competing orbital and neurocranial functional matrices differs among species, influencing modeling patterns. Distinctions among species are observed in the frontal bone, at a shared interface between the endocranial fossa and the orbit. The medial orbital wall is extensively resorptive in primates, whereas the medial orbit is generally depositional in Tupaia. As hypothesized, the orbital soft tissues encroach on available interorbital space. However, eye size cannot, by itself, explain the extent of reduction of the olfactory recess. In Loris, the posterior portion of medial orbit differed from the other primates. It showed evidence of outward drift where the olfactory bulb increased in cross‐sectional area. We suggest the olfactory bulbs are significant to orbit position in strepsirrhines, influencing an expanded interorbital breadth at early stages of development. Am J Phys Anthropol 154:424–435, 2014. © 2014 Wiley Periodicals, Inc.     

Brief communication: Blue eyes in lemurs and humans: Same phenotype,different genetic mechanism

Almost all mammals have brown or darkly‐pigmented eyes (irises), but among primates, there are some prominent blue‐eyed exceptions. The blue eyes of some humans and lemurs are a striking example of convergent evolution of a rare phenotype on distant branches of the primate tree. Recent work on humans indicates that blue eye color is associated with, and likely caused by, a single nucleotide polymorphism (rs12913832) in an intron of the gene HERC2, which likely regulates expression of the neighboring pigmentation gene OCA2. This raises the immediate question of whether blue eyes in lemurs might have a similar genetic basis. We addressed this by sequencing the homologous genetic region in the blue‐eyed black lemur (Eulemur macaco flavifrons; N = 4) and the closely‐related black lemur (Eulemur macaco macaco; N = 4), which has brown eyes. We then compared a 166‐bp segment corresponding to and flanking the human eye‐color‐associated region in these lemurs, as well as other primates (human, chimpanzee, orangutan, macaque, ring‐tailed lemur, mouse lemur). Aligned sequences indicated that this region is strongly conserved in both Eulemur macaco subspecies as well as the other primates (except blue‐eyed humans). Therefore, it is unlikely that this regulatory segment plays a major role in eye color differences among lemurs as it does in humans. Although convergent phenotypes can sometimes come about via the same or similar genetic changes occurring independently, this does not seem to be the case here, as we have shown that the genetic basis of blue eyes in lemurs differs from that of humans. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.