The morphogenesis of the scapula of Tupaia belangeri

The therian scapula was until now thought to show very primitive features during early morphogenesis, as are found in the scapula of adult monotremes (elevated position of the scapula, lack of a spina and a fossa supraspinata, laterally directed cavitas glenoidalis). A morphogenetic study of the scapula of Tupaia belangeri has proved some of these assumptions to be wrong. The scapula undergoes a tilting which shifts its angulus articularis cranially, but no descent of the scapula could be found. The supraspinous fossa, which was supposed to develop very late in ontogeny from the anterior border of the scapula (Lewis 1902, Cheng 1955), is present in Tapaiai from the start. Part of it ossifies in membrane. The scapular spine does not develop as a cartilaginous outgrowth from the anterior border, but is formed mainly as an appositional bone along the lateral surface of the scapula. The glenoid cavity and the humerus are initially directed laterally. They attain their definitive form after the heart has migrated downward and the arms have been adducted. This represents a true plesiomorphous character state in therian ontogeny.     

Load transfer across the scapula during humeral abduction

Stress analysis in the individual parts of the scapula under normal physiological conditions is necessary to understand the load transfer mechanism, its relation with morphology of bone and to analyse the deviations in stress patterns due to implantation of the glenoid. The purpose of this study was to obtain stress distribution in the scapula during abduction of the arm and to obtain a qualitative estimate of the function of coracoacromial ligament. An accurate three-dimensional (3D) finite element (FE) model of the natural scapula has been developed for this purpose, using computed tomography data and shell-solid modelling approach. The model was experimentally validated. A musculoskeletal shoulder model of forces that calculates all muscle, ligament and joint reaction forces, in six load cases (30-180 degrees) during unloaded humeral abduction was used as applied loading conditions for the 3D FE model. High tensile and compressive stresses (15-60 MPa) were generated in the thick bony ridges of the scapula, like the scapular spine, lateral border, glenoid and acromion. High compressive stresses (45-58 MPa) were evoked in the glenoid and at the connection of glenoid-scapular spine-infraspinous fossa. The stresses in the infraspinous fossa and supraspinous fossa were low (0.05-15 MPa). These results indicated that the transfer of major muscle and joint reaction take place predominantly through the thick bony ridges, whereas the fossa area act more as attachment sites of large muscles. During humeral abduction, coracoacromial ligament was stretched, and presumably will be under tension.     

A Comparison of Qualitative and Quantitative Methodological Approaches to Characterizing the Dorsal Side of the Scapula in Hominoidea and Its Relationship to Locomotion

Hominoidea have adapted to various forms of locomotion, each of which has specific requirements that are reflected in the shape of the scapula. We compared several qualitative and quantitative methods for characterizing the dorsal side of the scapula to detect morphological differences that reflect the adaptations of the scapula to locomotor behaviors. Our sample included 55 specimens of Hominoidea, representing five genera, including Homo, focusing specifically on the relative sizes of the scapular supraspinous and infranspinous fossae. In addition, we weighed the supraspinatus and infraspinatus muscles of 23 of the specimens to examine the feasibility of extrapolating muscle characteristics from osteological data. Our findings confirmed that the five genera exhibit significant differences in the relative size of the supraspinous and the infraspinous fossae that are related to their forms of locomotion. The supraspinous fossa was relatively small in Homo and Pongo but large in Pan, Gorilla, and Hylobates. The analysis of muscle weights showed that a substantial amount of information about soft tissues is lost in osteological analyses, leading us to recommend caution when drawing conclusions regarding forms of locomotion based only on osteological analyses.     

Sex determination using the scapula in New Kingdom skeletons from Tell El-Amarna

Both forensic and archaeological sciences use metric analysis of human skeletal remains for sex estimation of unknown individuals. Thomas Dwight first reported the utility of scapula metrics for sex estimation in 1894, and subsequent years have produced several techniques for sex estimation using scapula metrics. Levels of sexual dimorphism vary across time and space, making these methods not universally applicable. Novel discriminant functions for unique populations are thus necessary. The present study establishes metric standards for sex estimation for a New Kingdom Egyptian skeletal sample from Tell El-Amarna using scapular measurements. The sample for this research consists of 27 individuals (14 males; 13 females) whose sex estimate based on pelvic morphology is unambiguous. The five measurements showing the highest degree of sexual dimorphism (p ≤ 0.001) are used in the discriminant functions reported here: maximum length of the scapula, maximum length of the scapular spine, breadth of the infraspinous body, height of the glenoid fossa, and breadth of the glenoid fossa. The overall leave one out, cross-validated accuracy for the five reported discriminant functions ranges from 84.0 to 88.0%; similar to accuracies reported for the femur and humerus. Functions combining multiple variables produce higher accuracies than those based on single measurements. The unique population of Amarna, being comprised of emigrants from throughout Egypt, suggests these discriminant functions will have utility for Amarna period sites across the spatial distances of Egypt, and possibly the temporal range of the New Kingdom as a whole.     

Musculoskeletal scapular correlates of plantigrade and acrobatic positional activities in Papio cynocephalus anubis and Macaca fascicularis

This study investigates several musculoskeletal scapular correlates of quadrupedal behavior in predominantly plantigrade, Papio cynocephalus anubis and acrobatic, less plantigrade, Macaca fascicularis. Positional behaviors differ in these two primates reflecting the amount of time spent emphasizing one or the other of these captive behavioral regimes. Stresses associated with particular patterns of behavior result in different scapular morphologies. Papio exhibits a significantly broader scapula with a more dorsoventrally curved blade accompanying an enlarged teres major muscle. The supraspinous fossa is wider in Papio, while the infraspinous/teres major attachment is wider in Macaca. Angular measurements reflect the breadth dimension of the various fossae. These results utilize two species of primates to extend a methodology developed in previous studies and to suggest that a predictable interdependence occurs between scapular dimensions and certain behavioral activities.     

Rotator cuff muscle function and its relation to scapular morphology in apes

It is widely held that many differences among primate species in scapular morphology can be functionally related to differing demands on the shoulder associated with particular locomotor habits. This perspective is largely based on broad scale studies, while more narrow comparisons of scapular form often fail to follow predictions based on inferred differences in shoulder function. For example, the ratio of supraspinous fossa/infraspinous fossa size in apes is commonly viewed as an indicator of the importance of overhead use of the forelimb, yet paradoxically, the African apes, the most terrestrial of the great apes, have higher scapular fossa ratios than the more suspensory orangutan. The recent discovery of several nearly complete early hominin scapular specimens, and their apparent morphological affinities to scapulae of orangutans and gorillas rather than chimpanzees, has led to renewed interest in the comparative analysis of human and extant ape scapular form. To facilitate the functional interpretation of differences in ape scapulae, particularly in regard to relative scapular fossa size, we used electromyography (EMG) to document the activity patterns in all four rotator cuff muscles in orangutans and gibbons, comparing the results with previously published data for chimpanzees.     

Effects of attachment position and shoulder orientation during calibration on the accuracy of the acromial tracker

The acromial tracker is used to measure scapular rotations during dynamic movements. The method has low accuracy in high elevations and is sensitive to its attachment location on the acromion. The aim of this study was to investigate the effect of the attachment position and shoulder orientation during calibration on the tracker accuracy. The tracker was attached to one of three positions: near the anterior edge of the acromion process, just above the acromial angle and the meeting point between the acromion and the scapular spine. The scapula locator was used to track the scapula during bilateral abduction simultaneously. The locator was used to calibrate the tracker at: no abduction, 30°, 60°, 90° and 120° humerothoracic abduction. ANOVA tests compared RMS errors for different attachment positions and calibration angles. The results showed that attaching the device at the meeting point between the acromion and the scapular spine gave the smallest errors and it was best to calibrate the device at 60° for elevations ≤90°, at 120° for elevations >90° and at 90°or 120° for the full range of abduction. The accuracy of the tracker is significantly improved if attached appropriately and calibrated for the range of movement being measured.     

Crouched posture and high fulcrum, a principle in the locomotion of small mammals: The example of the rock hyrax (Procavia capensis) (Mammalia: Hyracoidea)

The cineradiographic study of the locomotion of the rock hyrax (Procavia capensis) and the functional interpretation of its locomotory system, reveals that the main action of proximal segments is combined with flexed position and low movements of limb joints. This observation can be applied to the locomotion of other small mammals. In the forelimb, scapular rotation and translation account for more than 60% of step length. Effective shoulder joint movements are mostly restricted to less than 20°, and elbow movements range mainly between 20°-50°. The detachment of the shoulder girdle of therian mammals from the axial skeleton, and development of a supraspinous fossa, are correlated with movements at a high scapular fulcrum. Movements at such a high fulcrum are in interdependency with a crouched posture. Only flexed limbs can act as shock absorbers and prevent vertical changes in the center of gravity. Basic differences in forelimb movements exist between larger primates (humeral retraction) and smaller mammals (scapula retraction). In the hyrax, propulsion is due mainly to hip joint movements in symmetrical gaits, but sagittal lumbar spine movements play the dominant role at in-phase gaits. Joint and muscular anatomy, especially of the shoulder region, are discussed in view of the kinematic data.     

Reconciling the convergence of supraspinous fossa shape among hominoids in light of locomotor differences

Differences in scapular morphology between modern humans and the African and lesser apes are associated with the distinct locomotor habits of these groups. However, several traits, particularly aspects of the supraspinous fossa, are convergent between Homo and Pongo—an unexpected result given their divergent locomotor habits. Many morphological assessments of the scapula rely on the limited number of static landmarks available, and traditional approaches like these tend to oversimplify scapular shape. Here, we present the results of two geometric morphometric (GM) analyses of hominoid supraspinous fossa shape—one employing five homologous landmarks and another with 83 sliding semilandmarks—alongside those of traditional methods to evaluate if three-dimensional considerations of fossa shape afford more comprehensive insights into scapular shape and functional morphology. Traditional measures aligned Pongo and Homo with narrow and transversely oriented supraspinous fossae, whereas African ape and Hylobates fossae are broader and more obliquely situated. However, our GM results highlight that much of the convergence between Homo and Pongo is reflective of their more medially positioned superior angles. These approaches offered a more complete assessment of supraspinous shape and revealed that the Homo fossa, with an intermediate superior angle position and moderate superoinferior expansion, is actually reminiscent of the African ape shape. Additionally, both Pongo and Hylobates were shown to have more compressed fossae, something that has not previously been identified through traditional analyses. Thus, the total morphological pattern of the Pongo supraspinous fossa is unique among hominoids, and possibly indicative of its distinctive locomotor habits. Am J Phys Anthropol 156:498–510, 2015. © 2015 Wiley Periodicals, Inc.     

A comparison of the ontogeny of shape variation in the anthropoid scapula: functional and phylogenetic signal

This article compares ontogenetic shape variation in the scapula of 17 anthropoid species using three-dimensional landmark-based geometric morphometrics. These data are used to investigate functional and phylogenetic signal in the major components of scapular variation and to evaluate the degree to which postnatal growth contributes to interspecific differences in shape. Results indicate that the shape of the infant and adult scapula is primarily associated with positional behavior (e.g., orthograde suspensory nonquadrupeds versus pronograde quadrupeds), but within this functional structure there is phylogenetic signal, particularly at infant stages. Growth most closely correlates with infant/adult shape and locomotor function. These results suggest that the shape of the infant scapula drives the pattern of postnatal scapular growth and adult morphology. As such, variation in postnatal growth is not the primary source of interspecific variation in adult shape. Instead, interspecific differences in scapular morphology are hypothesized to be the result of selection for variation in embryonic developmental processes that affect shape.     

3D reconstructions of quail–chick chimeras provide a new fate map of the avian scapula

Limbed vertebrates have functionally integrated postcranial axial and appendicular systems derived from two distinct populations of embryonic mesoderm. The axial skeletal elements arise from the paraxial somites, the appendicular skeleton and sternum arise from the somatic lateral plate mesoderm, and all of the muscles for both systems arise from the somites. Recent studies in amniotes demonstrate that the scapula has a mixed mesodermal origin. Here we determine the relative contribution of somitic and lateral plate mesoderm to the avian scapula from quail-chick chimeras. We generate 3D reconstructions of the grafted tissue in the host revealing a very different distribution of somitic cells in the scapula than previously reported. This novel 3D visualization of the cryptic border between somitic and lateral plate populations reveals the dynamics of musculoskeletal morphogenesis and demonstrates the importance of 3D visualization of chimera data. Reconstructions of chimeras make clear three significant contrasts with existing models of scapular development. First, the majority of the avian scapula is lateral plate derived and the somitic contribution to the scapular blade is significantly smaller than in previous models. Second, the segmentation of the somitic component of the blade is partially lost; and third, there are striking differences in growth rates between different tissues derived from the same somites that contribute to the structures of the cervical thoracic transition, including the scapula. These data call for the reassessment of theories on the development, homology, and evolution of the vertebrate scapula.     

3D Morphometric and posture study of felid scapulae using statistical shape modelling

We present a three dimensional (3D) morphometric modelling study of the scapulae of Felidae, with a focus on the correlations between forelimb postures and extracted scapular shape variations. Our shape modelling results indicate that the scapular infraspinous fossa becomes larger and relatively broader along the craniocaudal axis in larger felids. We infer that this enlargement of the scapular fossa may be a size-related specialization for postural support of the shoulder joint.     

The scapulocoracoid of the Queensland lungfish Neoceratodus forsteri (Dipnoi: Sarcopterygii): morphology, development and evolutionary implications for bony fishes (Osteichthyes)

Among bony fishes, the ontogenetic sequence by which the actinopterygian scapulocoracoid develops has been well described, but that of the sarcopterygian scapulocoracoid is poorly known, as the majority of taxa are only known from fossils. To rectify this, the cartilaginous scapulocoracoid of the extant lungfish Neoceratodus forsteri is examined. In initial stages of its development, the scapulocoracoid of Neoceratodus has a simple rounded shape, and supports the glenoid fossa. It appears nearly contemporaneously with the proximal endochondral element (humerus) of the pectoral fin. Pectoral fin elements develop by segmentation from a continuous field of cartilaginous precursor cells extending distally from the glenoid region of the scapulocoracoid. Subsequent scapulocoracoid development produces a ventromedial process, which is not associated with this field of precursor cells. A dorsal process also develops outside this field. Thus, the scapulocoracoid of Neoceratodus may consist of at least two developmentally distinct regions; (1) the ventromedial being homologous with the coracoid of actinopterygians, tetrapods and other jawed vertebrates and (2) a smaller dorsal process, homologous to the scapular region. The two, together with the glenoid region, give an overall triangular shape. The scapulocoracoids of fossil lungfish and other sarcopterygian fishes are also triangular and are composed of scapular and coracoid regions, rather than the 'buttresses' associated with scapulocoracoids of the Actinopterygii and Tetrapoda.     

Tracking the scapula using the scapula locator with and without feedback from pressure-sensors: A comparative study

BackgroundThe scapula locator method has associated intra-observer and inter-observer errors caused by the dependency on the observer to locate the scapular landmarks. The potential effect of the pressures applied by the observer on the measured scapular kinematics when this method is used has also been overlooked so far. The aim of this study was to investigate the effect of using feedback on the pressures applied on the scapula using the locator on the intra-observer and inter-observer reliabilities of the method as well as on the kinematics obtained using this method.MethodsThree observers tracked the scapular motion of the dominant shoulder of each subject using the locator with no reference to pressure-feedback for three trials of bilateral elevation in the scapular plane and using the locator with pressure-feedback for three other trials. Variations between the measurements obtained were used to calculate the intra-observer errors and variations between the measurements obtained by the three observers for the same subject were used to calculate inter-observer errors. Repeated-measures ANOVA tests were used to look at differences between the two methods in terms of intra-observer and inter-observer errors and scapular kinematics.FindingsUsing pressure-feedback reduced the intra-observer errors but had no effect on the inter-observer errors. Different scapular kinematics was measured using the two methods.InterpretationsPressure-feedback improves the reliability of the scapula locator method. Differences in the scapular kinematics suggest that unregulated pressures have an effect on the physiological scapular motion.     

Geometric morphometrics of the scapula of South American caviomorph rodents (Rodentia: Hystricognathi): Form, function and phylogeny

The scapula of the ecomorphologically diverse South American caviomorph rodents was studied through geometric morphometric techniques, using landmarks and semilandmarks to capture the shape of this complex morphological structure. Representatives of 33 species from all caviomorph superfamilies, as well as Hystrix cristata for comparisons, were analyzed. Marked differences in scapular shape were found among the major caviomorph lineages analyzed, particularly in the shape and length of the scapular spine and development of the great scapular notch. Shape differences were not influenced by body size, and only partially influenced by locomotor mode. Thus, at this scale of analysis, phylogenetic history seems to be the strongest factor influencing scapular shape. The scapular shape of erethizontids, chinchillids and Cuniculus paca could represent the less specialized state with respect to the highly differentiated scapula of octodontoids and most cavioids. In this sense, the characteristic scapular morphologies of octodontoids and cavioids could reflect particular functional capabilities and constraints associated with the evolution of prevalent locomotor modes within each lineage.     

On the phylogenetic position of monotremes (Mammalia,Monotremata)

Henosferida from the Middle-Upper Jurassic of Western Gondwana is the most probable sister group for monotremes. They share the derived pretribosphenic structure of lower molars combined with the presumably absent protocone on the upper molars and the plesiomorphic retention of postdentary bones and pseudangular process of the lower jaw. In addition, the two groups share the dental formula with three molars and the position of the Meckel’s groove, which passes ventral to the mandibular foramen. In the course of subsequent evolution, monotremes acquired the mammalian middle ear with three auditory ossicles independently of therian mammals and multituberculates. Jurassic Laurasian Shuotheriidae are probably a sister group of the Gondwanian clade Henosferida + Monotremata. The Jurassic shuotheriid Pseudotribos shows a great plesiomorphic similarity to monotremes in the structure of the pectoral girdle, with a large interclavicle immovably connected to the clavicle. In the lineages leading to therian mammals and multituberculates, the pectoral girdle changed probably independently and in parallel in connection with the establishment of the parasagittal posture of the forelimbs (reduction of the interclavicle, mobile articulation of the interclavicle with clavicle, reduction of the procoracoid, and development of a supraspinous fossa of the scapula) and formation of the mammalian middle ear with three auditory ossicles.     

Assessment of scapular morphology and bone quality with statistical models

The design of total shoulder arthroplasty implants are guided by anatomy. The objective of this study was to develop statistical models to quantify shape and material property variation in the scapula. Material-mapped models were reconstructed from CT scans for a training set of subjects. Statistical shape (SSM) and intensity (SIM) models were created; SSM modes described scaling, changes in the medial border and acromial process, and elongation of the scapular blade. SIM modes captured bone quality changes in the anterior and inferior glenoid. Bone quality was independent of scapular morphology. Variation described by the statistical representations can inform implant design and sizing.     

Evolution of the turtle bauplan: the topological relationship of the scapula relative to the ribcage

The turtle shell and the relationship of the shoulder girdle inside or ‘deep’ to the ribcage have puzzled neontologists and developmental biologists for more than a century. Recent developmental and fossil data indicate that the shoulder girdle indeed lies inside the shell, but anterior to the ribcage. Developmental biologists compare this orientation to that found in the model organisms mice and chickens, whose scapula lies laterally on top of the ribcage. We analyse the topological relationship of the shoulder girdle relative to the ribcage within a broader phylogenetic context and determine that the condition found in turtles is also found in amphibians, monotreme mammals and lepidosaurs. A vertical scapula anterior to the thoracic ribcage is therefore inferred to be the basal amniote condition and indicates that the condition found in therian mammals and archosaurs (which includes both developmental model organisms: chickens and mice) is derived and not appropriate for studying the developmental origin of the turtle shell. Instead, among amniotes, either monotreme mammals or lepidosaurs should be used.     

Dual origin and segmental organisation of the avian scapula

Bones of the postcranial skeleton of higher vertebrates originate from either somitic mesoderm or somatopleural layer of the lateral plate mesoderm. Controversy surrounds the origin of the scapula, a major component of the shoulder girdle, with both somitic and lateral plate origins being proposed. Abnormal scapular development has been described in the naturally occurring undulated series of mouse mutants, which has implicated Pax1 in the formation of this bone. Here we addressed the development of the scapula, firstly, by analysing the relationship between Pax1 expression and chondrogenesis and, secondly, by determining the developmental origin of the scapula using chick quail chimeric analysis. We show the following. (1) The scapula develops in a rostral-to-caudal direction and overt chondrification is preceded by an accumulation of Pax1-expressing cells. (2) The scapular head and neck are of lateral plate mesodermal origin. (3) In contrast, the scapular blade is composed of somitic cells. (4) Unlike the Pax1-positive cells of the vertebral column, which are of sclerotomal origin, the Pax1-positive cells of the scapular blade originate from the dermomyotome. (5) Finally, we show that cells of the scapular blade are organised into spatially restricted domains along its rostrocaudal axis in the same order as the somites from which they originated. Our results imply that the scapular blade is an ossifying muscular insertion rather than an original skeletal element, and that the scapular head and neck are homologous to the 'true coracoid' of higher vertebrates.     

Objective classification of scapular kinematics in participants with movement faults of the scapula on clinical assessment

The aim of this study was to assess the potential of employing a classification tool to objectively classify participants with clinically assessed movement faults (MFs) of the scapula. Six participants with a history of shoulder pain with MFs of the scapula and 12 healthy participants with no movement faults (NMFs) performed a flexion movement control test of the scapula, while scapular kinematic data were collected. Principal component scores and discrete kinematic variables were used as input into a classifier. Five out of the six participants with a history of pain were successfully classified as having scapular MFs with an accuracy of 72%. Variables related to the upward rotation of the scapula had the most influence on the classification. The results of the study demonstrate the potential of adopting a multivariate approach in objective classification of participants with altered scapular kinematics in pathological groups.