The morphofunctional implications of the glenoid labrum of the glenohumeral joint in hominoids.

OBJECTIVES: A morphocline of the glenoid cavity has been used to infer differences in locomotor behaviors; however, the glenoid cavity is surrounded by the glenoid labrum, a fibrocartilaginous structure that could influence the functionality of the glenoid. The objectives of this study are to explore the effects of the glenoid labrum on the area, depth, and morphology of the glenoid cavity in primates. MATERIALS AND METHODS: Photogrammetry was used to build 3D models of the glenoid, with and without the labrum, and three- (3D) and two-dimensional (2D) geometric morphometrics (GM) was applied. 2D areas were collected from zenithal images for glenoids with and without labrum to evaluate the availability of articular surface area. RESULTS: In the 2D GM the morphocline is present in the dry-bone sample but not with the presence of the glenoid labrum. In the 3D GM there are differences between species mainly concerning the depth of the glenoid cavity. 2D areas reveal that the amount of articular area of the glenoid cavity increases with the presence of the labrum, particularly in humans. DISCUSSION: The glenoid labrum changes the shape, increases the depth and the surface area of the glenoid cavity, particularly in humans. Therefore, the glenoid labrum might hold a functional role, increasing the stability of the glenohumeral joint of primates in general, and especially in humans.

Trabecular structure of the elbow reveals divergence in knuckle-walking biomechanical strategies of African apes.

African apes engage in a distinct form of locomotion called knuckle-walking, but there is much ambiguity as to when and how this locomotor behavior evolved. This study aims to elucidate potential differences in knuckle-walking elbow posture and loading in African apes through the study of trabecular bone. Using a whole-epiphysis approach, we quantified variation in the trabecular structure of the distal humerus of chimpanzees, western lowland gorillas, and mountain gorillas in comparison to orang-utans, siamangs, and a sample of Old and New World monkeys. Results demonstrate differences in the distribution of trabecular bone within the distal humerus that are consistent across taxa that habitually use a flexed-elbow posture in comparison to those that use an extended elbow during locomotion. Western lowland gorillas show an extended-elbow pattern consistent with the straight forelimb position during knuckle-walking, whereas chimpanzees show a flexed-elbow pattern. Unexpectedly, mountain gorillas show an intermediate pattern between their western counterparts and chimpanzees. The differences found in elbow joint posture between chimpanzees and gorillas, and between gorilla species, point to diversification in the knuckle-walking biomechanical strategies among African apes, which has implications in the debate regarding the locomotor behavior from which human bipedalism arose.

A proximal radius of Barberapithecus huerzeleri from Castell de Barberà: Implications for locomotor diversity among pliopithecoids.

Pliopithecoids are a diverse group of Miocene catarrhine primates from Eurasia. Their positional behavior is still unknown, and many species are known exclusively from dentognathic remains. Here, we describe a proximal radius (IPS66267) from the late Miocene of Castell de Barberà (Vallès-Penedès Basin, NE Iberian Peninsula) that represents the first postcranial specimen of the pliopithecoid Barberapithecus huerzeleri. A body mass estimate based on the radius is compared with dental estimates, and its morphology is compared with that of extant and fossil anthropoids by qualitative means as well as by landmark-based three-dimensional geometric morphometrics. The estimated body mass of ∼5 kg for IPS66267 closely matches the dental estimates for the (female) holotype, thereby discounting an alternative attribution to the large-bodied hominoid recorded at Castell de Barberà. In multiple features (oval and moderately tilted head with a pronounced lateral lip and a restricted articular area for the capitulum; proximodistally expanded proximal radioulnar joint; and short, robust, and anteroposteriorly compressed neck), the specimen differs from hominoids and resembles instead extant nonateline monkeys and stem catarrhines. The results of the morphometric analysis further indicate that the Barberapithecus proximal radius shows closer similarities with nonsuspensory arboreal cercopithecoids and the dendropithecid Simiolus. From a locomotor viewpoint, the radius of Barberapithecus lacks most of the features functionally related to climbing and/or suspensory behaviors and displays instead a proximal radioulnar joint that would have been particularly stable under pronation. On the other hand, the Barberapithecus radius differs from other stem catarrhines in the less anteroposteriorly compressed and less tilted radial head with a deeper capitular fovea, suggesting a somewhat enhanced mobility at the elbow joint. We conclude that pronograde arboreal quadrupedalism was the main component of the locomotor repertoire of Barberapithecus but that, similar to other crouzeliids, it might have displayed better climbing abilities than pliopithecids.

Quantitative shape analysis of the deltoid tuberosity of modern humans (Homo sapiens) and common chimpanzees (Pan troglodytes).

PURPOSE: To identify anatomical differences in the deltoid tuberosity of Homo sapiens and Pan troglodytes, potentially relating to the different uses of the forelimb in these two phylogenetically related species. BASIC PROCEDURES: We have used three-dimensional geometric morphometrics (3D GM) to analyze the deltoid tuberosity of scanned humeri from 30 H. sapiens and 27 P. troglodytes. We also used the 3D scans of the humeri to calculate the surface area of the deltoid tuberosity. Finally, we dissected the deltoid muscles of three H. sapiens and three P. troglodytes to determine the relative mass and the physiological cross-sectional area (PCSA) of each part of the muscle. MAIN FINDINGS: The 3D GM analysis of the deltoid tuberosity identified an anteroposterior enlargement of the P. troglodytes tuberosity, with a lateral displacement of the middle segment, whereas in H. sapiens, there was a distal displacement of the middle segment. Muscle architecture analysis indicated higher normalized values ​​of the PCSA of the clavicular and acromial deltoid in P. troglodytes. PRINCIPAL CONCLUSIONS: The anatomical features observed in our P. troglodytes specimens serve to strengthen the three parts of the deltoid muscle. This fact can be related to the use of the forelimb in locomotion, both arboreal and knuckle-walking, in this species. Humans use the forelimb mainly in manipulative tasks, so they do not develop - as do chimpanzees - the anatomical features that increase the deltoid force. Our findings have shown that the different uses of the forelimb in modern humans and common chimpanzees can affect both muscle architecture and bone morphology, either jointly or separately.

The morphology and evolutionary history of the glenohumeral joint of hominoids: A review.

The glenohumeral joint, the most mobile joint in the body of hominoids, is involved in the locomotion of all extant primates apart from humans. Over the last few decades, our knowledge of how variation in its morphological characteristics relates to different locomotor behaviors within extant primates has greatly improved, including features of the proximal humerus and the glenoid cavity of the scapula, as well as the muscles that function to move the joint (the rotator cuff muscles). The glenohumeral joint is a region with a strong morphofunctional signal, and hence, its study can shed light on the locomotor behaviors of crucial ancestral nodes in the evolutionary history of hominoids (e.g., the last common ancestor between humans and chimpanzees). Hominoids, in particular, are distinct in showing round and relatively big proximal humeri with lowered tubercles and flattened and oval glenoid cavities, morphology suited to engage in a wide range of motions, which enables the use of locomotor behaviors such as suspension. The comparison with extant taxa has enabled more informed functional interpretations of morphology in extinct primates, including hominoids, from the Early Miocene through to the emergence of hominins. Here, I review our current understanding of glenohumeral joint functional morphology and its evolution throughout the Miocene and Pleistocene, as well as highlighting the areas where a deeper study of this joint is still needed.

Expression of myosin heavy chain isoforms mRNA transcripts in the temporalis muscle of common chimpanzees (Pan troglodytes).

PURPOSE: The common chimpanzee (Pan troglodytes) is the primate that is phylogenetically most closely related to humans (Homo sapiens). In order to shed light on the anatomy and function of the temporalis muscle in the chimpanzee, we have analyzed the expression patterns of the mRNA transcripts of the myosin heavy chain (MyHC) isoforms in different parts of the muscle. BASIC PROCEDURES: We dissected the superficial, deep and sphenomandibularis portions of the temporalis muscle in five adult P. troglodytes and quantified the expression of the mRNA transcripts of the MyHC isoforms in each portion using real-time quantitative polymerase chain reaction. MAIN FINDINGS: We observed significant differences in the patterns of expression of the mRNA transcripts of the MyHC-IIM isoform between the sphenomandibularis portion and the anterior superficial temporalis (33.6% vs 47.0%; P=0.032) and between the sphenomandibularis portion and the anterior deep temporalis (33.6% vs 43.0; P=0.016). We also observed non-significant differences between the patterns of expression in the anterior and posterior superficial temporalis. PRINCIPAL CONCLUSIONS: The differential expression patterns of the mRNA transcripts of the MyHC isoforms in the temporalis muscle in P. troglodytes may be related to the functional differences that have been observed in electromyographic studies in other species of primates. Our findings can be applicable to the fields of comparative anatomy, evolutionary anatomy, and anthropology.

Expression of MyHC isoforms mRNA transcripts in different regions of the masseter and medial pterygoid muscles in chimpanzees.

OBJECTIVE: The aim of this study is to examine the expression pattern of the different myosin heavy chain (MyHC) isoforms in the masseter and medial pterygoid muscles by real time quantitative polymerase chain reaction (RT-qPCR) to obtain information at molecular level which can be related to the functional characteristics of these two muscles. DESIGN: The masseter, deep and superficial portion, and medial pterygoid muscles of five adult Pan troglodytes were dissected in order to obtain samples of the anterior and posterior regions of each portion of the masseter and of the medial pterygoid. The expression of MyHC isoforms mRNA transcripts was analyzed by RT-qPCR. RESULTS: No significant differences in expression of MyHC isoforms between the masseter and the medial pterygoid were found. In contrast, when comparing the superficial and the deep portion of the masseter, we found that the MyHC-IIM isoform was expressed at a significantly higher level in the superficial portion. CONCLUSIONS: The superficial portion of the masseter and the medial pterygoid muscle have the same expression pattern regarding the different MyHC isoforms. On the other hand, the deep portion of the masseter, which is activated mainly during lateral and repositioning movements of the mandible, has a lower MyHC-IIM isoform expression than the superficial portion. Our findings provide new data on functional aspects of the masseter and medial pterygoid that can complement results obtained by other techniques.

Quantification of Myosin Heavy Chain Isoform mRNA Transcripts in the Supraspinatus Muscle of Vertical Clinger Primates.

Vertical clinging is a specialized form of locomotion characteristic of the primate family Callitrichidae. Vertical clinging requires these pronograde primates to maintain a vertical posture, so the protraction of their forelimbs must resist gravity. Since pronograde primates usually move as horizontal quadrupeds, we hypothesized that the supraspinatus muscle of vertical clingers would present specific characteristics related to the functional requirements imposed on the shoulder area by vertical clinging. To test this hypothesis, we quantified by real-time quantitative polymerase chain reaction the mRNA transcripts of myosin heavy chain (MHC) isoforms in the supraspinatus muscle of 15 species of pronograde primates, including vertical clingers. Our results indicate that the supraspinatus of vertical clingers has a specific expression pattern of the MHC isoforms, with a low expression of the transcripts of the slow MHC-I isoform and a high expression of the transcripts of the fast MHC-II isoforms. We conclude that these differences can be related to the particular functional characteristics of the shoulder in vertical clingers, but also to other anatomical adaptations of these primates, such as their small body size.

Like father, like son: assessment of the morphological affinities of A.L. 288-1 (A. afarensis), Sts 7 (A. africanus) and Omo 119-73-2718 (Australopithecus sp.) through a three-dimensional shape analysis of the shoulder joint.

The postcranial evidence for the Australopithecus genus indicates that australopiths were able bipeds; however, the morphology of the forelimbs and particularly that of the shoulder girdle suggests that they were partially adapted to an arboreal lifestyle. The nature of such arboreal adaptations is still unclear, as are the kind of arboreal behaviors in which australopiths might have engaged. In this study we analyzed the shape of the shoulder joint (proximal humerus and glenoid cavity of the scapula) of three australopith specimens: A.L. 288-1 (A. afarensis), Sts 7 (A. africanus) and Omo 119-73-2718 (Australopithecus sp.) with three-dimensional geometric morphometrics. The morphology of the specimens was compared with that of a wide array of living anthropoid taxa and some additional fossil hominins (the Homo erectus specimen KNM-WT 15000 and the H. neanderthalensis specimen Tabun 1). Our results indicate that A.L. 288-1 shows mosaic traits resembling H. sapiens and Pongo, whereas the Sts 7 shoulder is most similar to the arboreal apes and does not present affinities with H. sapiens. Omo 119-73-2718 exhibits morphological affinities with the more arboreal and partially suspensory New World monkey Lagothrix. The shoulder of the australopith specimens thus shows a combination of primitive and derived traits (humeral globularity, enhancement of internal and external rotation of the joint), related to use of the arm in overhead positions. The genus Homo specimens show overall affinities with H. sapiens at the shoulder, indicating full correspondence of these hominin shoulders with the modern human morphotype.

Morphological affinities of the proximal humerus of Epipliopithecus vindobonensis and Pliopithecus antiquus: suspensory inferences based on a 3D geometric morphometrics approach.

Suspension plays a major adaptive role in shaping primate postcranial morphology, which therefore enables this positional behavior to be inferred in extinct taxa. The proximal humerus stands as a key region for inferring forelimb suspensory capabilities because its morphology can be effectively linked, from a functional viewpoint, to differences in suspension use between primate taxa. Here we provide an assessment of the suspensory capabilities of two pliopithecoids (Epipliopithecus vindobonensis and Pliopithecus antiquus) by means of a 3D geometric morphometric analysis of proximal humeral shape. The comparative sample includes proximal humeri from eight extant anthropoid genera, as well as other extinct catarrhines (the propliopithecoid Aegyptopithecus zeuxis, the stem hominoid Nyanzapithecus vancouveringorum, and an unascribed small catarrhine, GSP 28062, from the Middle Miocene of Pakistan). Body mass estimates based on allometric regressions of humeral head superoinferior diameter are also provided. Our results support some degree of forelimb suspensory behaviors for Epipliopithecus and GSP 28062. In contrast, and unlike previous qualitative assessments, our analysis shows that P. antiquus has a distinct glenohumeral morphology, much closer to that displayed by generalized arboreal quadrupeds with no evidence of suspensory adaptations (as in Aegyptopithecus and stem hominoids from Africa).

Shape analysis of the proximal humerus in orthograde and semi-orthograde primates: correlates of suspensory behavior.

"Suspensory locomotion" is an expression that encompasses a series of specialized forms of locomotion that mainly orthograde primates use to achieve below-branch traveling. It implies a number of features in the entire body associated with the use of the forelimb in overhead positions. The glenohumeral joint is one of the main joints involved in effective suspensory locomotion, being subject to a delicate balance between the high degree of mobility and stabilization needed to successfully engage in suspensory behaviors. Here, we present a 3D geometric morphometric study that explores the form of the proximal humerus of six orthograde and semi-orthograde genera (Hylobates, Pongo, Pan, Gorilla, Ateles, and Lagothrix) and a pronograde genus, Colobus, to determine to what extent suspensory locomotor requirements are driving the shape of this epiphysis. Results show the presence of a morphocline related to degree of suspension in the shape of the articular surface, with highly suspensory taxa (i.e., Hylobates) exhibiting particular morphological traits at the articular surface that provide a greater range of circumduction. The placement and orientation of the rotator cuff muscles' insertion sites on the tubercles appear associated with the divergent forces operating at the joint in quadrupedal or above-head use of the hand.

Brief communication: Developmental versus functional three-dimensional geometric morphometric-based modularity of the human proximal humerus.

The proximal humerus is formed by three secondary ossification centers during the postnatal trajectory of the human infant. The ossification centers later grow into the structures of the articular surface, major tubercle, and minor tubercle. There is a purported functional division between the articular surface and the tubercles, with the articular surface mainly responsible for the range of movement of the shoulder joint, and the tubercles bearing the insertions of the rotator cuff muscles, mainly devoted to securing the joint against humeral displacement. Using three-dimensional geometric morphometrics, we tested the presence of such developmental and functional divisions in the proximal humerus, applying the RV coefficient of Escoufier to these a priori hypothesized modules. Our results indicate that the proximal humerus might be a generally integrated structure. However, a weak signal for modular configuration was present, with slightly stronger support for the two modules depicting the boundaries between the purported functional regions of the epiphysis: the articular surface and the tubercles.

Brief communication: Morphological effects of captivity: A geometric morphometric analysis of the dorsal side of the scapula in captive-bred and wild-caught Hominoidea.

Many osteological collections from museums and research institutions consist mainly of remains from captive-bred animals. The restrictions related to the space of their enclosures and the nature of its substrate are likely to affect the locomotor and postural behaviors of captive-bred animals, which are widely considered uninformative regarding bone morphology and anatomical adaptations of wild animals, especially so in the case of extant great apes. We made a landmark-based geometric morphometrics analysis of the dorsal side of the scapular bone of both wild-caught and captive-bred great apes to clarify the effect of captivity on the morphology of a bone greatly involved in locomotion. The comparison suggested that captivity did not have a significant effect on the landmark configuration used, neither on average scapular shape nor shape variability, being impossible to distinguish the scapulae of a captive-bred animal from that of a wild-caught one. This indicates that the analyzed scapulae from captive Hominoidea specimens may be used in morphological or taxonomic analyses since they show no atypical morphological traits caused by living conditions in captivity.

3D geometric morphometric analysis of the proximal epiphysis of the hominoid humerus.

In this study we perform a three-dimensional geometric morphometric (3D GM) analysis of the proximal epiphysis of the humerus in extant great apes, including humans, in order to accurately describe the functional anatomical differences between these taxa. In addition, a fossil hominin specimen of Australopithecus afarensis was included in a multivariate GM analysis in order to test the potential of this methodological approach for making locomotor inferences from fossil remains. The results obtained show significant differences in proximal humeral morphology among the taxa studied, which had thus far largely remained unnoticed. Based on morphofunctional considerations, these anatomical differences can be correlated to differences in the locomotor repertoires of the taxa, thus confirming that the proximal humerus is suitable for constructing paleobiological inferences about locomotion. Modern humans display markedly divergent features, which set them apart from both the extant great apes and the fossil hominin A. afarensis. The morphology of the proximal epiphysis of the humerus of the latter more closely resembles that of the orangutans, thus suggesting that despite hindlimb adaptations to bipedalism, the forelimb of this taxon was still functionally involved in arboreal behaviors, such as climbing or suspension.

New dental remains of Hispanopithecus laietanus (Primates: Hominidae) from Can Llobateres 1 and the taxonomy of Late Miocene hominoids from the Vallès-Penedès Basin (NE Iberian Peninsula).

Here we report 12 teeth of the fossil great ape Hispanopithecus (Hominidae: Dryopithecinae: Hispanopithecini), recovered in 2011 from the locality of Can Llobateres 1 (MN9, early Vallesian, Late Miocene, ca. 9.7 Ma [millions of years ago]) in the Vallès-Penedès Basin (Catalonia, Spain). Besides an isolated dP(3) from layer CLL1.1b in the eastern (classical) sector of the site, all of the remaining teeth come from facies CLL1.0 (roughly equivalent to CLL1.2 and CLL1.1b), located in the newly excavated western sector, and representing at least two different individuals. Based on facet congruence and degree of wear, all of the upper cheek teeth, a central incisor and a lateral incisor most likely correspond to a single young adult individual of unknown sex, whereas a very worn I(2) and a female C(1) represent one or two additional individual(s). Morphological and metrical comparisons allow us to attribute these remains to Hispanopithecus laietanus, which is the single hominoid species recognized at CLL1. The newly described teeth represent a significant addition to the hypodigm of this taxon, enabling us to more completely assess the degree of variation displayed by several teeth. In light of the new specimens, the previous tooth position assignment of several upper molars from Can Llobateres and Can Poncic is revised, and the criteria employed to distinguish Hispanopithecus crusafonti from H. laietanus are critically evaluated. On the basis of the available upper cheek teeth from these localities, a distinction at the species level between both samples is tentatively favored, mainly on the basis of P(3), M(1) and M(2) proportions as well as I(1) lingual morphology and proportions. The results of the 2011 field season unambiguously confirm that hominoid-bearing fossiliferous layers from CLL1 are not exhausted. Additional excavations at this site are promising for the discovery of additional remains of H. laietanus in the near future.