Ulnar shape of extant primates: Functional signals and covariation with triquetrum shape.

OBJECTIVES: In this study, we investigated the shape differences of the distal ulna in a phylogenetic context among a broad range of primate taxa. Furthermore, we evaluated covariation between ulnar and triquetrum shape and a possible association between ulnar shape and locomotor behavior. MATERIALS AND METHODS: We applied 3D geometric morphometrics on a large dataset comprising the distal ulna of 124 anthropoid primate specimens belonging to 12 different genera. For each species, a mean shape was calculated using 11 Procrustes-aligned surface landmarks on the distal ulna. These mean shapes are used in a bgPCA, pPCA, and PACA and 3D morphs were used to visualize more subtle differences between taxa. A p2B-PLS analysis was performed to test the covariance between distal ulnar and triquetrum shape. RESULTS: The results show that more closely related species exhibit a similar distal ulnar shape. Overall, extant hominid ulnae show a shape shift compared to those of extant monkeys and hylobatids. This includes a shortening of the ulnar styloid process and dorspalmarly widening of the ulnar head, shape characteristics that are independent of phylogeny. Within the hominids, Pongo pygmaeus seem to possess the most plesiomorphic distal ulnar shape, while Gorilla and Homo sapiens display the most derived distal ulna. Cercopithecoids, hylobatids, and P. pygmaeus are characterized by a relatively deep ECU groove, which is a shape trait dependent of phylogeny. Although there was no significant covariation between distal ulnar shape and triquetrum shape, the shape differences of the distal ulna between the different primate taxa reveal a possible link with locomotor behavior. CONCLUSIONS: The comparative analyses of this study reveal different shape trends in a phylogenetic context. Highly arboreal primates, such as hylobatids and Ateles fusciceps, show a distal ulnar morphology that appears to be adapted to tensile and torsional forces. In primates that use their wrist under more compressive conditions, such as quadrupedal cercopithecoids and great apes, the distal ulnar morphology seems to reflect increased compressive forces. In modern humans, the distal ulnar shape can be associated to enhanced manipulative skills and power grips. There was no significant covariation between distal ulnar shape and triquetrum shape, probably due to the variation in the amount of contact between the triquetrum and ulna. In combination with future research on wrist mobility in diverse primate taxa, the results of this study will allow us to establish form-function relationships of the primate wrist and contribute towards an evidence-based interpretation of fossil remains.

Principal component and linear discriminant analyses for the classification of hominoid primate specimens based on bone shape data.

In this study, we tested the hypothesis that machine learning methods can accurately classify extant primates based on triquetrum shape data. We then used this classification tool to observe the affinities between extant primates and fossil hominoids. We assessed the discrimination accuracy for an unsupervised and supervised learning pipeline, i.e. with principal component analysis (PCA) and linear discriminant analysis (LDA) feature extraction, when tasked with the classification of extant primates. The trained algorithm is used to classify a sample of known fossil hominoids. For the visualization, PCA and uniform manifold approximation and projection (UMAP) are used. The results show that the discriminant function correctly classified the extant specimens with an F1-score of 0.90 for both PCA and LDA. In addition, the classification of fossil hominoids reflects taxonomy and locomotor behaviour reported in literature. This classification based on shape data using PCA and LDA is a powerful tool that can discriminate between the triquetrum shape of extant primates with high accuracy and quantitatively compare fossil and extant morphology. It can be used to support taxonomic differentiation and aid the further interpretation of fossil remains. Further testing is necessary by including other bones and more species and specimens per species extinct primates.

Covariation between wrist bone morphology and maximal range of motion during ulnar deviation and supination in extant nonhuman primate taxa.

This study investigates the maximal range of motion (ROM) during wrist deviation and forearm rotation for five different primate genera and the possible correlation with the shape of the distal ulna, triquetrum and hamate. A two-block phylogenetic partial least square analysis was performed to test this covariation in a phylogenetic context, using shape coordinates and a matrix of maximal ROM data as input data. The results show that gibbons have the highest ROM for both ulnar deviation and supination, whereas Macaca exhibited the lowest ROM for supination, and Pan had the lowest ROM for ulnar deviation. These results can be attributed to differences in locomotor behaviour, as gibbons need a large wrist mobility in all directions for their highly arboreal lifestyle, whereas Macaca and Pan need a stable wrist during terrestrial locomotion. However, we found no correlation between distal ulna/triquetrum/hamate shape and maximal ROM during ulnar deviation and supination in the different primate taxa. A larger dataset, in combination with behavioural and biomechanical studies, is needed to establish form-function relationships of the primate hand, which will aid the functional interpretation of primate fossil remains.

Branching patterns of the vascularization and innervation of the primate forelimb.

In this study, we investigate the branching patterns of the vascularization and innervation of the primate forelimb by performing detailed dissections of five unembalmed nonhuman primate specimens belonging to five different species, that is, rhesus macaque (Macaca mulatta), white-handed gibbon (Hylobates lar), Western gorilla (Gorilla gorilla), chimpanzee (Pan troglodytes), and bonobo (Pan paniscus). Results are compared with five embalmed human specimens (Homo sapiens), and anatomical data of previous studies on nonhuman primates are also included to provide a broader comparative framework. The results show that the overall configuration of the forelimb blood vessels and nerves of the different primate species is similar, although some apparent interspecific differences are found. In all nonhuman primates, in contrast to humans, the superficial vena basilica is absent. Moreover, in gorilla, chimpanzee, and bonobo, the superficial vena cephalica is confined to the forearm. In humans, both an arteria interossea anterior and posterior are present, while in nonhuman primates, only an arteria interossea anterior is present, which migrates to the posterior side at the level of the musculus pronator quadratus. For the innervation, the nervus (n.) medianus and n. ulnaris connect in the forearm of the gorilla and macaque. In the gibbon, the brachial plexus shows some differences in the branching pattern at the fasciculus level compared to the other primates. We conclude that the forelimb innervation branching pattern shows some minor differences between the nonhuman primate species, compared to higher plasticity in the vascularization. However, the exact functional implications of these differences still remain unclear. Therefore, more research on a broader range of primate species and sampling more specimens for each taxon are needed.

Functional signals and covariation in triquetrum and hamate shape of extant primates using 3D geometric morphometrics.

In this study, we want to investigate the covariation in the shape of two carpal bones, the triquetrum and hamate, and the possible association with locomotor behavior in a broad range of primate taxa. We applied 3D Geometric Morphometrics on a large data set comprising 309 anthropoid primates of 12 different genera. Principal component analyses were performed on the covariance matrix of 18 (triquetrum) and 23 (hamate) Procrustes-aligned surface landmarks. A two-block partial least square analysis was done to test the covariance between triquetrum and hamate shape, without relying on the predictive models implicit in regression analyses. The results show that the carpal shape of quadrupedal anthropoids, which mainly use their wrist under compressive conditions, differs from that of suspensory primates as their wrist is possibly subjected to tensile and torsional forces. Within the hominids, differences in shape also distinguish more terrestrial from more arboreal species. Even within the great apes, we are able to capture shape differences between species of the same genus. In combination with behavioral and biomechanical studies, the results of this research can be used to establish form-function relationships of the primate hand which will aid the functional interpretation of primate fossil remains.

The forearm and hand musculature of semi-terrestrial rhesus macaques (Macaca mulatta) and arboreal gibbons (fam.Hylobatidae). Part II. Quantitative analysis.

Nonhuman primates have a highly diverse locomotor repertoire defined by an equally diverse hand use. Based on how primates use their hands during locomotion, we can distinguish between terrestrial and arboreal taxa. The 'arboreal' hand is likely adapted towards high wrist mobility and grasping, whereas the 'terrestrial' hand will show adaptations to loading. While the morphology of the forearm and hand bones have been studied extensively, functional adaptations in the forearm and hand musculature to locomotor behaviour have been documented only scarcely. In this paper, we investigate the forelimb musculature of the highly arboreal gibbons (including Hylobates lar,Hylobates pileatus,Nomascus leucogenys,Nomascus concolor and Symphalangus syndactylus) and compare this with the musculature of the semi-terrestrial rhesus macaques (Macaca mulatta). Anatomical data from previous dissections on knuckle-walking bonobos (Pan paniscus) and bipedal humans (Homo sapiens) are also included to further integrate the analyses in the scope of catarrhine hand adaptation. This study indicates that the overall configuration of the arm and hand musculature of these primates is very similar but there are some apparent differences in relative size which can be linked to differences in forelimb function and which might be related to their specific locomotor behaviour. In macaques, there is a large development of wrist deviators, wrist and digital flexors, and m. triceps brachii, as these muscles are important during the different phases of palmi- and digitigrade quadrupedal walking to stabilize the wrist and elbow. In addition, their m. flexor carpi ulnaris is the most important contributor to the total force-generating capacity of the wrist flexors and deviators, and is needed to counteract the adducting torque at the elbow joint during quadrupedal walking. Gibbons show a relatively high force-generating capacity in their forearm rotators, wrist and digital flexors, which are important muscles in brachiation to actively regulate forward movement of the body. The results also stress the importance of the digital flexors in bonobos, during climbing and clambering, and in humans, which is likely linked to our advanced manipulation skills.

The forearm and hand musculature of semi-terrestrial rhesus macaques (Macaca mulatta) and arboreal gibbons (Fam. Hylobatidae). Part I. Description and comparison of the muscle configuration.

Primates live in very diverse environments and, as a consequence, show an equally diverse locomotor behaviour. During locomotion, the primate hand interacts with the superstrate and/or substrate and will therefore probably show adaptive signals linked with this locomotor behaviour. Whereas the morphology of the forearm and hand bones have been studied extensively, the functional adaptations in the hand musculature have been documented only scarcely. To evaluate whether there are potential adaptations in forelimb musculature to locomotor behaviour, we investigated the forearm and hand musculature of the highly arboreal gibbons (including Hylobates lar, Hylobates pileatus, Nomascus leucogenys, Nomascus concolor, Symphalangus syndactylus) and compared this with the musculature of the semi-terrestrial rhesus macaques (Macaca mulatta) by performing complete and detailed dissections on a sample of 15 unembalmed specimens. We found that the overall configuration of the upper arm and hand musculature is highly comparable between arboreal gibbons and semi-terrestrial macaques, and follows the general primate condition. Most of the identified differences in muscle configuration are located in the forearm. In macaques, a prominent m. epitrochleoanconeus is present, which potentially helps to extend the forearm and/or stabilize the elbow joint during quadrupedal walking. The m. flexor carpi radialis shows a more radial insertion in gibbons, which might be advantageous during brachiation, as it can aid radial deviation. The fingers of macaques are controlled in pairs by the m. extensor digiti secondi et tertii proprius and the m. extensor digiti quarti et quinti proprius-a similar organization can also be found in their flexors-which might aid in efficient positioning of the hand and fingers on uneven substrates during quadrupedal walking. In contrast, extension of the little finger in gibbons is controlled by a separate m. extensor digiti minimi, whereas digits 2 to 4 are extended by the m. extensor digitorum brevis, suggesting that simultaneous extension of digits 2-4 in gibbons might be important when reaching or grasping an overhead support during brachiation. In conclusion, the overall configuration of the forelimb and hand musculature is very similar in gibbons and macaques, with some peculiarities which can be linked to differences in forelimb function and which might be related to the specific locomotor behaviour of each group.

Insights into the musculature of the bonobo hand.

The human hand is well known for its unique dexterity which is largely facilitated by a highly mobile, long and powerful thumb that enables both tool manufacturing and use, a key component of human evolution. The bonobo (Pan paniscus), the closest extant relative to modern humans together with the chimpanzee (Pan troglodytes), also possesses good manipulative capabilities but with a lower level of dexterity compared with modern humans. Despite the close phylogenetic relationship between bonobos and humans, detailed quantitative data of the bonobo forelimb musculature remains largely lacking. To understand how morphology may influence dexterity, we investigated the functional anatomy of the bonobo hand using a unique sample of eight bonobo cadavers, along with one chimpanzee and one human (Homo sapiens) cadaver. We performed detailed dissections of unembalmed specimens to collect quantitative datasets of the extrinsic and intrinsic hand musculature, in addition to qualitative descriptions of the forelimb muscle configurations, allowing estimation of force-generating capacities for each functional group. Furthermore, we used medical imaging to quantify the articular surface of the trapeziometacarpal joint to estimate the intra-articular pressure. Our results show that the force-generating capacity for most functional groups of the extrinsic and intrinsic hand muscles in bonobos is largely similar to that of humans, with differences in relative importance of the extensors and rotators. The bonobo thumb musculature has a lower force-generating capacity than observed in the human specimen, but the estimated maximal intra-articular pressure is higher in bonobos. Most importantly, bonobos show a higher degree of functional coupling between the muscles of the thumb, index and lateral fingers than observed in humans. It is conceivable that differentiation and individualization of the hand muscles rather than relative muscle development explain the higher level of dexterity of humans compared with that of bonobos.