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.

The hands of nonhuman primates directly interact with the surrounding environment during locomotion and need to accommodate a large variety of superstrate and/or substrate sizes and orientation (e.g. Daver et al., 2012; Kikuchi et al., 2012; Kivell, 2016; Lewis, 1989). Therefore, together with the large variety in locomotor repertoire between different primate taxa, it is expected that hand morphology and the levels of wrist mobility will reflect these differences in functional demands placed on the hand (e.g. Daver et al., 2012; Jenkins and Fleagle, 1975; Lewis, 1969; Orr, 2017; Potau et al., 2022; Schilling et al., 2014). However, although wrist kinematics has been studied in some extant nonhuman primates (Daver et al., 2012; Jenkins and Fleagle, 1975; Jenkins, 1981; Jouffroy and Medina, 2002; van Leeuwen et al., 2019, 2022; Orr et al., 2023; Schmitt, 1994; Thompson, 2020), the relationship between wrist bone morphology and maximal range of motion remains unresolved.

The configuration of the radioulnar joint (i.e. articulation between the distal radius and ulna) and ulnocarpal joint (i.e. articulation between the distal ulna and proximal carpal row) of the wrist is highly variable across primates (Fig. 1) (e.g. Cartmill and Milton, 1977; Lewis, 1969, 1972, 1989; O'Connor, 1975; Sarmiento, 1988). The radioulnar joint of humans and apes shows an expanded ulnar head and the formation of a true synovial (diarthrodial) joint at the distal radioulnar articulation, which is linked to increased forearm rotation (pronation and supination) (Lewis et al., 1970; O'Connor and Rarey, 1979). For the ulnocarpal joint, the shape of the distal ulna varies substantially across primates (Kivell, 2016; Lewis, 1989; Sarmiento, 1988). A direct ulnocarpal articulation is seen in Old World monkeys (e.g. Macaca), whereas hylobatids and Pan show a partially blocked ulnocarpal contact, and the ulnar styloid process of Pongo, Gorilla and modern humans is fully excluded from the articulation with the proximal carpal row (for more details, see Vanhoof et al., 2023).

Fig. 1.

Schematic representation (coronal sections) of the different wrist morphotypes in the primates studied. (A) Old and New World monkeys: ulnocarpal articulation in which the ulnar styloid process (red circle) articulates with the triquetrum (blue) and pisiform (pink). (B) Gibbons and siamangs: ulnocarpal articulation partially blocked by the presence of a triangular ligament. (C) Chimpanzees and bonobos: ulnocarpal articulation partially blocked because of a non-complete fusion of the triangular articular disc and the semilunar meniscus. (D) Orangutans, gorillas and humans: ulnocarpal articulation absent owing to an interposed large fibrocartilaginous triangular articular disc. The retraction of the ulnar styloid process in the hominoid lineage co-occurs with the formation of a true synovial (diarthrodial) distal radioulnar joint between an expanded ulnar head and ulnar notch of the radius. S, scaphoid; L, lunate; T, triquetrum; P, pisiform; R, radius; U, ulna. Figure adapted from Lewis (1969).

Fig. 1.

Schematic representation (coronal sections) of the different wrist morphotypes in the primates studied. (A) Old and New World monkeys: ulnocarpal articulation in which the ulnar styloid process (red circle) articulates with the triquetrum (blue) and pisiform (pink). (B) Gibbons and siamangs: ulnocarpal articulation partially blocked by the presence of a triangular ligament. (C) Chimpanzees and bonobos: ulnocarpal articulation partially blocked because of a non-complete fusion of the triangular articular disc and the semilunar meniscus. (D) Orangutans, gorillas and humans: ulnocarpal articulation absent owing to an interposed large fibrocartilaginous triangular articular disc. The retraction of the ulnar styloid process in the hominoid lineage co-occurs with the formation of a true synovial (diarthrodial) distal radioulnar joint between an expanded ulnar head and ulnar notch of the radius. S, scaphoid; L, lunate; T, triquetrum; P, pisiform; R, radius; U, ulna. Figure adapted from Lewis (1969).

In the literature, is has been suggested that the retraction of the ulnar styloid process within the hominoid primate lineage might be functionally linked to brachiation, climbing behaviour and palmigrade hand postures, as it would allow a greater wrist mobility, particularly ulnar deviation and supination, while a restriction in wrist mobility is associated with digitigrade hand postures and knuckle-walking (Cartmill and Milton, 1977; Kivell, 2016; Lewis, 1969; Orr, 2017; Sarmiento, 1988). However, the effect of distal ulnar morphology on ulnocarpal loading and wrist mobility has been studied more rigorously in modern humans owing to the importance in a medical context (e.g. Kataoka et al., 2012; Palmer and Werner, 1981; Sachar, 2012). Modern humans display what is called ‘ulnar variance’, i.e. variation in the length of the ulna relative to the radius (Kataoka et al., 2012). In addition, surgical procedures that lead to ulnar shortening are used to treat specific wrist pathologies (e.g. ulnar impaction syndrome; Loh et al., 1999; Saffar, 2007). Decreasing the length of the distal ulna, for example, has been shown to lead to significant changes in ulnocarpal loading (Palmer and Werner, 1984). In nonhuman primates, most studies have focused on extension limiting mechanisms of the wrist in terrestrial taxa in the context of knuckle-walking (e.g. Corruccini, 1978; Jenkins and Fleagle, 1975; Kivell and Schmitt, 2009; Orr, 2005; Tuttle, 1967). The functional implications of the variation in relative ulnar styloid length thus remain unclear. Moreover, relatively little attention has been given to ulnar deviation and supination of the wrist, despite their importance in locomotion and human evolution. Ulnar deviation and supination of the wrist likely played a role in the intensification of tool use, as they appear to be important when using a ‘power squeeze’ grip to hold tools during clubbing and throwing (Marzke et al., 1992; Rhode et al., 2010; Wolfe et al., 2006; Young, 2003).

The long ulnar styloid process and fully elaborated ulnocarpal articulation in semi-terretrial macaques (genus Macaca) might be important for providing stability on the ulnar carpus during digitigrade quadrupedal walking (Hayama et al., 1994; Higurashi et al., 2018; Mittermeier, 1978; O'Connor, 1975; Patel, 2009a,b; Schmitt, 2003; Wright, 2007). They use an ulnarly deviated wrist during their digitigrade/palmigrade terrestrial walking, but also when walking on arboreal supports (Demes et al., 1998; Lemelin and Schmitt, 1998; Rawlins, 1993; Sarmiento, 1988; Schmitt et al., 2016; Thompson, 2020). However, recent research has shown that the degree of ulnar deviation is not directly dependent on the presence of ulnocarpal contact (Jouffroy and Medina, 2002; Orr et al., 2023). The reduction of the ulnar styloid process in the hominoid lineage probably reduces stress on the ulnar side of the wrist, or might be a byproduct of adaptations that increase supination (Orr et al., 2023). Moreover, the wrist joint of arboreal hylobatids (further referred to as ‘gibbons’) exhibits a very high mobility in all directions (Richmond, 2006; Sarmiento, 1988) even though their ulnar styloid process is also relatively long. Gibbons use a considerable amount of ulnar deviation and supination during brachiation, for which this high wrist mobility is needed (Sarmiento, 1988). In contrast to gibbons, knuckle-walking chimpanzees and bonobos (genus Pan) have a relatively stiff wrist with the carpals packed tightly together and a short ulnar styloid process, which indicates a lower wrist mobility (Corruccini, 1978; Orr, 2017; Orr et al., 2010; Sarmiento, 1988; Vanhoof et al., 2021). African apes use an ulnarly deviated wrist during climbing, especially on smaller supports (Neufuss et al., 2017; Sarmiento, 1988), but also during the early phase of the knuckle-walking gait cycle (Jenkins and Fleagle, 1975; Sarmiento, 1988; Thompson, 2020; Tuttle, 1967). During initial contact with the substrate, Pan use an ulnarly deviated wrist, in combination with some level of extension (Finestone et al., 2018; Jenkins and Fleagle, 1975; Thompson et al., 2018). This ulnarly deviated wrist is retained throughout the swing phase as well as during stance, and the stable wrist probably promotes weight transfer (Corruccini, 1978; Young, 2003).

Within the wrist, the triquetrum and hamate are positioned on the ulnar side and are therefore most likely to influence mobility on this side of the wrist. For example, the orientation of the triquetral facet of the hamate is correlated with range of motion (ROM) during ulnar deviation (Orr et al., 2023). In addition, in previous research we have shown that these carpal bones show a strong covariation in shape and a possible link with differences in locomotor behaviour (Vanhoof et al., 2021). However, although the triquetrum articulates with the distal ulna (directly or indirectly) and hamate (Almécija et al., 2015; Cartmill and Milton, 1977; Joshi et al., 2007; Kivell, 2016; Lewis, 1971; Marzke et al., 1992; Palmer and Werner, 1981; Youlatos, 1996), the link between the morphology of these bones and the ROM of the wrist during ulnar deviation and supination remains untested in nonhuman primates.

In this study, we quantified the maximal ROM of the wrist deviation and forearm rotation in different nonhuman anthropoid primates and investigated the covariation with morphology of the triquetrum/hamate/distal ulna. Maximal ROM was used as a proxy for the functional capacity of the wrist. We tested the following hypotheses: (H1) the maximal ROM of ulnar deviation would be higher than the maximal ROM of radial deviation; (H2) highly arboreal gibbons would show the highest ROM during ulnar deviation and supination, whereas semi-terrestrial macaques would show the lowest ROM and Pan would have a moderate ROM; and (H3) the bone shape of the different primate genera can be reasonably associated with differences in maximal ROM of the wrist during ulnar deviation and supination.

Specimen collection

The samples used in this study include fresh-frozen cadaveric material of 19 extant anthropoid primate specimens of five different genera (Macaca, Nomascus, Hylobates, Symphalangus and Pan). Because of the small sample size, the specimens were grouped at genus level. We obtained the nonhuman primate cadavers via collaborations with different European zoos and institutes. All species belong to the parvorder of the Catarrhini with different phylogenetic positions relative to humans. No animals were killed for this project. Only adult specimens without alterations in the postcranial skeleton were used. Details of the samples are provided in Table 1. As we only used 3D meshes in this study, no ethical approval was needed.

Table 1.

Specimen details

Specimen details
Specimen details

CT-scanning and segmentation

Each cadaver specimen was CT-scanned in five different wrist positions: neutral, maximal ulnar deviation (UD) and radial deviation (RD), maximal pronation (PRO) and supination (SUP) (using a 64 slice Discovery HD 750 CT scanner, GE Healthcare, Little Chalfont, UK; display field of view: 250 mm, slice thickness: 0.625 mm, pixel spacing: 0.293/0.293 mm, voxel size: 0.054 mm3, 100 kV, 180 mA, 512×512 pixels). A custom-made radiolucent rig was used to standardize the wrist (and elbow) positions of the different-sized specimens (Fig. 2). The PRO and SUP scans included the entire radius, ulna, carpal bones and the third metacarpal (MC3), whereas the UD and RD scans only included the distal radius and ulna, and entire carpal and metacarpal bones. All CT images were segmented using dedicated image processing software (Mimics – version 24.0, Materialise, Leuven, Belgium) to create 3D surface models of the radius, ulna, carpal bones and MC3 of each specimen. These 3D bone models of the maximal positions were used to calculate the maximal range of motion of each movement pair, which were then used in the covariation analyses.

Fig. 2.

Illustration of the custom-made rig to standardize wrist and elbow positions of the different-sized specimens. (A) Chimpanzee forelimb fixed in maximal ulnar deviation. (B) Chimpanzee forelimb fixed in maximal supination.

Fig. 2.

Illustration of the custom-made rig to standardize wrist and elbow positions of the different-sized specimens. (A) Chimpanzee forelimb fixed in maximal ulnar deviation. (B) Chimpanzee forelimb fixed in maximal supination.

Three-dimensional geometric morphometrics

Fixed surface landmarks based on the definitions of Almécija et al. (2015) were used to capture the overall shape of the distal ulna (11 landmarks), triquetrum (18 landmarks) and hamate (23 landmarks) (Almécija et al., 2015). Full details on landmark definitions and positioning can be found in Fig. S1 (see also Vanhoof et al., 2021, 2023). Landmark editor software was used for landmark placement (version 3.0) (Wiley et al., 2005). The Procrustes-aligned landmark coordinates were used in a two-block partial least squares analysis to test for covariation between shape and maximal ROM during UD and SUP (see below). In addition, a principal component analysis (PCA) was used to explore major patterns of shape variation among the different hylobatid taxa.

Quantification of maximal ROM

Available in-house developed scripts for use in PyCharm Community Edition 2021.3.2 were adapted to calculate the maximal ROM of RD, UD, PRO and SUP relative to the reference position (i.e. neutral position). For RD and UD, the movement of MC3 was calculated relative to the radius, using the radius-based coordinate system (Vanneste et al., 2021) based on three anatomical landmarks in correspondence with the guidelines of the International Society of Biomechanics for the human forearm (Wu and Cavanagh, 1995) (Fig. 3A). For PRO and SUP, the movement of MC3 was calculated relative to the ulna (which remains relatively static during this motion), using an ulnar-based coordinate system defined using rigid body parameters (i.e. principal moments of inertia) (Fig. 3B).

Fig. 3.

Visualization of both coordinate systems used to calculate the movement of the third metacarpal (MC3) and illustrations of the associated movements. (A) Radius-based coordinate system used for calculating the maximal ROM in RD and UD (i.e. the movement of MC3 relative to the radius). The three anatomical landmarks include: (1) the lowest point on the distal border of the ulnar notch; (2) the proximal border of the ulnar notch; and (3) the tip of the radial styloid. These three anatomical landmarks determine a local coordinate system consisting of an x-axis (green), y-axis (red) and z-axis (blue). The black arrow indicates the movement of MC3 during UD. (B) Ulnar coordinate system used for calculating the maximal ROM in PRO and SUP (i.e. the movement of MC3 relative to the ulna). Based on the shape of the ulna, Python defined the different axes (x-axis=green, y-axis=red, z-axis=blue) based on rigid body parameters. The white arrow indicates the movement of MC3 during SUP. A adapted from D'Agostino et al. (2017). B adapted from Python output.

Fig. 3.

Visualization of both coordinate systems used to calculate the movement of the third metacarpal (MC3) and illustrations of the associated movements. (A) Radius-based coordinate system used for calculating the maximal ROM in RD and UD (i.e. the movement of MC3 relative to the radius). The three anatomical landmarks include: (1) the lowest point on the distal border of the ulnar notch; (2) the proximal border of the ulnar notch; and (3) the tip of the radial styloid. These three anatomical landmarks determine a local coordinate system consisting of an x-axis (green), y-axis (red) and z-axis (blue). The black arrow indicates the movement of MC3 during UD. (B) Ulnar coordinate system used for calculating the maximal ROM in PRO and SUP (i.e. the movement of MC3 relative to the ulna). Based on the shape of the ulna, Python defined the different axes (x-axis=green, y-axis=red, z-axis=blue) based on rigid body parameters. The white arrow indicates the movement of MC3 during SUP. A adapted from D'Agostino et al. (2017). B adapted from Python output.

The 3D bone meshes were registered using iterative closest point and coherent point drift techniques (Vanneste et al., 2021). The result was the 3D movement of MC3 relative to the radius or ulna. For RD and UD, the maximal deviation was determined as a Euler rotation around the x-axis (frontal plane), and for PRO and SUP around the z-axis (sagittal plane). Afterwards, the obtained ROM values of the various specimens were analyzed to identify significant differences in wrist mobility between the different species. First, the correlations between total radioulnar deviation and RD/UD were calculated and plotted to determine the contribution of both UD and RD to the total ROM during radioulnar deviation. The same was done for PRO and SUP relative to total pro-supination. Significant differences in UD and SUP between the different taxa were verified using ANOVA and Tukey HSD tests. In this study, we report uniplanar maximal ROM of the wrist for radioulnar deviation (RD/UD) and forearm rotation (PRO/SUP) using cadaver specimens.

Covariation analysis

We performed a two-block phylogenetic partial least squares (2B-pPLS) analysis to test for covariation between ulnar shape and the kinematic output in a phylogenetic structure (Marugán-Lobón, 2010; Rohlf and Corti, 2000; van Heteren et al., 2016). In 2B-PLS, in contrast to a multivariate regression, both ‘blocks’ are treated symmetrically rather than as one set of variables (x-axis) being used to predict variation in the other set of variables (y-axis). The new pairs of variables represent linear combinations of variables within the original two sets (‘blocks’), so that these new variables account for as much of the covariation as possible to find relationships between the two original ‘blocks’ without assuming that one is the cause for the variation in the other. In our study, one block represents triquetrum/hamate/distal ulnar shape (x-axis), and the other block represents a matrix of the kinematic output (y-axis). The RV coefficient, a multivariate analogue of the squared correlation, was used as an overall measure of association between the two blocks (Escoufier, 1973), and a permutation test (10,000 alterations) was employed against the null hypothesis of complete independence.

All statistical analyses were performed in the R environment (version 4.2.2) using the Geomorph v 4.0.4 package (https://cran.r-project.org/package=geomorph; Baken et al., 2021). R was also used to create the graphical output to interpret the results and for visualization, using the package rgl v. 0.103.5 (https://cran.r-project.org/package=rgl). The significance value was set at 0.05.

Correlations

The correlation plots for total radioulnar deviation are shown in Fig. 4. Both plots show a positive and significant correlation (RD: P=0.0004, UD: P=2.57e-07; Table S1), which means that when total radioulnar deviation increases, both RD and UD contribute to this increase. However, the positive correlation is stronger for UD owing to a higher correlation coefficient (0.90 versus 0.75 for RD), which indicates that UD contributes more to the total wrist mobility in the frontal plane. Fig. 5 shows the correlation plots regarding pro-supination. Both correlations are significant (P=0.0004; Table S1) and positive and the correlation coefficient is only slightly higher for SUP (0.84 versus 0.73 for PRO), which means that when total pro-supination increases, both PRO and SUP equally contribute to this motion in the transverse plane.

Fig. 4.

Correlation plots for total radioulnar deviation (RDUD). Both plots show a positive and significant correlation. An increase of total radioulnar deviation thus means an increase of both RD and UD, though the latter contributes relatively more to total wrist mobility in the frontal plane. (A) RD: correlation coefficient=0.74, P=0.0004. (B) UD: correlation coefficient=0.90; P=2.57e-07. Sample size: Macaca n=7, Pan n=3, Hylobates n=4, Nomascus n=2, Symphalangus n=2.

Fig. 4.

Correlation plots for total radioulnar deviation (RDUD). Both plots show a positive and significant correlation. An increase of total radioulnar deviation thus means an increase of both RD and UD, though the latter contributes relatively more to total wrist mobility in the frontal plane. (A) RD: correlation coefficient=0.74, P=0.0004. (B) UD: correlation coefficient=0.90; P=2.57e-07. Sample size: Macaca n=7, Pan n=3, Hylobates n=4, Nomascus n=2, Symphalangus n=2.

Fig. 5.

Correlation plots for total pro-supination (PROSUP). Both plots show a positive and significant correlation. An increase of total pro-supination thus means an increase of both PRO and SUP, though the latter contributes relatively more to total wrist mobility in the transverse plane. (A) PRO: correlation coefficient=0.73, P=0.0006. (B) SUP: correlation coefficient=0.84; P=1.39e-05. Sample size: Macaca n=7, Pan n=3, Hylobates n=4, Nomascus n=2, Symphalangus n=2.

Fig. 5.

Correlation plots for total pro-supination (PROSUP). Both plots show a positive and significant correlation. An increase of total pro-supination thus means an increase of both PRO and SUP, though the latter contributes relatively more to total wrist mobility in the transverse plane. (A) PRO: correlation coefficient=0.73, P=0.0006. (B) SUP: correlation coefficient=0.84; P=1.39e-05. Sample size: Macaca n=7, Pan n=3, Hylobates n=4, Nomascus n=2, Symphalangus n=2.

Maximal UD and SUP of the different primate genera

Fig. 6A shows the maximal UD of the different primate genera. It is clear that Hylobates and Symphalangus have the highest maximal UD, with an average excursion of 44.5±9.6 and 50.5±4.0 deg, respectively. This is significantly higher than that of Pan (17.5±4.9 deg, Hylobates: P=0.0009; Symphalangus: P=0.003; Table S2). Macaca and Nomascus are situated in between the other hylobatids and Pan, with an average excursion of 31.2±5.6 and 32.9±4.5 deg, respectively. Macaca is significantly different from Hylobates (P=0.02) and Symphalangus (P=0.05). Fig. 6B shows the maximal SUP for the different primate genera. The hylobatids show the highest ROM during SUP (average excursion: Nomascus: 140.1±7.5 deg, Symphalangus: 127.6±19.9 deg, Hylobates: 122.3±9.0 deg), which is significantly different from Macaca (66.1±14.8 deg, Nomascus: P=0.0003, Symphalangus: P=0.002, Hylobates: P=0.0004, Table S2). In contrast to maximal UD, it is Macaca that shows the lowest excursion for maximal SUP. Pan is significantly different from Nomascus (P=0.03).

Fig. 6.

Maximal ulnar deviation and supination. (A) Maximal ulnar deviation (UD). Hylobates and Symphalangus show the highest maximal UD (average excursion: 44.46±9.59 and 50.49±4.03 deg), which is significantly different from Pan (17.52±4.85 deg, Hylobates: P=0.0009; Symphalangus: P=0.003). Macaca and Nomascus are situated in between (average excursion: 31.23±5.56 and 32.87±4.49 deg), and Macaca is significantly different from Hylobates (P=0.02) and Symphalangus (P=0.05). (B) Maximal supination (SUP). The hylobatids show the highest range of motion (average excursion: Nomascus: 140.13±7.54 deg, Symphalangus: 127.56±19.90 deg, Hylobates: 122.25±8.99 deg), which is significantly different from Macaca (66.13±14.8 deg, Nomascus: P=0.0003, Symphalangus: P=0.002, Hylobates: P=0.0004). In contrast to maximal UD, Macaca shows the lowest excursion for maximal SUP. The grey meshes illustrate movement of the distal ulna, triquetrum, and hamate during UD and SUP for the different primate taxa. Sample size: Macaca n=7, Pan n=3, Hylobates n=4, Nomascus n=2, Symphalangus n=2.

Fig. 6.

Maximal ulnar deviation and supination. (A) Maximal ulnar deviation (UD). Hylobates and Symphalangus show the highest maximal UD (average excursion: 44.46±9.59 and 50.49±4.03 deg), which is significantly different from Pan (17.52±4.85 deg, Hylobates: P=0.0009; Symphalangus: P=0.003). Macaca and Nomascus are situated in between (average excursion: 31.23±5.56 and 32.87±4.49 deg), and Macaca is significantly different from Hylobates (P=0.02) and Symphalangus (P=0.05). (B) Maximal supination (SUP). The hylobatids show the highest range of motion (average excursion: Nomascus: 140.13±7.54 deg, Symphalangus: 127.56±19.90 deg, Hylobates: 122.25±8.99 deg), which is significantly different from Macaca (66.13±14.8 deg, Nomascus: P=0.0003, Symphalangus: P=0.002, Hylobates: P=0.0004). In contrast to maximal UD, Macaca shows the lowest excursion for maximal SUP. The grey meshes illustrate movement of the distal ulna, triquetrum, and hamate during UD and SUP for the different primate taxa. Sample size: Macaca n=7, Pan n=3, Hylobates n=4, Nomascus n=2, Symphalangus n=2.

Covariation between shape and wrist mobility

The results of the 2B-pPLS analysis for the triquetrum show that although there is a positive correlation with both UD (Fig. 7A) and SUP (Fig. 7B), the overall association is not significant between triquetrum shape and maximal ROM during UD (r-PLS=0.81 and P=0.09) and SUP (r-PLS=0.78 and P=0.14; Table S3). The results for the hamate show that for both UD and SUP (Fig. 8) the correlation is positive though not significant (UD: r-PLS=0.78 and P=0.15; SUP: r-PLS=0.80 and P=0.17; Table S3). The 2B-pPLS analysis for the distal ulna also shows that for UD (Fig. 9A) and SUP (Fig. 9B) there is no significant correlation (UD: r-PLS=0.55 and P=0.31; SUP: r-PLS=0.73 and P=0.16; Table S3).

Fig. 7.

Covariation between triquetrum shape maximal ulnar deviation and supination. (A) Maximal ulnar deviation (UD) and (B) maximal supination (SUP). The 2B-pPLS analysis shows that for both UD and SUP there is a positive correlation with triquetrum shape, though this is not significant (UD: P=0.09; SUP: P=0.14).

Fig. 7.

Covariation between triquetrum shape maximal ulnar deviation and supination. (A) Maximal ulnar deviation (UD) and (B) maximal supination (SUP). The 2B-pPLS analysis shows that for both UD and SUP there is a positive correlation with triquetrum shape, though this is not significant (UD: P=0.09; SUP: P=0.14).

Fig. 8.

Covariation between hamate shape and maximal ulnar deviation and supination. (A) Maximal ulnar deviation (UD) and (B) maximal supination (SUP). The 2B-pPLS analysis shows that for both UD and SUP there is a positive correlation with hamate shape, though this is not significant (UD: P=0.15; SUP: P=0.17).

Fig. 8.

Covariation between hamate shape and maximal ulnar deviation and supination. (A) Maximal ulnar deviation (UD) and (B) maximal supination (SUP). The 2B-pPLS analysis shows that for both UD and SUP there is a positive correlation with hamate shape, though this is not significant (UD: P=0.15; SUP: P=0.17).

Fig. 9.

Covariation between distal ulnar shape and maximal ulnar deviation and supination. (A) Maximal ulnar deviation (UD) and (B) maximal supination (SUP). The 2B-pPLS analysis shows that for both UD and SUP there is a positive correlation with distal ulnar shape, though this is not significant (UD: P=0.31; SUP: P=0.16).

Fig. 9.

Covariation between distal ulnar shape and maximal ulnar deviation and supination. (A) Maximal ulnar deviation (UD) and (B) maximal supination (SUP). The 2B-pPLS analysis shows that for both UD and SUP there is a positive correlation with distal ulnar shape, though this is not significant (UD: P=0.31; SUP: P=0.16).

In this study, the maximal ROM during radioulnar deviation and forearm rotation was calculated for five different primate genera. In addition, we investigated the possible covariation between maximal ROM of ulnar deviation and supination and the shape of the distal ulna, triquetrum and hamate.

Wrist range of motion

There was a slightly higher contribution of UD to total radioulnar deviation (Fig. 4) which supports the hypothesis (H1) that a larger wrist ROM would be most pronounced on the ulnar side of the wrist.

We only found partial support for the hypothesis (H2) that gibbons would show the highest ROM for both UD and SUP, whereas macaques would show the lowest ROM. Gibbons indeed displayed the highest ROM for both UD (Nomascus: 32.9±4.5 deg, Hylobates: 49.1±9.6 deg, Symphalangus: 50.5±4.0 deg; Fig. 6A) and SUP (Nomascus: 140.1±7.5 deg, Hylobates: 122.3±9.0 deg, Symphalangus: 127.6±19.9 deg; Fig. 6B), and the UD values corresponded to the ROM of Hylobates (49 deg) reported in previous research (Jouffroy and Medina, 2002). For SUP, Macaca showed the lowest ROM, whereas for UD, Pan had the lowest wrist mobility (Fig. 6). This variation in UD ROM between the different primate taxa, but probably also SUP ROM, may relate to the use of terrestrial versus arboreal substrates (Orr et al., 2023) and the differences in compressive and tensile loads involved in locomotion (Lemelin and Schmitt, 1998; Richmond, 2007; Schmitt et al., 2016; Stern and Oxnard, 1973; Swartz et al., 1989).

The high ROM exhibited by gibbons can be explained by their suspensory behaviour, including brachiation, for which a highly mobile wrist is needed (Jenkins, 1981; Richmond, 2006; Sarmiento, 1988; Vanhoof et al., 2020). In addition, they have specific morphological characteristics, such as a ball-and-socket structure of the midcarpal joint as well as a radial inclination of the ulnar styloid process, which enables significant wrist SUP required in the support phase of brachiation (Lemelin and Schmitt, 1998; Prime and Ford, 2016; Sarmiento, 1988; Vanhoof et al., 2020). The higher ROM for UD in Macaca compared with Pan can be attributed to the greater use of quadrupedal walking of macaques during arboreal travel. Especially on small arboreal supports, Macaca use an ulnar deviated wrist to move safely and securely across the superstrate (Lemelin and Schmitt, 1998; Richmond et al., 2016). Lemelin and Schmitt (1998) showed that macaques use significantly more ulnar deviation when walking on small simulated arboreal supports compared with other cercopithecoids (Lemelin and Schmitt, 1998). During quadrupedal walking, rhesus macaques closely align their forearms with the substrate reaction force vector in the sagittal plane. Their elbows are positioned lateral to the point of substrate contact, which causes the wrist to be used in an ulnar deviated position (Demes et al., 1998) and the lower wrist mobility guarantees stabilization of the wrist, diminishing the energetic costs associated with digitigrade hand postures (Daver et al., 2012). Our study indicated that rhesus macaques exhibit a relatively large maximal ROM during UD (31.2±6.0 deg), whereas the results of Jouffroy and Medina (2002) are twice as high for Macaca (56 deg) and their macaque value is even higher than that of Hylobates (Jouffroy and Medina, 2002). However, they only used one macaque specimen, so this result needs to be interpreted with caution.

In Pan, it is suggested that the lower wrist mobility is functionally linked to knuckle-walking. Their strengthened and more solid wrist is efficient at supporting the often large body weight while resisting forces when the joint is loaded during terrestrial travel (Bucchi et al., 2023; Corruccini, 1978; Kivell, 2016; Kivell and Begun, 2007; Orr, 2017; 2018; Orr et al., 2010; Sarmiento, 1988). In addition, limited ROM in UD in terrestrial primates could facilitate more efficient use of the forelimb during terrestrial walking (Daver et al., 2012; Jones, 1967; Orr, 2017; Tuttle, 1967, 1969). As for SUP, Pan exhibits a higher ROM compared with Macaca, which may be related to the clambering/climbing behaviours of Pan during arboreal travel. In contrast, macaques propel themselves arboreally in the same way as terrestrially, namely via quadrupedal walking (Pontzer and Wrangham, 2004; Rawlins, 1993; Sarringhaus et al., 2014; Wells and Turnquist, 2001). In addition, O'Connor and Rarey (1979) also showed that wrist rotation is significantly lower in Macaca compared with other cercopithecoids and hominoids (O'Connor and Rarey, 1979).

Thompson (2020) reports higher UD values and lower SUP values for Pan in comparison to Macaca, which is the opposite of what our results indicated. Although they only captured hand use on a concrete floor in a lab, and primates probably use a greater proportion of their ROM on naturalistic substrates or even lab-based ‘arboreal’ substrates, it does show that primates do not use their maximal ROM during daily activities. We calculated the maximal ROM of the wrist based on passive movements, whereas Thompson (2020) measured movements during active locomotion (i.e. walking). The maximal ROM is the potential motion the wrist joint can undergo, but only a limited percentage of this is effectively used in daily life activities (i.e. the functional ROM). The recent study of Orr et al. (2023) on ulnar deviation mobility also reports higher values compared with our study (Macaca mulatta: average of 54 deg, Pan: average of 46 deg) (Orr et al., 2023). However, Orr et al. (2010) used a different method to define the long axis of the full forearm (Orr et al., 2010). We could not apply their coordinate system on our dataset; therefore, we used the in-house developed coordinate systems based on the human radius and ulna (Vanneste et al., 2021; Wu and Cavanagh, 1995). These differences in coordinate frame definition seem relevant regarding the differences in ulnar deviation ROM and therefore the maximal ROM absolute values are not directly comparable among our studies. However, we have been consistent in collecting maximal ROM using the same scanning setup and coordinate frame across our dataset, which allows us to mutually compare our different studied specimens.

Although we did not find significant differences in maximal ROM between the hylobatid genera (Fig. 6), we investigated potential shape variation between the hylobatids in the light of differences in body size and locomotion behaviour. White-handed gibbons (Hylobates lar, 4.5 kg) use more leaping and rapid, ricochetal brachiation during travel compared with siamangs (Symphalangus, 12 kg for an adult male), who use more climbing and slower brachiation (Fleagle, 1976).

For the triquetrum, a bivariate scatterplot of PC1 against PC2 (Fig. S2A) separates Nomascus from Hylobates (P=0.01) and Symphalangus (P=0.02) along PC1 (Table S4). Nomascus (positive PC1 values) has a proximodistally long and mediolaterally narrow triquetrum shape, and the facet for the ulna has a slightly deeper cup-like structure. The more cylindrically shaped triquetrum in combination with a relatively flat ulnar articular surface in Hylobates and Symphalangus probably increases the amount of ‘gliding’ possible between the ulnar styloid and the carpus. This morphology allows for a large amount of forearm rotation and ulnar deviation of the wrist, both important during brachiation (Almécija et al., 2015; Lewis, 1977; Sarmiento, 1988). The more ‘robust’ shapes of the triquetrum of Nomascus might be linked to their use of more continuous brachiation (i.e. less ricochetal brachiation) and more climbing or leaping (Wright et al., 2008). For the shape of the hamate and distal ulna, Hylobates show a lot of intrageneric variation. It seems that the triquetral facet on the hamate is relatively larger in Hylobates, which might indicate a larger UD mobility (i.e. gliding on the hamate facet of the triquetrum). This might important during ricochetal brachiation, as they ‘throw’ themselves from one branch to another between each contact with a handhold (i.e. true flight phase) (Chang et al., 2000; Prime and Ford, 2016; Reichard et al., 2016). However, for both the hamate and distal ulna, no significant differences were found between Hylobates, Nomascus and Symphalangus (Fig. S2B,C, Table S4).

Within hylobatids, the maximal ROM during SUP is comparable between the three genera (Fig. 6B), whereas for UD, the ROM of Nomascus is more similar to that of Macaca (Fig. 6A). The specific morphology of Nomascus thus seems to have a larger effect on maximal ROM during UD. Unfortunately, there are very limited data on ranging and locomotor behaviour of Nomascus, a critically endangered genus of the hylobatid family. In addition, owing to the small sample size, it is not clear whether the differences in body size and/or locomotion can explain the differences in distal ulnar, triquetrum and hamate morphology, and thus the results need to be interpreted with caution.

Covariation between wrist morphology and maximal ROM

We hypothesized that the shape differences between the different primate genera are associated with differences in maximal ROM of the wrist during UD and SUP. However, the results of the covariation analysis do not show a correlation between shape and maximal ROM (Figs 7–9). This may be due to several reasons.

Genera with a more recent evolutionary divergence are expected to have more correlated shapes, so accounting for that auto-correlation in a PGLS analysis can explain why the results are less correlated. More primate taxa with distinct phylogenetic positions need to be included to investigate this further. Moreover, although our sample size is too small to control for phylogeny, the datapoints in the regressions are not statistically independent. Therefore, the phylogenetic relationship should be taken into account in future studies.

General primate wrist mobility, besides bone morphology, is influenced by a whole array of other factors such as muscles, ligaments and shape of articulation facets. For example, recent research on ligaments showed that differences between chimpanzees and humans could be linked to stabilization of the wrist during flexion and ulnar deviation (Potau et al., 2022). In addition, more external factors such as age, gender and environment can influence overall wrist mobility. The impact of all these components has not been rigorously documented before, which makes research on these separate aspects very valuable in order to obtain a more complete understanding of wrist mobility in primates.

Conclusions

Gibbons show the highest range of motion for ulnar deviation and supination, which is related to their brachiation and suspensory locomotion. Macaques have an intermediate wrist mobility, with limited supination, which can be linked to their terrestrial and arboreal quadrupedal locomotion with digitigrade or palmigrade hand postures. Pan is characterized by a rigid and stable, and therefore less mobile, wrist, which is probably a functional adaptation to weight-bearing functions during knuckle-walking. However, supination in Pan is high and can be related to hand use during arboreal locomotor mode. In all primate genera, we found no significant association between maximal ROM during UD/SUP and distal ulnar/triquetrum/hamate shape. In future studies, it would be interesting to sample different developmental stages of a broader range of taxa and to also include more individuals per species to account for intraspecific variation. In addition, the combination of morphological and functional data together with in vivo investigations and behavioural research is essential to obtain comprehensive form–function relationships of the wrist joint and hand, which can provide more insight into the evolutionary history of the human forearm and hand.

The authors thank the different zoos and institutes that provided the primate specimens: Pieter Cornillie (Ghent University, campus Merelbeke), Koen Nelissen (KU Leuven, campus Gasthuisberg), François Druelle (Zoological and Botanical Park of Mulhouse, France), Robby Van der Velden (Pakawi Park, Belgium), Sergio Almécija (American Museum of Natural History, Division of Anthropology, New York), Emmanuel Gilissen (Royal Museum for Central Africa, Belgium) and Pierre de Wit (Adventure Zoo Emmen, The Netherlands). Furthermore, we thank Dr Olivier Vanovermeire and Henk Lacaeyse from the Medical Imaging Department, AZ Groeninge (Kortrijk, Belgium), for CT-scanning of the specimens. We also thank Colette Wagemans for her help during the analysis. Finally, we thank the students who assisted during segmentation of the CT scan images.

Author contributions

Conceptualization: M.J.M.V.; Methodology: M.J.M.V., L.G.; Software: L.G.; Validation: M.J.M.V.; Formal analysis: M.J.M.V.; Investigation: M.J.M.V.; Data curation: M.J.M.V.; Writing - original draft: M.J.M.V.; Writing - review & editing: L.G., I.D., E.E.V.; Visualization: M.J.M.V.; Supervision: E.E.V.

Funding

This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Competing interests

The authors declare no competing or financial interests.

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