# Functional and behavioral variation in intrinsic hand and foot digit proportions in primates

Séverine L.D. Toussaint, Vincent d'Amato, Joanna Desmidt, Mélanie Berthet, Benoît Quintard, François Druelle

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Séverine L.D. Toussaint, Vincent d'Amato, Joanna Desmidt, Mélanie Berthet, Benoît Quintard, et al. Functional and behavioral variation in intrinsic hand and foot digit proportions in primates. Journal of Human Evolution, 2025, 203, pp.103679. 10.1016/j.jhevol.2025.103679. hal-05191140

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# Functional and behavioral variation in intrinsic hand and foot digit proportions in primates

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Séverine L.D. Toussaint<sup>a, b, *</sup>, Vincent D'Amato<sup>c</sup>, Joanna Desmidt<sup>d</sup>, Mélanie Berthet<sup>e</sup>, Benoît Quintard<sup>f</sup>, François Druelle<sup>c, d, g</sup>

## ARTICLE INFO

**Article history:**

Received 3 October 2024

Accepted 23 March 2025

Available online xxx

Handling Editor: Dr S Xing

**Keywords:**

Phalanx

Metapod

Grasping

Locomotion

## ABSTRACT

The relative elongation of the digits on the autopods has long been considered as an adaptation for an arboreal lifestyle shared by several tetrapods. In primates, this morphological adaptation constitutes one of the defining characters of the order and is correlated to their enhanced manual and pedal grasping capabilities. However, primates are highly diversified in terms of body mass and locomotor repertoire, and it remains unclear to what extent the elongation of proximal and intermediate phalanges relative to metapodials (i.e., the phalangeal index) correlates with body mass or grasping performances during arboreal locomotion. In this study, we tested the effect of body mass, grasping performance, and phylogeny on the manual and pedal phalangeal indexes in 58 species of nonhuman primates, including strepsirrhines, platyrrhines, and catarrhines. We computed a grasping score as a proxy for grasping performance based on the known locomotor repertoire of each species. We found that body mass negatively correlates with the intrinsic digit proportions of the hand, whereas the grasping score positively correlates with the intrinsic digit proportions of both the hand and foot. Our results highlight the different functional roles of the hand and foot in nonhuman primates. The hand is more influenced by changes in body size (allometric constraints), while the foot primarily functions to anchor to arboreal supports. Moreover, finger elongation appears most critical for enhancing grasping performance in species weighing over 5 kg as the general decrease in power-to-weight ratio and the specific postural adaptations in larger species likely increase locomotor constraints on the forelimb. By building a finer model of the morphofunctional complexes of the hand and foot in primates, linking phalangeal index, body mass, and locomotor repertoire, this comparative study will also help to better understand the evolution of autopodial adaptations in other arboreal models such as in rodents and marsupials.

© 2025 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license

(http://creativecommons.org/licenses/by/4.0/).

## 1. Introduction

The specific morphological adaptations of primates' hand and foot, such as the relative elongation of their digits, are among the defining characters of the order and are largely considered as shared by their common ancestor (Cartmill, 1992; Hamrick, 2001; Bloch and Boyer, 2002; Kirk et al., 2008; Boyer et al., 2013). Such elongation of digits in primates is primarily attributed to an

elongation of the proximal and intermediate phalanges relative to the metapodials (Hamrick, 2001; Kirk et al., 2008). Relatively longer phalanges have been described in several arboreal tetrapods including mammals, amphibians, and birds and have been previously suggested to enhance grasping performance during arboreal locomotion (Lemelin and Grafton, 1998; Lemelin, 1999; Hamrick, 2001; Hopson, 2001; Lemelin and Schmitt, 2007; Kirk et al., 2008; Pouydebat et al., 2023; Young, 2023). In this context, the increase of the phalangeal index (PI), defined as the sum of the lengths of proximal and intermediate phalanges relative to the metapodial length, is typically explained in primates as an

<footnote><sup>a</sup> UMR 7207, Centre de Recherche en Paléontologie-Paris, CNRS-MNHN-SU, 75005 Paris, France</footnote>

<footnote><sup>b</sup> AG Vergleichende Zoologie, Institut für Biologie, Humboldt Universität zu Berlin, 10115 Berlin, Germany</footnote>

<footnote><sup>c</sup> UMR 7194, Histoire Naturelle des Humanités Préhistoriques, CNRS-MNHN-UPVD, 75116 Paris, France</footnote>

<footnote><sup>d</sup> Functional Morphology Laboratory, University of Antwerp, 2610 Antwerp, Belgium</footnote>

<footnote><sup>e</sup> Besançon Museum, 25000 Besançon, France</footnote>

<footnote><sup>f</sup> Zoological and Botanical Park of Mulhouse, 68100 Mulhouse, France</footnote>

<footnote><sup>g</sup> UMR 7268, Anthropologie bio-culturelle, Droit, Ethique et Santé, AMU-CNRS-EFS, 13015 Marseille, France</footnote>

<footnote>* Corresponding author.
E-mail address: severine.toussaint@mnhn.fr (S.L.D. Toussaint).</footnote>
adaptation for an arboreal lifestyle and an early specialization for
the use of the fine-branch milieu (Hamrick, 2001; Lemelin and
Schmitt, 2007; Boyer et al., 2013). Early primates successfully
invaded the arboreal niche around 65 Ma ago, with key adaptations
such as enhanced limb mobility and autopodial grasping capacity,
reducing the risk of falling and increasing their maneuverability
(Cartmill, 1972, 1992). In effect, relatively longer phalanges enable
the digits to completely wrap around small-diameter branches and
vines (Lemelin, 1999; Lemelin and Schmitt, 2007; Toussaint et al.,
2020). However, it is unclear yet to what extent the PI might be
related to grasping performance in the context of specific arboreal
locomotor adaptations within primates.

Arboreal locomotion is complex and integrates a variety of
specific behavioral and musculoskeletal adaptations. Among pri-
mates, although some catarrhine species exhibit terrestrial habits,
all nonhuman primates remain highly arboreal and show consid-
erable diversification in their locomotor modes and postural spe-
cializations, ranging from above-branch quadrupedal walking to
vertical climbing and leaping, below-branch suspension, and
brachiation (Hunt et al., 1996; Fleagle, 2013; Granatosky, 2018).
Each substrate preference and locomotor specialization induce
different constraints, which translate into different uses of the
grasping capabilities depending on the species (Hunt et al., 1996;
Toussaint et al., 2020). Moreover, a number of behavioral and
musculoskeletal studies have highlighted that in primates, the
forelimb and hindlimb exhibit very distinctive functional roles
compared to other arboreal tetrapods (e.g., Kimura, 1992; Demes
et al., 1994; Hashimoto et al., 2011; Patel et al., 2015; Granatosky
and Schmitt, 2017; Granatosky et al., 2019; Young, 2023). The foot
is posturally less variable across species and is capable of a more
powerful grasping, contrary to the hand whose postures are more
variable across species, probably due to their greater involvement
in nonlocomotor behaviors (Cartmill, 1972; Preuschoft, 2002; Patel
et al., 2015; Hanna et al., 2017; Toussaint et al., 2020).

Previous ontogenetic studies have investigated the changes in
intrinsic autopodial proportions during growth in catarrhine pri-
mates (capuchins monkeys [Young and Heard-Booth, 2016] and
olive baboons [Druelle et al., 2018; Boulinguez-Ambroise et al.,
2021]). They found that juveniles globally exhibit longer pha-
langes than adults, concomitantly with a higher demand of
grasping behaviors during youth, notably for secure clinging to
their mother's fur, and during play and exploratory behaviors
which involve a greater proportion of climbing and arboreal sup-
ports use (Druelle et al., 2018). These results corroborate the
hypothesis that relative phalangeal and metapodial elongation is
closely related to a greater proportion of arboreal locomotor
repertoire. Nevertheless, a study on rats, *Rattus norvegicus*, has
shown a similar ontogenetic pattern in this rodent species,
applying a potentially shared pattern within mammals, or at least
Euarchontoglires (Young et al., 2019). This adaptation may have
undergone further evolutionary development within the primate
order, influenced by distinct selective pressures acting on both the
hand and the foot.

Another fundamental aspect that must be considered when
studying grasping performance in the context of arboreal locomo-
tion is body mass as it directly correlates with the gravitational
forces, imposing increased mechanical challenges on the locomotor
system (e.g., Napier, 1967; Schmidt-Nielson, 1984; Cartmill, 1985;
Biewener, 1989; Lemelin and Jungers, 2007; Hanna et al., 2008). For
instance, climbing in trees imposes more energetic constraints as
the body mass increases, and it is energetically more demanding to
climb vertical supports than walking horizontally for primates
weighing more than 0.5 kg (Taylor et al., 1972; Hanna et al., 2008;
Hanna and Schmitt, 2011). Extant primates exhibit a broad range of
body masses across groups, from the pygmy mouse lemur,

Microcebus berthae (strepsirrhine) weighting about 30 g, to the
western gorilla, *Gorilla gorilla* (catarrhine) that can reach a weight
of 200 kg or more (in males, see Fig. 1A). However, male gorillas are
the least arboreal of all extant nonhuman apes (e.g., Doran, 1997;
Hunt, 2016), suggesting that beyond a certain body mass, the me-
chanical challenges of arboreal locomotion (propulsion, balance
control, stability, maneuverability, and energetic cost) may exceed
what can be offset by specific morphological adaptations. The
biggest exclusive arboreal primates are the orangutans *Pongo* spp.,
weighting about 60–90 kg (Thorpe and Crompton, 2006; Thorpe
et al., 2009). This variation in body mass is accompanied by a
variation in locomotor habits and substrate preferences (Demes
and Günther, 1989; Schmidt, 2011; Fleagle, 2013).

Lemelin and Jungers (2007) investigated the relationship be-
tween autopodial intrinsic proportions and body mass in a wide
sample of strepsirrhines and tarsiers (<7 kg) and found that as body
mass increases, the relative length of the digits globally decreases
within these groups (i.e., negative allometry). A detailed analysis of
the data in the study by Lemelin and Jungers revealed some specific
scaling trends within families, as well as some notable exceptions
in tarsiers (Tarsius sp.) and aye-ayes (Daubentonia sp.) that possess
remarkably long fingers compared to their toes in relation to their
body size, a morphology likely linked to their specialized modes of
prey acquisition involving the hands.

To our knowledge, no study has yet investigated the combined
relationship between intrinsic proportions of the hand and foot, a
quantitative assessment of grasping ability associated with specific
locomotor adaptations, and body mass in a comparative and
phylogenetic context across nonhuman primates. Although
numerous studies have investigated the shape and size of primate
feet and hands with an evolutionary perspective (Schultz, 1930;
Straus, 1942; Schultz, 1968; Tuttle, 1970; Richmond, 1998; Hamrick,
2001; Almécija et al., 2009, 2015; Patel, 2010; Patel et al., 2015;
Grabowski and Jungers, 2017; Prang, 2019; Prang et al., 2021), new
insights can still be gained by adopting a different approach. Here,
we propose a straightforward and simple mechanical model to test
the functional relationship between intrinsic digit proportions and
behavioral habits associated with grasping ability. By using a
quantitative assessment of the use of specific locomotor modes in
which grasping abilities are required, we aim to test the incidence
of a simple morphological parameter, easily obtained from the
skeletal morphology of the hands and feet, on the incidence of
grasping behaviors. In this study, we provide a broad comparison of
autopodial PI in 58 primate species, sampling all major groups and
locomotor diversity of primates. We computed a grasping score
(GS) to reflect the proportion of use of the digits during grasping
behaviors involved according to the locomotor repertoires of each
species (data extracted from the literature), following the previ-
ously developed methodology of Druelle et al. (2018). Such
behavioral data, widely documented in the literature on numerous
species, can provide a window on the grasping capacities of pri-
mates as they offer a general perspective on how primates rely on
behaviors requiring strong grasping capacities. If skeletal
morphology imposes constraints on the ability to grasp substrates
during locomotion, it should influence locomotor habits (i.e., pro-
portion of use) that depend on this capacity and impact the
ecological niche available. In this context, we propose that varia-
tions in spontaneous suspensory, climbing, and clambering
behaviors (see details below) can be used as a useful proxy for
evaluating grasping performance across primate species. Further-
more, since species are statistically nonindependent and our sam-
ple includes varying degrees of phylogenetic relatedness, we
accounted for the potential phylogenetic signal in our analyses
(Felsenstein, 1985; Harvey and Pagel, 1991). Hence, we tested the
relationship between autopodial intrinsic proportions and this
<figure><img src="image_4.png" /><figcaption>**Figure 1.** A) Consensus phylogenetic tree (chronogram) of the studied species obtained from the 10kTrees website (https://10ktrees.nunn-lab.org/; Arnold et al., 2010) including mean body mass mapped onto it using the *contMap* function in *phytools* in R. The estimate of ancestral states at the nodes is based on the principles of maximum likelihood under a Brownian motion model. B) Associated grasping scores of each species computed in this study are represented using bar plots. C) Radiographs of selected individuals belonging to various species studied. Abbreviations: RH = right hand; LH = left hand; RF = right foot; LF = left foot; MT = metapod; PP = proximal phalanx; IP = intermediate phalanx; 1 = digit 1; 2 = digit 2; 3 = digit 3; 4 = digit 4; 5 = digit 5. (For interpretation of the references to color in this figure, the reader is referred to the Web version of this article.)</figcaption></figure>

grasping performance proxy as well as body mass in a phylogenetic comparative context. In view of previous works, we hypothesize that intrinsic digit proportions will determine the locomotor habits of primates, specifically the amount of time they spend grasping substrates in challenging locomotor modes (i.e., climbing, suspensory modes, brachiation, clambering, transfer, sway, and bridge; see Hunt et al., 1996). We predict that 1) body mass impacts the intrinsic proportions of the autopods, with larger species likely to have shorter phalanges than their metapods; 2) specific locomotor strategies correlate with intrinsic proportion in primates, with species with higher GSs likely to have longer phalanges than their metapods; and 3) hand and foot intrinsic proportions may not correlate in the same way with body mass and GS due to their differential functional roles.

While this approach may overlook the complexity of primate grasping capacities by excluding soft tissues (muscles, tendons, ligaments, and fascia) and additional bone-derived metrics, simple models can still provide valuable insights in the context of primate function and evolution (Alexander, 1992) as they are particularly useful for interpreting fossil material, which is

inherently highly fragmentary and lacks any preservation of soft tissue elements.

## 2. Material and methods

### 2.1. *Studied specimens*

We studied hands and feet of 171 individuals from 58 species of nonhuman primates, including 14 lemuriformes, three lorisiformes, one tarsiiformes, 21 platyrrhines, and 19 catarrhines (see Supplementary Online Material [SOM] Table S1 for the complete list of specimens measured). Data were obtained from 1) radiographs of living individuals housed at the zoological parks of Mulhouse and Besançon and at the Primatology Station of Rousset sur Arc (France); 2) preserved skeletons of the comparative anatomy collections of the National Museum of Natural History of Paris (France), the Natural History Museum of London (UK), and the Field Museum of Natural History of Chicago (USA); 3) the literature (Zihlman and Underwood, 2013; Thompson et al., 2020); and 4) computed tomographic scans of preserved skeletons obtained in
the literature via the open-access MorphoSource depository (https://www.morphosource.org), provided by Sergio Almcija from the American Museum of Natural History of New York (USA), in the case of *G. gorilla* and *Pongo pygmaeus*, and shared by Evie Vereecke from KU Leuven (Belgium) in the case of the specimen of *Pan paniscus*. Radiographs were opportunistically collected over time upon routine veterinary checkups and interventions, and no animal was anesthetized for the sole purpose of this study. All radiographs were digitized with a resolution of 10 pixels per millimeter.

## 2.2. Data collection

We measured the linear maximal lengths of all metapods (i.e., metacarpals and metatarsals) and proximal and intermediate phalanges of each one of the five digits of one hand and one foot by an individual whenever possible (note that the pollex and hallux in primates, as well as most modern arboreal mammals, have lost the intermediate phalanx, so we only measured the metapod and proximal phalanx), following previously described protocols (e.g., Young and Heard-Booth, 2016; Druelle et al., 2018). Distal phalanges were not considered in this protocol due to the large morphological variability of this structure between species and to ensure consistent comparison with previous studies on mammalian intrinsic autopodial proportions (Napier, 1960; Lemelin and Grafton, 1998; Lemelin, 1999; Hamrick, 2001, 2007; Kirk et al., 2008; Patel et al., 2009; Young and Heard-Booth, 2016; Druelle et al., 2018). Measurements from preserved skeletons were taken directly in millimeters using a digital caliper. We selected articulated specimens to ensure exact identification of digits' number. Measurements from radiographs were taken using the software ImageJ and calibrated from pixels to millimeters using scale bars included in the radiographs, when available. Otherwise, the PI was estimated directly from pixels (see the ratio below). In these radiographs, autopods were positioned in the dorsal view so that the palmar and plantar surfaces lie on the X-ray cassette. (We used tape to maintain the autopods in this posture during the recording.) The obtained radiographs allow clear differentiation between digits and accurate measurement of each bone segment length.

We additionally collected the body mass of each individual/species studied. For data obtained from radiographs, we used the average body mass directly measured on each individual studied during routine veterinary checkups in zoos. For data obtained from preserved skeletons, we used the mean body mass by species from Fleagle (2013; see SOM Table S2). To evaluate the influence of using individual body mass from zoo specimens vs. using the mean body mass of wild animals extracted from literature, we conducted a complementary analysis using body mass extracted from Fleagle (2013) only for all species (see SOM Table S3; the results obtained are not different from the ones using body mass of animals from zoos).

## 2.3. Data analysis

**Phalangeal indices computation** We computed the PI for each hand and foot digit (D) for each individual as follows:

$$PI_D = \frac{(\text{proximal phalanx length}_D + \text{intermediate phalanx length}_D)}{\text{metapod length}_D}$$

Given the existing differences of relative lengths among digits within hands and feet (digits III and IV being longer than digits II and V, thus potentially affecting the associated digital intrinsic proportion), we computed the averaged PI of digits II to V, of digits II + V, and of digits III + IV for each hand and foot separately for

each individual. The PIs were then averaged by species (see SOM Table S2 for the complete dataset).

**Grasping score computation** We extracted from the literature the locomotor repertoire described for each species of interest whenever available (Table 1). We considered only the locomotor repertoire and excluded other behaviors such as the postural repertoire performed during social and feeding contexts (according to Hunt et al., 1996). While hands and feet are also involved in these behaviors, challenging locomotor activities that require strong grasping forces and endure high mechanical stress are more likely to be directly influenced by subtle variations in the musculoskeletal system. In effect, variations in intrinsic digit proportions may directly constrain the ability of primates to climb, suspend, and move effectively in the trees, and natural selection operates on these variations depending on the environment (Arnold, 1983; Lemelin and Grafton, 1998; Kirk et al., 2008). From the locomotor repertoires, we calculated a GS by extracting the total proportion of locomotor modes that involve the use of digits to grasp arboreal substrates (following the methodology developed in Druelle et al., 2018). Those locomotor modes include vertical ascent and descent, brachiation, clambering, transfer, sway, bridge, and all suspensory modes (including bimanual modes; see Gebo, 1992; Hunt et al., 1996 for precise definitions of each locomotor mode). We did not include arboreal quadrupedalism because although it is commonly used in primate arboreal locomotion, the size of the substrate is not consistently provided in the literature associated with this locomotor mode. However, the level of grasping capacities required to accomplish this behavior may greatly differ depending on the size, orientation, and compliance of the substrate (e.g., large branch vs. twigs; Toussaint et al., 2020). We therefore decided to exclude this heterogeneous category from our dataset. The GS obtained provides a percentage between 0 (no use of digital grasping during locomotion) and 100 (exclusive use of digital grasping during locomotion) for each species (Table 1; Fig. 1B). We could not compute the GS for the babakoto (*Indri indri*) and the owl monkeys (*Aotus* sp.), and for some species, we used the locomotor repertoire of another closely related species due to a lack of their respective locomotor repertoire quantification in the literature (see Table 1 for details).

**Phylogenetic computation** As primates share an evolutionary history, the digit intrinsic proportions and body mass are likely to exhibit patterns consistent with evolutionary processes (Grabowski and Jungers, 2017; Pampush et al., 2021), as well as for what concerns their behavioral habits (Kamilar and Cooper, 2013). Hence, we have taken into account the phylogenetic component in our analysis. Nevertheless, note that our objective is not to explore various phylogenetic models for these traits but instead to include the potential influence of the phylogenetic nonindependence between the species studied (Harvey and Pagel, 1991). Therefore, to relax the assumption of the typical Brownian motion model in our phylogenetic analyses, we used the λ of Pagel, and the branch length was optimized using maximum likelihood (see below).

We used a time-scaled phylogeny based on a consensus chromometric tree (i.e., branch lengths are proportional to absolute time) of extant primate species obtained from the 10kTrees website (https://10ktrees.nunn-lab.org/; Arnold et al., 2010) that provides phylogenies of extant mammalian groups sampled from a Bayesian analysis. However, as this phylogeny based on the taxonomy of GenBank does not exactly match all the taxa names of our morphological dataset and of the literature relative to locomotor repertoires, we approximated some of our initial species with the most closely related species present in the phylogeny (see Table 1). **Statistical analysis** All statistical analyses were performed using the R software v.4.0.3, supplemented by the 'caper,' 'phytools,' and 'sensiPhy' packages. All variables were log₁₀-transformed before
<table><caption>**Table 1**
Grasping score estimation and associated references of locomotor repertoires used by species.</caption><thead><tr><th colspan="3">Species studied</th><th rowspan="2">Grasping score</th><th rowspan="2">Reference</th></tr><tr><th>Measured</th><th>Used in phylogenetic tree</th><th>Used for locomotor repertoire</th></tr></thead><tbody><tr><td>Allochrocebus lhoesti</td><td>Cercopithecus lhoesti</td><td>Cercopithecus diana</td><td>22.00</td><td>In Hunt (2016), from McGraw (1998a, 1998b)</td></tr><tr><td>Aotus felinus</td><td>Aotus trivirgatus</td><td>N/A</td><td></td><td></td></tr><tr><td>Aotus trivirgatus</td><td>Aotus infulatus</td><td>N/A</td><td></td><td></td></tr><tr><td>Ateles fusciceps</td><td>Ateles fusciceps</td><td>Ateles paniscus</td><td>76.7<sup>a</sup></td><td>In Youlatos (2002), averaged from travel and feeding contexts</td></tr><tr><td>Callicebus cupreus</td><td>Callicebus hoffmannsi</td><td>Callicebus moloch</td><td>28.20</td><td>Youlatos (1999)</td></tr><tr><td>Callicebus personatus</td><td>Callicebus personatus</td><td>Callicebus moloch</td><td>28.20</td><td>Youlatos (1999)</td></tr><tr><td>Callithrix geoffroyi</td><td>Callithrix geoffroyi</td><td>Callithrix jacchus</td><td>13.00</td><td>Youlatos and Meldrum (2011)</td></tr><tr><td>Cebuella pygmaea</td><td>Callithrix pygmaea</td><td>Cebuella pygmaea</td><td>21.79<sup>a</sup></td><td>Averaged from Youlatos (1999) and Jackson (2011)</td></tr><tr><td>Cercopithecus hamlyni</td><td>Cercopithecus hamlyni</td><td>Cercopithecus diana</td><td>22.00</td><td>Hunt (2016)</td></tr><tr><td>Cercopithecus roloway</td><td>Cercopithecus diana</td><td>Cercopithecus diana</td><td>22.00</td><td>Hunt (2016)</td></tr><tr><td>Colobus guereza</td><td>Colobus guereza</td><td>Colobus angolensis</td><td>13.67</td><td>Dunham (2015)</td></tr><tr><td>Eulemur albocollaris</td><td>Eulemur fulvus albocollaris</td><td>Eulemur fulvus</td><td>27.45</td><td>Gebo (1987)</td></tr><tr><td>Eulemur coronatus</td><td>Eulemur coronatus</td><td>Eulemur coronatus</td><td>34.65</td><td>Gebo (1987)</td></tr><tr><td>Eulemur flavifrons</td><td>Eulemur macaco flavifrons</td><td>Eulemur macaco</td><td>38.61</td><td>Gebo (1987)</td></tr><tr><td>Eulemur fulvus albifrons</td><td>Eulemur fulvus albifrons</td><td>Eulemur fulvus</td><td>27.45</td><td>Gebo (1987)</td></tr><tr><td>Eulemur mongoz</td><td>Eulemur mongoz</td><td>Eulemur fulvus</td><td>27.45</td><td>Gebo (1987)</td></tr><tr><td>Eulemur rubriventer</td><td>Eulemur rubriventer</td><td>Eulemur fulvus</td><td>27.45</td><td>Gebo (1987)</td></tr><tr><td>Hapalemur alaotrensis</td><td>Hapalemur griseus alaotrensis</td><td>Hapalemur griseus</td><td>22.86</td><td>Gebo (1987)</td></tr><tr><td>Hylobates pileatus</td><td>Hylobates pileatus</td><td>Hylobates lar</td><td>77.00</td><td>Fleagle (1976)</td></tr><tr><td>Indri indri</td><td>Indri indri</td><td>N/A</td><td></td><td></td></tr><tr><td>Leontopithecus chrysomelas</td><td>Leontopithecus chrysomelas</td><td>Leontopithecus chrysomelas</td><td>25.74</td><td>Rosenberger and Stafford (1994)</td></tr><tr><td>Leontopithecus rosalia</td><td>Leontopithecus rosalia</td><td>Leontopithecus rosalia</td><td>15.73</td><td>Youlatos and Meldrum (2011)</td></tr><tr><td>Macaca nigra</td><td>Macaca nigra</td><td>Macaca assamensis</td><td>47.30</td><td>Huang et al. (2015)</td></tr><tr><td>Microcebus murinus</td><td>Microcebus murinus</td><td>Microcebus murinus</td><td>32.67</td><td>Gebo (1987)</td></tr><tr><td>Callithrix argentata</td><td>Callithrix argentata</td><td>Callithrix jacchus</td><td>13.00</td><td>Youlatos and Meldrum (2011)</td></tr><tr><td>Nomascus gabriellae</td><td>Nomascus gabriellae</td><td>Nomascus nasutus</td><td>91.00</td><td>Fan et al. (2013)</td></tr><tr><td>Nomascus leucogenys</td><td>Nomascus leucogenys</td><td>Nomascus nasutus</td><td>91.00</td><td>Fan et al. (2013)</td></tr><tr><td>Nomascus siki</td><td>Nomascus siki</td><td>Nomascus nasutus</td><td>91.00</td><td>Fan et al. (2013)</td></tr><tr><td>Pithecia pithecia</td><td>Pithecia pithecia</td><td>Pithecia monachus</td><td>24.80</td><td>Youlatos (1999)</td></tr><tr><td>Plecturocebus cupreus</td><td>Callicebus moloch</td><td>Callicebus moloch</td><td>28.20</td><td>Youlatos (1999)</td></tr><tr><td>Hapalemur alaotrensis</td><td>Hapalemur simus</td><td>Hapalemur griseus</td><td>22.86</td><td>Gebo (1987)</td></tr><tr><td>Propithecus coronatus deckenii</td><td>Propithecus deckenii</td><td>Propithecus verreauxi</td><td>45.00</td><td>Gebo (1987)</td></tr><tr><td>Propithecus verreauxi</td><td>Propithecus verreauxi</td><td>Propithecus verreauxi</td><td>45.00</td><td>Gebo (1987)</td></tr><tr><td>Saguinus bicolor</td><td>Saguinus bicolor</td><td>Saguinus geoffroyi</td><td>7.41</td><td>Garber (1991)</td></tr><tr><td>Saguinus imperator</td><td>Saguinus imperator</td><td>Saguinus mystax</td><td>12.15</td><td>Garber (1991)</td></tr><tr><td>Saguinus midas</td><td>Saguinus midas</td><td>Saguinus midas</td><td>14.38<sup>a</sup></td><td>In Youlatos and Meldrum (2011), averaged from two sites (French Guiana and Surinam)</td></tr><tr><td>Saguinus oedipus</td><td>Saguinus oedipus</td><td>Saguinus geoffroyi</td><td>7.41</td><td>Garber (1991)</td></tr><tr><td>Saimiri boliviensis</td><td>Saimiri boliviensis</td><td>Saimiri boliviensis</td><td>7.00</td><td>Youlatos and Meldrum (2011)</td></tr><tr><td>Saimiri sciureus</td><td>Saimiri sciureus</td><td>Saimiri sciureus</td><td>17.74<sup>a</sup></td><td>In Youlatos and Meldrum (2011), averaged from two sites (Ecuador and Surinam)</td></tr><tr><td>Sapajus xanthosternos</td><td>Cebus xanthosternos</td><td>Cebus capucinus</td><td>30.69</td><td>Gebo (1992)</td></tr><tr><td>Cebus apella</td><td>Cebus apella</td><td>Cebus albifrons</td><td>24.20</td><td>Youlatos (1999)</td></tr><tr><td>Cebus capucinus</td><td>Cebus capucinus</td><td>Cebus capucinus</td><td>30.69</td><td>Gebo (1992)</td></tr><tr><td>Symphalangus syndactylus</td><td>Symphalangus syndactylus</td><td>Symphalangus syndactylus</td><td>88.00</td><td>Fan et al. (2013)</td></tr><tr><td>Theropithecus gelada</td><td>Theropithecus gelada</td><td>Terrestrial cercopiths<sup>b</sup></td><td>1.02</td><td>Hunt (2016)</td></tr><tr><td>Trachypithecus francoisi</td><td>Trachypithecus francoisi</td><td>Trachypithecus leucocephalus</td><td>26.85</td><td>Huang and Li (2005)</td></tr><tr><td>Varecia rubra</td><td>Varecia rubra</td><td>Varecia variegata</td><td>43.56</td><td>Gebo (1987)</td></tr><tr><td>Varecia subcincta</td><td>Varecia variegata variegata</td><td>Varecia variegata</td><td>43.56</td><td>Gebo (1987)</td></tr><tr><td>Gorilla gorilla</td><td>Gorilla gorilla gorilla</td><td>Gorilla gorilla</td><td>14.65<sup>a</sup></td><td>In Hunt (2004), recalculated from Tuttle and Watts (1985), Remis (1995) and Doran (1996)</td></tr><tr><td>Pan troglodytes</td><td>Pan troglodytes troglodytes</td><td>Pan troglodytes</td><td>19.30</td><td>Sarringhaus et al. (2014)</td></tr><tr><td>Pan paniscus</td><td>Pan paniscus</td><td>Pan paniscus</td><td>63.11<sup>a</sup></td><td>In Hunt (2020), recalculated from Doran and Hunt (1996) and Ramos (2014)</td></tr><tr><td>Pongo pygmaeus</td><td>Pongo pygmaeus</td><td>Pongo pygmaeus</td><td>73.27</td><td>Thorpe and Crompton (2006)</td></tr><tr><td>Erythrocebus patas</td><td>Erythrocebus patas</td><td>Erythrocebus patas</td><td>4.90</td><td>Isbell et al. (1998)</td></tr><tr><td>Cercopithecus aethiops</td><td>Chlorocebus aethiops</td><td>Cercopithecus aethiops</td><td>29.17</td><td>Isbell et al. (1998)</td></tr><tr><td>Loris tardigradus and Loris gracilis</td><td>Loris tardigradus</td><td>Loris tardigradus</td><td>84.31<sup>a</sup></td><td>Averaged from Gebo (1987) and Nekaris (2000)</td></tr><tr><td>Nycticebus coucang</td><td>Nycticebus coucang</td><td>Nycticebus coucang</td><td>75.00</td><td>Gebo (1987)</td></tr><tr><td>Tarsius syrichta</td><td>Tarsius syrichta</td><td>Tarsius syrichta</td><td>37.00</td><td>Tilden (1990)</td></tr><tr><td>Papio anubis</td><td>Papio anubis</td><td>Papio anubis</td><td>1.40</td><td>Rose (1977)</td></tr></tbody></table>

<footnote><sup>a</sup> Species for which a mean grasping score was computed from more than one locomotor repertoire. This was performed when some variation was observed between different studies applied on the same species, when different activity contexts were provided without providing a general repertoire, or when the same species was observed at different sites.</footnote>

<footnote><sup>b</sup> As defined in Hunt (2016).</footnote>
statistical analysis to ensure normality and homoscedasticity assumptions. (These assumptions were tested using the Shapiro-Wilk test and Breusch-Pagan test, respectively, as well as by using a visual inspection of the distribution of the residuals.) We set statistical significance at *p* < 0.05.

We used phylogenetic generalized least squares (PGLS) linear models to test the relationships between the PIs (dependent variable) and the body mass (independent variable) and between the PIs (independent variable) and the GS (dependent variable). Then, to investigate the joint influence of the morphological parameters (i.e., intrinsic autopodial proportions and body mass) on the grasping capacities associated with locomotor modes, we used the PGLS method to test various associations of the effect of the PIs and the body mass on the GS. We used the Akaike Information Criterion (AIC) to select which of these models best describes these morphofunctional relationships (Table 2). The significance of individual coefficients of the resulting best-fitting model was assessed using the standard *t*-test. Finally, to evaluate the influence of the species sampled, and the robustness of the best-fitting model obtained, we used a sensitivity analysis for phylogenetic comparative methods using the 'influ_phylm' function in R, following Paterno et al. (2018).

As results using the average PI of digits II + V and digits III + IV did not significantly differ from those using the average PI of digits II to V of the hand and foot (see SOM Table S4 for comparative results), the following results present the analysis using the following four PIs: hand digit I (pollex), foot digit I (hallux), manual digits II to V combined, and pedal digits II to V combined.

## 3. Results

### 3.1. Relationship between intrinsic digit proportions and body mass

Phalangeal indices vary among primate groups. Strepsirrhines exhibit relatively higher PIs than haplorrhines (Fig. 2). Also, PIs of the hand are higher overall than those of the foot in all primate groups (Fig. 2).

We found a significant negative correlation between the body mass and the intrinsic proportions of the hand (pollex and manual digits II to V) in our studied species (PGLS: PI of manual digits II to V: adjusted r² = 0.13, t = -2.95, *p* = 0.005, Fig. 3A; PI of the pollex: adjusted r² = 0.07, t = -2.22, *p* = 0.031, Fig. 3B) but no significant correlation between the body mass and the foot proportions (Fig. 3C, D).

### 3.2. Relationship between intrinsic digit proportions and grasping score

We found a significant correlation between the GS and the intrinsic proportions of the hand (pollex and manual digits II to V) and the pedal digits II to V (PGLS: PI of manual digits II to V: adjusted r² = 0.25, t = 4.20, *p* = 0.0001, Fig. 4A; PI of the pollex: adjusted r² = 0.16, t = 3.23, *p* = 0.0022, Fig. 4B; PI of pedal digits II to V: adjusted r² = 0.31, t = 4.87, *p* < 0.0001, Fig. 4C), but not between the GS and the hallux intrinsic proportion (Fig. 4D). Interestingly, among the models tested, we found that the best model explaining the GS includes the intrinsic proportion of the pedal digits II to V (t = 4.05, *p* = 0.0002) and the interaction between the intrinsic proportion of the manual digits II to V and body mass (t = 2.81, *p* = 0.007; AIC = -2.06; Table 2; SOM Table S5). According to the sensitivity analysis, we observed that five species may influence the best-fitting model found: the olive baboon, Papio anubis (9.9% change), the black-headed spider monkey, Ateles fusciceps (8.5% change), the Sunda slow loris, Nycticebus coucang (8.4% change), the bonobo, P. paniscus (8.1% change), and the common patas monkey, Erythrocebus patas (6.8% change; see species sensitivity test in SOM Table S6 and SOM Fig. S1). However, alternatively removing these species from the dataset has no impact on the significance and general robustness of the best-fitting morphofunctional model obtained (SOM Table S7).

Interestingly, Preuschoft et al (1996) observed that biomechanical demands and constraints vary with size in primates in the same way as in other vertebrates, i.e., small primates rely on 'accelerating' strategies, while large ones rely on 'maintaining speed' strategies. In this context, they suggested that the size threshold at which primates switch from one biomechanical principle to the other is at about 2–5 kg (Preuschoft et al., 1996). Hence, we used a 5-kg threshold to generate two subsamples, enabling the division of our dataset into the 'smaller' and 'larger' species. We observe that the relationship between the GS and the intrinsic proportions of the manual digits II to V is significant for large species but not for small species (estimate = 7.67, t = 7.08, *p* < 0.0001, and estimate = 0.71, t = 1.11, *p* = 0.28, respectively; see Fig. 4A). Additionally, the relationship between the GS and the intrinsic proportions of the pedal digits II to V is significant for both groups but more pronounced in larger species than in smaller ones (estimate = 6.65, t = 6.31, *p* < 0.0001 and estimate = 1.58, t = 3.37, *p* = 0.0019, respectively; Fig. 4C).

<caption>**Table 2**</caption>

Models fitted with the grasping score as the dependent variable and the phalangeal indices and mean body mass as explicative factors. The model in bold corresponds to the best-fitted model obtained.

<table><thead><tr><th>Fixed-effect model</th><th>AIC</th><th>Residual standard error</th><th>Adjusted r-squared</th></tr></thead><tbody><tr><td>Null</td><td>26.97</td><td>0.08</td><td>0</td></tr><tr><td>H, BM, H:BM</td><td>10.04</td><td>0.04</td><td>0.4</td></tr><tr><td>F, BM, F:BM</td><td>2.01</td><td>0.04</td><td>0.49</td></tr><tr><td>Pol, BM, Pol:BM</td><td>19.7</td><td>0.06</td><td>0.21</td></tr><tr><td>Hal, BM, Hal:BM</td><td>30.3</td><td>0.09</td><td>0.009</td></tr><tr><td>H, Pol, H:Pol</td><td>11.74</td><td>0.04</td><td>0.39</td></tr><tr><td>F, Hal, F:Hal</td><td>2.75</td><td>0.03</td><td>0.58</td></tr><tr><td>H, F, H:F</td><td>3.06</td><td>0.03</td><td>0.54</td></tr><tr><td>Pol, Hal, Pol:Hal</td><td>22.35</td><td>0.06</td><td>0.17</td></tr><tr><td><b>H, F, H:BM, F:BM</b></td><td><b>-2.06<sup>a</sup></b></td><td><b>0.03</b></td><td><b>0.58</b></td></tr><tr><td>H, Pol, H:BM, Pol:BM</td><td>13.92</td><td>0.05</td><td>0.38</td></tr><tr><td>F, Hal, F:BM, Hal:BM</td><td>-0.88</td><td>0.03</td><td>0.59</td></tr><tr><td>Pol, Hal, Pol:BM, Hal:BM</td><td>22.97</td><td>0.08</td><td>0.15</td></tr><tr><td>H, Pol, F, Hal</td><td>11.54</td><td>0.05</td><td>0.37</td></tr></tbody></table>

The interaction between variables is indicated with a colon (:); for example, x1:x2 corresponds to the effect of the interaction between variables x1 and x2.

Abbreviations: BM = body mass; H = mean phalangeal index of the manual digits II to V; F = mean phalangeal index of the pedal digits II to V; Pol = phalangeal index of the pollex; Hal = phalangeal index of the hallux; AIC = Akaike Information Criterion.

<footnote>a Best-fitted model obtained.</footnote>
<figure><img src="image_5.png" /><figcaption>**Figure 2.** Consensus phylogenetic trees (chronogram) obtained from the 10kTrees website (https://10ktrees.nunn-lab.org/; Arnold et al., 2010) representing the phalangeal indices repartition (mapped using the *contMap* function in *phytools* in R) within the studied primate species, for A) the averaged phalangeal index of all manual digits II to V, B) the averaged phalangeal index of all pedal digits II to V, C) the phalangeal index of the first digit of the hand (pollex), and D) the phalangeal index of the first digit of the foot (hallux). The estimates of ancestral states at the nodes are based on the principles of maximum likelihood under a Brownian motion model. (For interpretation of the references to color in this figure, the reader is referred to the Web version of this article.)</figcaption></figure>

## 4. Discussion and conclusions

Our comparative analysis of the intrinsic digit proportions of the hand and foot within nonhuman primates suggests that the elon- gation of the phalanges relatively to the metapods is a morpho- functional adaptation strongly related to the evolutionary history of the primate order and that the variation of this pattern correlates

with their locomotor habits. Overall, our data reveal that the pha- langes of the hand are proportionally longer than the metacarpals compared to the phalanges and metatarsals of the foot in all pri- mate groups. This was previously demonstrated in several strep- sirrhines, tarsiiformes, and a few catarrhines (e.g., Lemelin, 1999; Lemelin and Jungers, 2007; Kirk et al., 2008; Patel and Maiolino, 2016; Young and Heard-Booth, 2016; Druelle et al., 2018), and
<figure><img src="image_6.png" /><figcaption>**Figure 3.** Phylomorphospace showing the relationships between the hand and foot intrinsic proportions of A) phalangeal index of manual digits II to V, B) phalangeal index of the pollex, C) phalangeal index of pedal digits II to V, and D) phalangeal index of the hallux and the mean body mass by species, identified by phylogenetic groups (ancestral-state reconstructions are provided using the *phylomorphospace* function in *phytools* in R and are based on maximum likelihood, according to Revell and Harmon, 2022). Significant relationships are presented with their associated PGLS models' projection and statistics (in gray dotted lines). Level of significance is set as *p* ≤ 0.05, **p** ≤ 0.01, ***p** ≤ 0.001. PGLS = phylogenetic generalized least squares. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)</figcaption></figure>

here, we confirm that this pattern is also shared in platyrrhines and other catarrhines despite their differing phylogenetic relatedness and locomotor specializations. Also, this study highlights that strepsirrhines exhibit longer phalanges relatively to the metapods than haplorrhines (i.e., a higher PI) and that catarrhines, especially cercopithecoids, are the primate species exhibiting the shortest phalanges relative to their metapods (i.e., lowest PIs, Fig. 2).

## 4.1. The differing influence of body mass on the intrinsic proportions of hands and feet

We found that the body mass significantly and negatively correlates with the PIs of the hand (pollex and manual digits II to V), i.e., species with higher body masses tend to exhibit a phalange-to-metacarpal ratio biased toward the metacarpals, but it is not correlated with the foot intrinsic proportions (Fig. 3). This result partially validates our first hypothesis (i.e., a larger species will exhibit lower PIs) but suggests that the hand is more affected than the foot by the weight-induced mechanical stress in the context of locomotor adaptation in primates. Three interpretations of this differing pattern can be proposed: 1) Overall, the phalanges of the hands are elongated compared to the metapods, in contrast to the feet (average PI of the hand in our sample = 1.32 and that of the foot = 0.94). This elongation may render the hand phalanges more subjected to stress induced by weight-bearing during arboreal locomotion, as well as walking. 2) The different postures adopted by the hands (mainly digitigrady) and feet (mainly semiplantigrady and plantigrady) in primates during walking may result in different loading regimes in the two segments (e.g., Patel et al., 2009; Berillon et al., 2010; Zeininger, 2022; Prang, 2024). 3) For a given environment, the branches to be grasped remain the same size, while the absolute sizes of the hand and foot vary between species,

with bigger species possessing longer absolute hands and feet. Smaller animals would thus require longer relative fingers and toes to encircle the same branch that a larger animal would have no difficulty encircling despite a lower PI. Furthermore, it has previously been shown that hand postures change according to the diameter and orientation of the supports when grasping during locomotion in primates of small to medium sizes (strepsirrhines and platyrrhines), while the foot postures appear less variable (see fig. 4 in Toussaint et al., 2020). In this context, it is possible that the hand encounters stronger selective pressures affected by the size of the supports they grasp, whereas the foot is less influenced. More functional explorations are needed to understand this differing pattern between hands and feet.

## 4.2. The grasping score as a quantitative measure of locomotor behaviors and its relationship to the intrinsic proportions of hands and feet

The GS is a quantitative measure (based on the extensive literature on primate positional behaviors) that aims to reflect the overall proportion of digits' use during locomotor behaviors. We found that this score significantly and positively correlates with the PIs of the hand (pollex and manual digits II to V) and with the pedal digits II to V, i.e., species with higher GSs tend to exhibit significantly longer phalanges than the metapods in both hand and foot, but it is not the case with the hallux (Fig. 4). This result partially validates our second hypothesis (i.e., a species having higher GSs will exhibit higher PIs) but shows that the intrinsic proportions of the hallux in extant nonhuman primates is not directly related to arboreal locomotor habits compared to the other digits. Furthermore, the PI of the hallux shows the least variability across our sample compared to the other PIs. The morphology of the foot,
<figure><img src="image_7.png" /><figcaption>**Figure 4.** Phylomorphospace showing the relationships between the computed grasping score and the hand and foot intrinsic proportions of A) phalangeal index of manual digits II to V, B) phalangeal index of hand first digit, C) phalangeal index of pedal digits II to V, and D) phalangeal index of foot first digit, by species, identified by phylogenetic groups (ancestral-states reconstructions are provided using the *phylomorphospace* function in *phytools* in R and are based on maximum likelihood, according to Revell and Harmon, 2022). Significant relationships are presented with their associated PGLS models' projection and statistics (in gray dotted lines). Level of significance is set as \*p* ≤ 0.05, \*\*p* ≤ 0.01, \*\*\*p* ≤ 0.001. In A and C, linear regressions for species grouped by body mass (BM) of under and over 5 kg are also represented, respectively. PGLS = phylogenetic generalized least squares. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)</figcaption></figure>

particularly the possession of a divergent and elongated hallux, constitutes the most ancestral and conserved adaptation in primates (e.g., Gebo, 1985; Bloch and Boyer, 2002; Dagosto, 2007; Sargis et al., 2007). This hallux is specifically adapted to life in the trees, providing a very efficient and powerful pincer grip. Its morphology and abducted postures during arboreal locomotion are highly conserved in primates, unlike the hand whose morphology and postures are more varied from species to species (Sargis et al., 2007; Patel et al., 2015; Toussaint et al., 2020). In this context, we suggest that intrinsic foot proportions are generally less subject to allometry (i.e., body mass) and that the hallux proportion is strongly constrained to ensure the grasping capacity as the primary function of anchoring to arboreal substrates. This is a conserved adaptation for grasping, still shared by all nonhuman primates. However, we observed that the intrinsic proportions of the other toes vary significantly from species to species, in response to locomotor habits, thereby providing a gradient in grasping effectiveness. The evolutionary history of the hand appears to be more complex in the sense that it does not only bear a locomotor function in primates but also is widely involved in manipulative and social behaviors (prey catching, food or object manipulation, grooming ...). Thus, the hands often need to let go of the support to achieve those other functions. Numerous studies have suggested that the functional differentiation of roles between the hand and foot took place quite early in the evolutionary history of primates (e.g., Wood Jones, 1916; Cartmill, 1972; Preuschoft, 2002; Patel et al., 2015), which would explain the greater diversity observed in the manual postures and morphologies exhibited across primate groups (e.g., Pouydebat

et al., 2006; Boyer et al., 2013; Toussaint et al., 2020). We therefore assume that the intrinsic proportions of the hand in primates are more subjected to allometric constraints than those of the foot because it is less subjected to the constraint of supporting the body on the support than the foot (e.g., Kimura, 1992; Demes et al., 1994; Hanna et al., 2006; Granatosky et al., 2016, 2018).

### 4.3. Hand and foot adaptations are functionally different in smaller and larger primates

Our findings largely support our third hypothesis (i.e., hand and foot Pls will not correlate equally with body mass and GS), indicating that the morphofunctional adaptation of the fingers is more constrained by allometry, whereas the morphofunctional adaptation of the toes primarily serves to provide body support and anchorage to arboreal substrates. Our AIC test confirmed that the best model explaining grasping ability links body mass with hand intrinsic proportions, while foot intrinsic proportions remain independent of body mass. When dividing the species sampled into two subgroups, those weighing under 5 kg and those weighing over 5 kg, according to the size threshold defined by Preuschoft et al. (1996), we found that the GS in fact significantly correlates with the intrinsic manual digits II to V proportions only in species weighing over 5 kg, while it correlates with pedal digits II to V proportions in both groups. This suggests that in larger species, the elongation of phalanges relatively to the metapods in both the hand and foot is critical for a more efficient grasping during arboreal locomotion, while relatively shorter phalanges are associated with
more terrestrial habits. In smaller species, hand proportions do not appear to be related to grasping abilities during locomotion.

Unlike other arboreal mammals, primates lack claws that they could use to dig into tree trunks. To effectively push or pull the body forward (propulsive forces) and resist gravity while climbing, clambering, or walking on branches, they must rely on their elon-gated, mobile, and flattened digits that can generate compressive forces by wrapping themselves around arboreal substrates (e.g., Cartmill, 1974, 1985, 1992; Preuschoft, 2004; Lemelin and Schmitt, 2007). But as body mass increases, so does the need of applying higher propulsive forces at the point of contact with the support to counteract gravity, particularly during climbing as well as below-branch locomotion. Indeed, during climbing and suspensory be-haviors (e.g., brachiation and inverted quadrupedalism), it has been shown that the forelimb becomes the primary limb for traction and weight-bearing (Cartmill, 1979, 1985; Johnson et al., 2015; Granatosky et al., 2016). In addition, climbing represents an essential behavior present in all locomotor repertoires of arboreal animals (e.g., Jones, 1916; Hanna et al., 2008). Experimental studies on small- to medium-sized strepsirhines, platyrhines, and macaques have shown that during vertical climbing, the hand ap-plies more tangential forces than the foot and that the foot applies more normal forces than the hand, suggesting that the hand con-tributes more to propulsion during climbing than during horizontal walking, where forces are more equally distributed (e.g., Hanna and Schmitt, 2011; Johnson et al., 2015; Hanna et al., 2017). Therefore, as the body mass increases, so does the need of traction and propul-sive forces specifically generated by the forelimb, and having a higher manual PI may contribute to this increased propulsive ca-pacity by enabling a better grasping on arboreal substrates. Inter-estingly, primates of larger body mass, i.e., catarrhines and especially Hominoida, are those who exhibit locomotor reper-toires that most require the use of the forelimb, such as for vertical climbing and suspensory behaviors like brachiation, which is accompanied with more upright postures (e.g., Isler, 2005; Hunt, 2016; Druelle et al., 2024). Hence, those species are among the ones exhibiting the highest GSs of our dataset. Our results are thus in line with previous theoretical models such as the one formulated by Preuschoft on the effect of body mass on the hind limb and forelimb dominance during vertical clinging and climbing in pri-mates, which predicted apes (the largest primate species) to be forelimb dominated in contrast with smaller species that are hind limb dominated (Preuschoft, 1990, 2002). Moreover, it is interesting to note that primates in general have a relatively lighter muscle mass in relation to their total body mass than other mammals, suggesting specific anatomical adaptations (e.g., tendon length, skeletal architecture, and ligaments properties) favoring hypo-musculature in this group, possibly due to a combination of factors involving early arboreal specialization and relative brain mass in-crease (Muchlinski et al., 2012). These adaptations are unique in mammals, and our results overall suggest that there is a trade-off between limb mechanics, phalangeal relative length, body pos-tures, and substrate preferences, which enabled Hominoida to maintain a high degree of arboreality while increasing their body mass to a certain point.

## 4.4. Limitations and future directions

This study bears a limitation which deserves to be addressed by future studies and which concerns the GS that we computed using the locomotor repertoire extracted from the literature. In the pre-vious ecological and behavioral studies that we used to gather the locomotor repertoire of the species studied, only the orientation of the arboreal substrates (e.g., vertical or horizontal) used during locomotion was commonly specified along with the type of

locomotion quantified. However, it is well established that the diameter and degree of compliance of branches also have a sig-nificant impact on the biomechanics of primates and other arboreal mammals (Young, 2023; Janisch et al., 2024). In effect, horizontal locomotion on thin and flexible branches certainly requires higher autopodial grasping capacity than horizontal locomotion on large branches as it requires the animals to adopt a specific position with their digits, wrapping them completely around the substrate to generate net angular impulses that balance pitching, yawing, and rolling torques around the body's center of mass (Cartmill, 1974, 1985; Lemelin and Schmitt, 2007; Lammers and Gauntner, 2008; Toussaint et al., 2020; Young, 2023). Therefore, the sole information of 'horizontal quadrupedal locomotion' is not sufficient to assess the level of grasping capacity required to accomplish this locomotor mode, and we decided not to include it in our GS computation, possibly introducing a bias in the analysis. Nevertheless, it should be noted that the selective pressures acting on quadrupedalism in extant primates are likely less intense than those on climbing and suspensory locomotion, given the complexity of the arboreal en-vironments in which they forage. As quadrupedalism constitutes one of the most common locomotor modes among mammals, we suggest that future field studies should refine it and more sys-tematically provide the associated substrate diameter when quantifying the positional repertoires of animals, notably by dis-tinguishing more clearly quadrupedal locomotion on small or large horizontal substrates. The same should apply for locomotion on vertical supports, although in this study, we did not exclude the vertical ascent and descent modes because these behaviors already require a certain autopodial grasping capacity to be achieved.

Having built a finer morphofunctional model linking PI, body mass, and locomotor repertoire, this study will enable stronger and quantitative functional inferences of locomotor adaptations in fossil primates that consist of isolated remains of metapodials and pha-langes. Also, it would be interesting for further studies to compare the intrinsic proportions of the hand and foot of primates with those of other arboreal mammals of small to large body mass that have developed convergent arboreal locomotor adaptations or grasping abilities such as some rodents, carnivorans, or marsupials (see Young, 2023 for a review) in order to gain broader insights toward the evolutionary history of autopodial evolution within arboreal mammals.

## Declaration of competing interest

The authors declare no competing interests.

## Acknowledgments

We thank the staff members of the zoological parks of Mulhouse and Besançon for their help in acquisition of radiographs and specifically Alexandrine Vesz, Benjamin Drouet, Mathilde Gluntz, Clément Perret-Thiry, Alizée Teychenée, Denis Michaux, Anaïs Nowakowsky, Irène Vonfeld, Clémence Verguin, Valentin Cassar and Tony Souvignet. We thank Brice Lefaux, the director of the botanical and zoological park of Mulhouse at the time the data were collected, and Margaux Pizzo, the director of Besançon Museum zoological park, for their support. We are very grateful to the staff members of the collections of comparative anatomy of the National Museum of Natural History of Paris, the Natural History Museum of London, and the Field Museum of Natural History of Chicago, respectively, Jacques Cuisin and Céline Bens, Louise Tomsett, and April Isch for providing access to the specimens and support in data acquisition. We are grateful to Gilles Berillon for providing access to the radiographs of the baboon individuals and to Sergio Almécija for providing access to the CT scans of orangutans and gorillas. The
CT scan of gorillas and orangutans were obtained, thanks to the National Science Foundation (BCS 1316947 to Sergio Almcija and William Jungers) and Stony Brook University. We thank Evie Ver-ecke and Peter Aerts for sending us the CT scan of a bonobo specimen (Edmond). This work was supported by the Fyssen Foundation and the Alexander von Humboldt Foundation post-doctoral grants (to S.L.D.T.). Financial support was also provided by the CNRS-INEE International Research Network no. GDRI0870 Bipedal Equilibrium (Resp. Gilles Berillon and François Marchal) and the HNHP (UMR 7194) laboratory (to F.D.). Finally, we thank the editors of *Journal of Human Evolution* and the three reviewers for their suggestions which greatly helped improve this manuscript.

## Author contributions

**Séverine L. D. Toussaint:** Writing – original draft, Visualization, Supervision, Methodology, Investigation, Funding acquisition, Data curation, Conceptualization. **Vincent D'Amato:** Investigation, Formal analysis. **Joanna Desmidt:** Investigation, Formal analysis. **Mélanie Berthet:** Data curation. **Benoît Quintard:** Data curation. **François Druelle:** Writing – original draft, Visualization, Validation, Supervision, Methodology, Investigation, Formal analysis, Data curation, Conceptualization.

## Supplementary Online Material

Supplementary Online Material related to this article can be found at https://doi.org/10.1016/j.jhevol.2025.103679.

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