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Dossier spécial - BipédieS chez les Primates : de la philosophie au comportement

Knuckle-walking and behavioural flexibility in great apes

La marche sur l’articulation des phalanges des mains et la flexibilité comportementale chez les grands singes
Emily LR Tarrega-Saunders, Charlotte King, Alice M Roberts et Susannah KS Thorpe

Résumés

Les différences cinématiques entre les marches sur l’articulation des phalanges des mains des chimpanzés et des gorilles ont fourni des preuves qui soutiennent la théorie selon laquelle cette marche a évolué indépendamment dans les lignées des Pan et des Gorilla et ne vient pas d’un ancêtre commun. Cette théorie a été utilisée pour contester l’idée que la bipédie des hominines a évolué à partir de la marche sur les phalanges. Le fait que le poignet soit étendu chez les chimpanzés pendant la marche sur les phalanges, contrairement aux gorilles qui ont une posture du poignet en forme de colonne pendant cette marche, a été associé au mode de vie plus arboricole des chimpanzés, et ces différences sont soi-disant contraintes par des différences importantes de la morphologie du carpe. Cependant, des données cinématiques plus récentes remettent en question la présence de deux types distincts de marche sur les phalanges chez les Pan et les Gorilla. Il devient également évident que les primates font preuve d'une grande flexibilité dans leur écologie locomotrice pour s'adapter aux conditions de leur habitat, indiquant que l'attribution d'une stéréotypie locomotrice à chaque espèce est inappropriée. De plus, le potentiel de plasticité au cours du développement anatomique représente un défi pour les prédictions évolutionnaires basées sur les relations étroites entre forme du squelette et fonction locomotrice. Sachant que les preuves rassemblées aujourd'hui montrent que les gorilles sont arboricoles de manière substantielle, cette étude explore la cinématique du poignet pendant la marche sur les phalanges de chimpanzés et de gorilles élevés en captivité, à la fois durant leur marche dans les arbres et sur la terre ferme, afin d’étudier l’hypothèse selon laquelle les différences cinématiques précédemment signalées sont contraintes par la phylogénie plutôt qu'une simple conséquence de l’environnement. Nous avons constaté que lorsque le comportement de marche sur les phalanges des gorilles est considéré dans un contexte arboricole, les gorilles présentent une posture des poignets plus étendue que les chimpanzés, et sont donc capables des mêmes réponses cinématiques aux supports arboricoles. Nous suggérons que la marche sur les phalanges incarne un héritage commun de flexibilité comportementale chez les chimpanzés et les gorilles, plutôt qu'un héritage commun de la marche sur les phalanges elle-même ou qu’une évolution indépendante de cette marche en réponse à différentes pressions environnementales. Nous suggérons de prendre en compte l'ensemble des contextes environnementaux d'une espèce, ainsi que l'influence potentielle de la plasticité développementale sur l'anatomie locomotrice lors des futures études sur la locomotion des hominoïdes afin de tirer des conclusions plus solides sur l'évolution du comportement locomoteur.

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Notes de la rédaction

Received 17/06/2021, accepted after revisions 16/12/2021, published online 28/02/2022 in the context of the special issue "BipedalismS in primates" (Varia 2021).

A translated version, in french, is available online.

Une version traduite, en français, est disponible en ligne.

Texte intégral

1 Introduction

1In order to understand the developmental and evolutionary drivers behind an organism’s behaviour, we must consider the links between morphological form and behavioural function, as well as their ecological contexts (known as the ecomorphological approach; Karr & James, 1975; Wainwright, 1991). When reconstructing the evolution of primate locomotion, ecology is a particularly important piece of the puzzle: a primate must be able to access food, escape predators and compete for mates, and its ability to move around its complex, three-dimensional environment directly affects the success of all these strategies (Cant, 1992; Saunders et al. 2017). The locomotor behaviour that a primate uses to negotiate its environment is not only quantified by the properties of the specific behaviours (e.g., quadrupedal walking or vertical climbing) that it employs on a regular basis, but also by its overall locomotor performance capacity. This includes behaviours that the primate can use when pushed to its performance limits, such as leaping over a large gap in the canopy or changing direction quickly on a narrow branch to escape a predator (Walker, 1979; Crompton & Sellers, 2007). While these behaviours may not be needed often, they can save the primate’s life, and will therefore also be under selective pressures (e.g. Garland & Losos, 1994).

2Locomotor efficiency and performance capacity are facilitated by an animal’s morphology, in combination with the physical structure of its habitat (Garland, 1994; Payne et al. 2006a, 2006b; Hogervorst & Vereecke, 2014). In fossil species, while some ecological data may be available, most information about overall morphology and locomotor behaviour must be inferred from skeletal morphology alone. Reconstruction of locomotor behaviour in fossil primates therefore requires reliable interpretations of skeletal morphology, which in turn require an understanding of the relationship between skeletal anatomy and behaviour in extant species (Crompton et al. 2008, 2010). This includes the way that locomotor behaviour is reflected in the skeleton, as well as the overall range of locomotor performance capacity that can be accommodated within certain morphological constraints. The ecological contexts of locomotion in extant species can be used to understand the evolutionary drivers behind certain behaviours, and, alongside paleoenvironmental data, can be used to test the ecological validity of locomotor reconstructions in extinct primates (Lovejoy, 1988; Benefit & McCrossin, 1995; Pickering et al. 2004; Pickford, 2006; White et al. 2009; Senut et al. 2018). Thus comparative data on the expression of functional morphology and locomotor behaviour across extant primates, as well as detailed information about the animals’ locomotor responses to different environments (such as different types of terrain or canopy structure; Cartmill, 1974; Stevens, 2008; Myatt & Thorpe, 2011), are vital to ecological interpretations of locomotor behaviour in fossil specimens.

3Many interpretations of locomotion in fossil hominoids are based on skeletal features that are present in a similar form in extant apes, such as inferring erect bipedalism from modern human-like morphology (e.g. Pickford et al. 2002; White, 2006; Crompton et al. 2008), or knuckle-walking from skeletal similarities with African apes (e.g. Richmond & Strait, 2000). However, while interspecific similarities or differences in certain morphological elements are likely to have some influence on variation in locomotor function, the assumption that they are direct reflections of locomotor capability oversimplifies the complex array of mechanisms that underpin behaviour and performance. Firstly, even if an animal’s morphology appears well adapted to a specific locomotor regime, it may still accommodate a wide range of other, mechanically disparate, behaviours. Primates have exceptionally flexible locomotor repertoires; for example, while we associate bipedalism with humans and require fossil specimens to exhibit morphological evidence for bipedalism to be included in the hominin clade (Crompton et al. 2008), all other extant apes and many monkey and prosimian species are capable of bipedal movement (Hewes, 1961; Fleagle, 1976; Thorpe & Crompton, 2006; Berillon et al. 2010; Hunt, 2016). Secondly, it is difficult to know whether an extinct animal’s morphological adaptations represent inherited anatomical features that were genetically-constrained, or are features that developed throughout postnatal development in response to behaviour, and were therefore the result of plasticity. Plasticity in mammalian muscle and bone is a well-documented phenomenon (Pilbeam, 2004; Barak et al. 2011; Shaw & Ryan, 2012), which may itself be under partial genetic control (Neufuss et al. 2014), but it has not often been considered in evolutionary reconstructions of hominoid locomotor behaviour. Observed types of phenotypic accommodation in the skeleton include alterations to trabecular orientation at joints in response to changes in loading direction (Barak et al. 2011), increased thickness of bone in response to repeated high forces exerted by muscles (Shaw & Stock, 2009), as well as larger-scale reorganisations of bone shape that facilitate locomotion after congenital limb defects (Slijper, 1942a, 1942b; West-Eberhard, 2003). Furthermore, plastic responses in soft tissue morphology to changes in locomotion can be accommodated without corresponding skeletal changes (Venkatamaran et al. 2013), which loosens the generally perceived tight link between skeletal form and behavioural function upon which locomotor reconstructions are based (Crompton et al. 2008, 2010). Therefore, while it may be possible to hypothesise that certain skeletal features in fossil specimens (such as trabecular orientation; Barak et al. 2011) resulted from plasticity, the potential for plasticity across the musculoskeletal system in general presents considerable challenges to phylogenetic interpretations of morphology and locomotor behaviour.

4As well as allowing individuals to adapt to external conditions within their lifetimes, morphological plasticity may also be an important driver of longer-term evolutionary change (West-Eberhard, 2003). For example, it may be an important precursor to speciation between geographically separated populations due to its role in producing morphological novelties, which spread rapidly after appearing and are eventually retained through genetic accommodation (West-Eberhard, 2005). A study of orangutans from two separated populations reported that differences in various aspects of their behavioural ecology were much more influenced by environmental differences than genetic variation (Krützen et al. 2011). The extent to which their morphologies differed is unknown, but if the two habitats elicited different locomotor responses, habitat variation may have had a stronger influence on their locomotor anatomy than genetic drift. Thus the influences of plastic responses to environmental variables on the evolution of morphology and behaviour, at both species- and individual-level, should not be overlooked.

5Anatomical plasticity increases the complexity of the relationships between morphology, behaviour and habitat, presenting challenges to accurate reconstructions of extinct hominoid locomotion. One means of combatting this problem is to ensure that data on the form-function relationships in extant species are highly specific. Kinematics provides detailed characteristics of locomotor behaviour that can be associated with specific habitat parameters. For example, the angles of joint rotation in an ape walking along a branch can be interpreted in relation to specific structural properties of the branch (Myatt & Thorpe, 2011; Schoonaert et al. 2016). This brings ecology into form-function comparisons in a more meaningful way than through using overly broad categorisations of habitat use (e.g. whether the animal is terrestrial or arboreal). Kinematic analyses that link form, function and habitat in a specific way facilitate more accurate interpretations of specific fossil morphologies. The approach also allows biomechanical quantification of the locomotor variation that exists within a species and which can therefore be accommodated by a particular morphology (Crompton et al. 2003; Schmitt, 2003). Finally, it can identify mechanical similarity between different types of locomotion, or between analogous locomotor behaviours in different species or individuals to shed light on locomotor evolution (e.g. Fleagle et al. 1981; Gebo, 1996). Mechanical similarity in a particular locomotor behaviour between two species has been used to indicate that the behaviour was inherited by both species from their common ancestor, rather than being a result of convergent evolution (Alexander, 1991; Crompton et al. 2003).

6One of the most significant examples of kinematics being used to change a major theory of hominoid evolution is the evidence used to refute the ‘knuckle-walking hypothesis’ for the evolution of hominin bipedalism (the idea that pre-bipedal hominins used the quadrupedal knuckle-walking gait employed by modern African apes; Washburn, 1967; Tuttle, 1974; Richmond et al. 2001). More recent behavioural, morphological and environmental evidence suggests that knuckle-walking is not the result of a single evolutionary development in an African ape common ancestor, and was therefore unlikely to be present in the hominin clade. Morphological features supposedly related to knuckle-walking (such as ridges on the capitate and hamate bones) are absent from the hominin fossil record, yet are present in non-knuckle-walking monkeys (Kivell & Schmitt, 2009). There are also ontogenetic and postural differences between the knuckle-walking behaviour of chimpanzees and gorillas (Inouye, 1994). Here, a crucial piece of kinematic evidence is the biomechanical difference between the wrist postures employed by the two genera during knuckle-walking: chimpanzees have been found to use a more extended wrist during the stance phase of knuckle-walking, whereas gorillas employ a more columnar posture (Figure 1; Inouye, 1994; Kivell & Schmitt, 2009). This was attributed to chimpanzees’ more frequent use of arboreal supports compared with gorillas, and supposedly constrained by skeletal differences, including increased dorsal concavity of the scaphoid and waisting of the capitate. These morphological adaptations were hypothesised to allow chimpanzees to support a more extended wrist posture during weight-bearing compared with gorillas (Kivell & Schmitt, 2009; Figure 1). Scaphoid concavity was also found in non-knuckle-walking monkeys, which may be associated with wrist extension during palmigrade quadrupedalism (Kivell & Schmitt, 2009). However, assumptions that these skeletal differences reflect fundamental differences in locomotor capability should be treated with caution, given the potential for soft tissue plasticity to facilitate behavioural capacity without observable skeletal change (Venkataraman et al. 2013).

Figure 1

Figure 1

A comparison of a) the extended wrist posture in chimpanzees and b) the neutral, columnar posture in gorillas during knuckle-walking. Adapted from Kivell & Schmitt (2009).

7This mechanical difference in wrist posture between chimpanzees and gorillas was used to advocate independent evolution, rather than common inheritance, of knuckle-walking in the Pan and Gorilla lineages (Dainton & Macho, 1999; Kivell & Schmitt, 2009). Independent evolution of knuckle-walking in chimpanzees and gorillas is based on the idea that their shared adaptations are related to other shared behaviours (perhaps vertical climbing, which is a crucial locomotor skill for accessing arboreal resources), and knuckle-walking developed after the evolutionary split between the two genera as the most efficient means of terrestrial locomotion for an animal with those shared adaptations (Crompton et al. 2010). Increased arboreality in chimpanzees caused a difference in selection pressure between the two genera, and chimpanzees were required to develop anatomical and behavioural adaptations to moving on a wider range of supports (Kivell & Schmitt, 2009; Crompton et al. 2010). However, in a separate kinematic study, Finestone et al. (2018) did not find significant differences in wrist excursion between captive chimpanzees and gorillas, casting doubt on the presence of two distinct forms of knuckle-walking in the two genera. Yet the extent to which chimpanzees and gorillas differ in their knuckle-walking responses to different environments remains unknown, as the findings of both Kivell & Schmitt (2009) and Finestone et al. (2018) were based on terrestrial locomotion only in gorillas. It is notable that Western lowland gorillas can be highly arboreal (Remis, 1999), and are thought to be more similar in their canopy locomotion to orangutans, who are almost exclusively arboreal, than to chimpanzees (Thorpe & Crompton, 2006). Gorilla populations also differ extensively in their arboreality based on habitat features such as canopy cover and resource availability (Crompton, 2016). Kinematic evidence for independent evolution of knuckle-walking has therefore missed a core component of gorilla locomotor ecology, and data on gorilla locomotion in more environmental contexts may reveal greater locomotor variation.

8In this paper, we ask whether the kinematic differences in wrist posture between chimpanzees and gorillas used by Kivell & Schmitt (2009) to advocate independent evolution of knuckle-walking are present when arboreal locomotion in gorillas is also considered. We will investigate wrist kinematics of both terrestrial and off-ground knuckle-walking in captive chimpanzees and gorillas, and assess the responses of both species to different types of weight-bearing support. This will be used to predict the extent to which knuckle-walking function in the wrist is anatomically and phylogenetically constrained in the African apes. We will also use the results to consider whether variation in knuckle-walking mechanics is a response to environmental context, and whether anatomical or behavioural plasticity may be more influential in knuckle-walking development and evolution than previously thought.

2 Methods

9Seven adult chimpanzees (Pan troglodytes; two males, five females) and six adult gorillas (Gorilla gorilla gorilla; four males, two females) were studied in their captive environments at Paignton Zoo (male gorillas) and Twycross Zoo (chimpanzees and female gorillas), UK (see Table 1 for subject details). All study subjects were filmed from the public viewing area, and in compliance with the zoos’ ethical guidelines all individuals were untrained, unmarked and had no physical contact with observers. Standard video cameras (Panasonic HC-V520, 30 fps) were positioned perpendicular to frequently-used routes through the enclosures. Sequences of knuckle-walking were selected from footage of individuals walking at a steady speed in a direction perpendicular to the camera, and in which the subject’s stride pattern appeared unconstrained by the environment (walking along a row of equally-spaced supports, for example, would dictate an individual’s step length and therefore their locomotor mechanics). Following the method of Watson et al. (2009), sequences in which the subject’s locomotion was deemed to be within 10° of perpendicular, and within a 10° vertical filming angle, were selected, meaning that out-of-plane angular corrections did not need to be applied to measurements (Stevens et al. 2006). Eleven sequences were selected for chimpanzees (3 arboreal and 8 terrestrial) and 23 for gorillas (10 arboreal and 13 terrestrial). These were calibrated using known body measurements or measurements on the weight-bearing supports.

Table 1

Table 1

Subject details

10Sequences were manually digitised frame-by-frame using Kinovea (v0.8.15, www.kinovea.org) in order to calculate the wrist flexion/extension angle of the forelimb closest to the camera. Following the method of Isler (2005), angles were measured using digitisation of segment long axes. The maximum and minimum angles observed during the stance phase of each sequence were used for statistical analysis. For each sequence, we also recorded whether the individual was arboreal (used for all off-ground supports) or terrestrial, and used discreet categories to record orientation angle (0° [horizontal]; U-shaped; <45°; 45≤90°) and diameter (>10cm; 10≤19cm; 20≤29cm; >30cm) of the weight-bearing support. Support compliance was not included as chimpanzees were only observed on rigid supports (e.g. the ground or elevated logs), and gorillas were observed on either rigid or super-flexible supports (e.g. horizontally suspended straps). Neither enclosure contained supports that elicited branch-like oscillation. The enclosures do not offer the diversity of support choice that exists in the wild, which will constrain the captive individuals’ locomotor behaviour. However, the captive environments provide a useful means of investigating wrist kinematics on off-ground supports in both species, providing this limitation is considered during interpretation of the results.

11The effects of arboreality, support angle and support diameter on wrist extension were tested using Multiple Regression models with Bonferroni correction for maximum and minimum wrist angle during the forelimb stance phase. Significant differences in wrist angles between chimpanzees and gorillas were identified using Independent Sample T Tests. All statistical analyses were completed using R (v4.0.5).

3 Results

12Wrist extension was significantly higher in gorillas than in chimpanzees (t [32] = -2.51, p = 0.017; Figure 2). The average maximum wrist angle was 182° in chimpanzees and 189° in gorillas, and average minimum wrist angle was 123° in chimpanzees and 134° in gorillas. Both of these parameters varied more substantially among gorilla sequences than among chimpanzee sequences. There was no significant difference in wrist extension between the two species when only terrestrial knuckle-walking sequences were considered, as this reduced the maximum wrist angles observed in gorillas (Figure 2).

Figure 2

Figure 2

Maximum wrist extension observed in chimpanzees (n = 11) and gorillas (n = 23). Boxplots represent the median, interquartile range and total range of the data. Note that the y axis begins at 140°.

13Multiple Regression analysis revealed that maximum wrist extension was also significantly higher during arboreal than during terrestrial knuckle-walking in both chimpanzees (R2 = 0.596, F [1,9] = 15.78, t [Support: ground] = -3.97, p = 0.003) and gorillas (R2 = 0.336, F [2,20] = 6.55, t [Support: ground] = -3.58, p = 0.006). Minimum wrist extension angles in each sequence were also generally highest among arboreal knuckle-walking in both species, although not significantly so. Wrist kinematics were not individually associated with support angle or diameter. However, while support compliance could not be tested, it is notable that the sequences that contained the most extended wrist postures in gorillas were observed on super-flexible supports (suspended straps).

4 Discussion

14While the weight-bearing supports used by the apes in this study did not emulate the branch-like compliance of their wild environment, our results support previous findings that wrist extension is associated with arboreal, rather than terrestrial, knuckle-walking. However, the results do not support a fundamental phylogenetic difference in wrist performance between chimpanzees and gorillas, and the increased wrist extension in gorillas compared with chimpanzees observed in this captive setting is the direct opposite of the interspecific difference in wild individuals found by Kivell & Schmitt (2009). Those authors associated differences in carpal morphology between chimpanzees and gorillas with reduced stability of the radiocarpal joint in gorillas, allowing a greater range of wrist extension during weight-bearing in chimpanzees but necessitating more columnar loading in gorillas. Yet, in our study subjects, we find that gorillas employ not only more wrist extension than chimpanzees, but levels of extension that exceed what could be described as columnar loading (up to 210°; 30° more than a columnar position of 180°). Gorillas, therefore, are not so constrained in their wrist use during locomotion by carpal morphology as previously thought.

15Positional behaviour is ultimately a response to an animal’s environment, and most directly to the distribution and functional properties of weight-bearing supports (Saunders et al. 2017). Therefore, fundamental interspecific differences can only be identified when the species being compared are exposed to a similar locomotor substrate, and one gait can only be fully quantified in a species when all environmental contexts of that gait are considered. The zoo enclosures used in this study do not cover this range of environmental contexts, but nevertheless they provide an opportunity for a simplified terrestrial/arboreal comparison in both species. The increased wrist extension in gorillas compared with chimpanzees in this study is likely explained by differences in support availability between the enclosures of the two species. Gorillas were observed walking on off-ground supports much more frequently than chimpanzees, as well as on more compliant supports, and, similar to the findings of Finestone et al. (2018), there were no differences between the two species in their terrestrial knuckle-walking. It is notable that the most extended wrist postures observed in gorillas were on flexible substrates, supporting further the link between wrist extension and arboreal locomotion. Differences in support availability between the enclosures in this study and the habitats of wild individuals observed by Inouye (1994) will also have had considerable influence on the locomotor behaviours reported in those studies, and we agree with previous authors’ suggestions that differences in locomotor substrate use within their habitats have led wild chimpanzees and gorillas to differ in the types of knuckle-walking that they habitually employ. However, this does not affect an important finding: that gorillas are capable of the same kinematic response to arboreal supports as chimpanzees, and that interspecific differences are more likely to be a result of substrate rather than phylogenetic constraint. Wrist extension is, of course, only one small part of the biomechanical profile of knuckle-walking, and other important differences in hand posture have been observed in wild individuals. These include increased use of the fifth digit for weight-bearing in gorillas compared with chimpanzees (Inouye, 1994), and a more medial-facing palm in chimpanzees (Tuttle, 1967; Inouye, 1994; Matarazzo, 2013; Thompson, 2020). While these differences may support independent evolution of knuckle-walking in Pan and Gorilla, like wrist extension they may also be products of substrate use and not reflections of fundamental interspecific constraints in locomotor ability.

16This study shows that chimpanzees and gorillas may be capable of similar locomotor flexibility; not that they merely share the same, stereotyped gait mechanics. Therefore, we do not suggest that knuckle-walking was inherited by both Pan and Gorilla lineages from their last common ancestor; but nor do we support the idea that it reflects two different behaviours that evolved independently. Rather, we propose a different scenario: that chimpanzees and gorillas inherited a shared propensity for morphological and behavioural flexibility that allowed knuckle-walking to develop.

17As Crompton et al. (2010) suggest, perhaps knuckle-walking represents the most efficient means of terrestrial locomotion for animals that are fundamentally adapted to vertical climbing. Plasticity in soft tissue morphology may mean that skeletal differences in the wrist between the two genera are not related to locomotor capacity (although they may reflect adaptation to locomotion on different types of frequently-used substrate). Currently we do not know the performance capacity that can be accommodated within particular morphological constraints. Therefore when interpreting fossil remains, while we can use an animal’s skeletal anatomy to predict the type of locomotion the animal is most adapted to, we cannot reliably predict its full range of locomotor abilities.

18It is also becoming apparent that the accommodation of behavioural flexibility without morphological changes may be equally as important as morphological plasticity in primate locomotion. Evidence that gorillas are able to respond to arboreal supports in a manner kinematically similar to chimpanzees, alongside observations of the arboreal locomotion of wild lowland and mountain gorillas (Remis, 1999; Thorpe & Crompton 2006; Neufuss et al. 2018), reveal that gorillas may have more flexible locomotor repertoires than is often assumed. Mountain gorillas, which are traditionally thought to be particularly constrained in their locomotor abilities (e.g. Reynolds, 1965), also employ a variety of hand postures during quadrupedal locomotion, including palmigrade- and fist-walking as well as knuckle-walking, in response to substrate properties (Thompson et al. 2018). Modern humans are another example of a hominoid that is generally perceived to be constrained in both locomotor morphology and locomotor capacity (Latimer et al. 1987; Lovejoy, 1988; Latimer, 1991). However, the range of modern human behaviours that have been observed across the globe reveals substantial locomotor diversity, including a variety of tree-climbing strategies (Kraft et al. 2014), as well as the behaviours of groups such as parkour athletes, gymnasts and rock-climbers (Halsey et al. 2016). Many of the locomotor behaviours used by these groups of people are arguably outside of the range of locomotor performance supposedly accommodated by human skeletal anatomy. Thus, the entire hominoid clade, including humans, may be characterised by a propensity for substantial locomotor flexibility, as a strategy for safe and efficient negotiation of the complex arboreal environment (Saunders et al. 2017).

19This study represents only a small snapshot of the overall importance of considering the full range of habitats employed by a species when quantifying its locomotor behaviour. We have considered the impact of one additional environment (off-ground supports) on the kinematic variation within one gait (knuckle-walking), but have still revealed previously undocumented locomotor responses that challenge simplistic evolutionary interpretations of locomotion. The idea that interspecific differences in locomotion may only reflect environmental differences, rather than phylogenetically constrained differences in locomotor performance, will have implications for evolutionary reconstructions of other types of locomotion. Perhaps many primate locomotor behaviours are not themselves phylogenetically conserved, but a result of behavioural responses to similar environments in animals who share phylogenetically conserved morphology, and/or an inherited capacity for morphological and behavioural plasticity. In order to further our understanding of locomotor evolution in hominoids, a fresh look at the locomotion of living apes, which considers their full range of environmental contexts, is necessary. Kinematics provides specific information on locomotor responses to environmental variables, but is not always feasible in wild habitats. However, as in this study, specific environmental variables can be replicated in captive settings, from which biomechanical data can be easily collected. These locomotor ecology datasets would provide more detailed information with which morphology can be compared, and allow more reliable interpretations of the fossil record. Together, these approaches would enable a deeper understanding of the evolutionary drivers behind hominoid locomotion.

Acknowledgements

20We thank James Ashley for contributing to data collection, and Twycross Zoo and Paignton Zoo for accommodating the research. We thank two anonymous reviewers and the Associate Editor for their valuable comments on the manuscript. We also thank the University of Birmingham for funding the PhD in which this research project was undertaken.

Conflict of Interest

21The authors declare that they have no competing interests.

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    Ce document est une traduction en français de l'article original rédigé en anglais. Cette traduction a été réalisée par l'INIST CNRS (INstitut de l'Information Scientifique et Technique).

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Table des illustrations

Titre Figure 1
Légende A comparison of a) the extended wrist posture in chimpanzees and b) the neutral, columnar posture in gorillas during knuckle-walking. Adapted from Kivell & Schmitt (2009).
URL http://journals.openedition.org/primatologie/docannexe/image/10855/img-1.png
Fichier image/png, 100k
Titre Table 1
Légende Subject details
URL http://journals.openedition.org/primatologie/docannexe/image/10855/img-2.jpg
Fichier image/jpeg, 332k
Titre Figure 2
Légende Maximum wrist extension observed in chimpanzees (n = 11) and gorillas (n = 23). Boxplots represent the median, interquartile range and total range of the data. Note that the y axis begins at 140°.
URL http://journals.openedition.org/primatologie/docannexe/image/10855/img-3.png
Fichier image/png, 255k
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Référence électronique

Emily LR Tarrega-Saunders, Charlotte King, Alice M Roberts et Susannah KS Thorpe, « Knuckle-walking and behavioural flexibility in great apes »Revue de primatologie [En ligne], 12 | 2021, mis en ligne le 28 février 2022, consulté le 05 juin 2023. URL : http://journals.openedition.org/primatologie/10855 ; DOI : https://doi.org/10.4000/primatologie.10855

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Auteurs

Emily LR Tarrega-Saunders

School of Biosciences, University of Birmingham, Birmingham, B15 2TT, UK
Email address: elrsaunders@gmail.com

Charlotte King

School of Biosciences, University of Birmingham, Birmingham, B15 2TT, UK
Email address: CXK984@bham.ac.uk

Alice M Roberts

School of Biosciences, University of Birmingham, Birmingham, B15 2TT, UK
Email address: alice@alice-roberts.co.uk

Susannah KS Thorpe

School of Biosciences, University of Birmingham, Birmingham, B15 2TT, UK
Corresponding author: S.K.Thorpe@bham.ac.uk

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