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Keywords:

  • ecomorphology;
  • geometric morphometrics;
  • grasping;
  • musteloids

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information

The ability to grasp and manipulate is often considered a hallmark of hominins and associated with the evolution of their bipedal locomotion and tool use. Yet, many other mammals use their forelimbs to grasp and manipulate objects. Previous investigations have suggested that grasping may be derived from digging behaviour, arboreal locomotion or hunting behaviour. Here, we test the arboreal origin of grasping and investigate whether an arboreal lifestyle could confer a greater grasping ability in musteloid carnivorans. Moreover, we investigate the morphological adaptations related to grasping and the differences between arboreal species with different grasping abilities. We predict that if grasping is derived from an arboreal lifestyle, then the anatomical specializations of the forelimb for arboreality must be similar to those involved in grasping. We further predict that arboreal species with a well-developed manipulation ability will have articulations that facilitate radio-ulnar rotation. We use ancestral character state reconstructions of lifestyle and grasping ability to understand the evolution of both traits. Finally, we use a surface sliding semi-landmark approach capable of quantifying the articulations in their full complexity. Our results largely confirm our predictions, demonstrating that musteloids with greater grasping skills differ markedly from others in the shape of their forelimb bones. These analyses further suggest that the evolution of an arboreal lifestyle likely preceded the development of enhanced grasping ability.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information

The use of the forelimbs in grasping is common to a large number of vertebrates ranging from amphibians to mammals (Grzimek, 1990; Iwaniuk & Whishaw, 2000; Sustaita et al., 2013). Although the ability to grab food, to hold it and to manipulate it has been observed in a variety of aquatic and arboreal frogs (Gray et al., 1997; Manzano et al., 2008), this ability is often thought to be an essentially mammalian trait (Ivanco et al., 1996; Iwaniuk et al., 1999, 2000; Endo et al., 2007; Sacrey et al., 2009). In eutherians, behaviours associated with grasping are widespread and have been observed in species belonging at least to six orders (Pilosa, Chiroptera, Rodentia, Carnivora, Scandentia and Primates). Previous investigations of prehension have suggested that the ability to grasp with the forelimbs might be derived from locomotor behaviours such as digging (Brácha et al., 1990), arboreal thin-branch climbing (Grillner & Wallén, 1985; Godinot, 1991, 2007; Antón et al., 2006; Salesa et al., 2006; Manzano et al., 2008; Reghem et al., 2012) or the need to manipulate prey (Gray et al., 1997; Iwaniuk & Whishaw, 2000). In spite of data accumulated on different taxa, particularly within Primates (Christel, 1993; Byrne et al., 2001; Corp & Byrne, 2002; Pouydebat et al., 2008, 2009, 2011; Crast et al., 2009; Reghem et al., 2011), the evolution of grasping behaviour has received relatively little attention, and our understanding of this behaviour and the underlying anatomical traits facilitating its evolution remains consequently limited (see Sustaita et al., 2013).

The morphology of the forelimb has often been suggested to be a good indicator of locomotor ecology (Ewer, 1973; Gonyea, 1978; Argot, 2001; Andersson, 2003, 2004, 2005; Flores & Díaz, 2009; Halenar, 2011) with previous studies mainly focusing on the relationship between elbow morphology (Andersson, 2003, 2004; Schutz & Guralnick, 2007; Halenar, 2011) and locomotor mode. Furthermore, in these studies, the focus has been mainly on the humerus, whereas the other long bones of the forelimb (ulna and radius) remain largely unstudied. Yet, all of these elements are crucial to ensure effective movement of the forelimb, especially in tasks requiring fine motor control such as arboreal locomotion or grasping. Thus, a better understanding of the anatomy of these elements in taxa specialized for different locomotor behaviours, in comparison with the morphology observed in grasping taxa, may shed light on the ecological context and the evolutionary origins of grasping ability.

To investigate the evolution of morphological adaptations of the forelimb related to grasping, we here present a quantitative morphological analysis of the three long bones of the forelimb in musteloid carnivorans. The Musteloidea (Mephitidae, Ailuridae, Procyonidae and Mustelidae) are a good model system for this kind of study for a number of reasons. First, they are ecologically diverse, containing a remarkable diversity of lifestyles that ranges from arboreal species, such as the kinkajou and the red panda, to aquatic species, such as the sea otter. Second, the diversity of lifestyles observed in each clade suggests that they have colonized the same type of habitats and acquired the behavioural traits of interest independently. Among the musteloids, three families contain species able to grasp and manipulate objects, providing a unique opportunity to examine the variation in forelimb shape in a group of closely related species differing in their lifestyle and grasping ability. Third, the phylogenetic relationships among musteloids are well resolved (Sato et al., 2009, 2012; Eizirik et al., 2010): the mustelids (weasels, badgers, otters and their relatives) and the procyonids (coatis, raccoons, the kinkajous and their relatives) are sister taxa, whereas the ailurids (which is represented by the unique living representative, the red panda) and the mephitids (skunks) form successive sister lineages to this clade (Fig. 1).

image

Figure 1. The phylogenetic relationships of the musteloid species used in this study, derived from Slater et al. (2012). The time scale is in million years.

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In this study, we use 3D geometric morphometric methods to quantitatively compare the anatomy of the long bones of the forelimb in musteloids with different lifestyles and grasping ability. Within each lifestyle (arboreal, semi-arboreal and terrestrial), we compare the forelimb morphology of species with different grasping ability (well developed, intermediately developed and poorly developed) where possible. This allows us to (i) test whether arboreal lifestyle precedes grasping ability, (ii) investigate the morphological adaptations related to grasping ability and the differences and/or similarities between arboreal species with different grasping abilities. We predict that if grasping is derived from an arboreal lifestyle as has been suggested previously, then the anatomical specializations of the forelimb for an arboreal lifestyle must be similar to those involved in grasping. Moreover, we predict that arboreal species with a well-developed grasping ability will have articulations that will provide an increase in the range of pronation and supination to facilitate rotation at the wrist and thus allowing more complex movements (Gray et al., 1997).

Materials and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information

Sample

Long bones of the forelimb (humerus, ulna and radius) of 49 individuals belonging to 8 species of procyonids, 1 species of ailurid, 1 of mephitid and 8 of mustelids were used in our study. The number of specimens of each species ranged from 1 to 7 individuals per species (Table 1). All specimens were adults and predominantly of wild-caught origin. Equal numbers of males and females were included where possible. Forelimb bones were obtained from the following collections: Mammifères et Oiseaux, Muséum National d'Histoire Naturelle, Paris, France; the Naturhistorisches Museum, Basel, Switzerland; the Harvard Museum of Comparative Zoology, Cambridge, Massachusetts, and the Smithsonian National Museum of Natural History, Washington, District of Columbia, USA. See Data S1 for a list of the specimens used in the analyses. All the bones of the forelimb were digitized using a Breuckmann 3D surface scanner at the Muséum National d'Histoire Naturelle, Paris (white light fringe StereoSCAN3D model with a camera resolution of 1.4 megapixels).

Table 1. Details of specimens used in analyses with species name, common name, number of individuals included (N), family, lifestyle and grasping ability
SpeciesCommon name N FamilyLifestyleGrasping ability
Spilogale putorius Eastern spotted skunk1MephitidaeTerrestrialPoorly developed
Ailurus fulgens Red panda5AiluridaeArborealIntermediately developed
Eira barbara Tayra1MustelidaeSemi-arborealPoorly developed
Ictonyx striatus Zorilla1MustelidaeTerrestrialPoorly developed
Martes foina Stone marten2MustelidaeSemi-arborealPoorly developed
Martes martes Pine marten2MustelidaeSemi-arborealPoorly developed
Mustela lutreola European mink2MustelidaeTerrestrialPoorly developed
Mustela putorius European polecat2MustelidaeTerrestrialPoorly developed
Neovison vison American mink1MustelidaeTerrestrialPoorly developed
Vormela peregusna Marbled polecat2MustelidaeTerrestrialPoorly developed
Potos flavus Kinkajou4ProcyonidaeArborealWell developed
Procyon cancrivorus Crab-eating raccoon2ProcyonidaeSemi-arborealIntermediately developed
Procyon lotor Northern raccoon4ProcyonidaeSemi-arborealIntermediately developed
Nasua narica White-nosed coati4ProcyonidaeSemi-arborealPoorly developed
Nasua nasua South American coati3ProcyonidaeSemi-arborealPoorly developed
Bassaricyon alleni Allen's olingo3ProcyonidaeArborealWell developed
Bassaricyon gabbii Bushy-tailed olingo3ProcyonidaeArborealWell developed
Bassariscus astutus Ringtail7ProcyonidaeSemi-arborealPoorly developed

Ancestral Character State Reconstruction

To test whether the evolution of an arboreal lifestyle preceded the evolution of grasping ability, an ancestral state reconstruction of lifestyle and food-handling behaviour was conducted as follows (Table 1). Three categories of lifestyles were defined following Nowak (2005) and Wilson & Mittermeier (2009): an arboreal lifestyle defines species that spend the majority of their time in the trees; a semi-arboreal lifestyle represents species that spend time both in trees and on the ground without a clear preference for either, and a terrestrial lifestyle defines species that spend the majority of their time on the ground. Three categories of grasping ability are also defined following the descriptions in Iwaniuk & Whishaw (1999) and Antón et al. (2006) for procyonids and ailurids, and the descriptions in Nowak (2005) and Wilson & Mittermeier (2009) for all other species. These categories are species with a well-developed grasping ability, an intermediately developed grasping ability and a poorly developed grasping ability.

The ancestral state reconstructions were performed using the parsimony reconstruction method in Mesquite (Maddison & Maddison, 2011). This method summarizes state change of characters (lifestyle or grasping ability) over the tree by minimizing the number of steps of character change. The unordered states assumption was used as model of evolution, which means that each change of character along the tree is counted as a changed. We used the time-calibrated phylogeny of caniform carnivorans from Slater et al. (2012) as the framework for our analyses. The tree uses the family-level phylogeny of Carnivora from Eizirik et al. (2010) as a backbone, with time-calibrated molecular phylogenies for each family appended to it. Full details of the phylogenetic reconstruction are provided in the supplementary information of Slater et al. (2012). For our analyses, we pruned the tree so that only species represented in our data set remained (Fig. 1).

Quantification of Shape Variation Using 3D Geometric Morphometrics

Because of the complex shape of the elbow articulation, it cannot be correctly represented using traditional landmarks. Thus, a 3D sliding semi-landmark procedure was used to quantify forelimb morphology based on scanned specimens (Bookstein, 1997; Gunz et al., 2005). With this procedure, sliding semi-landmarks on surfaces and curves are transformed into spatially homologous landmarks (Parr et al., 2012) that can be used to compare shapes. Sliding semi-landmarks are allowed to slide along the curves and surfaces that are predefined on each surface while minimizing the bending energy. Morphometric data (landmarks, curves) were obtained using the software package Idav Landmarks (Wiley et al., 2005), whereas Edgewarp3D 3.31 (Bookstein & Green, 2002) was used to obtain the sliding semi-landmarks. To do so, we first created a template representing the entire variation of the musteloid data set.

Each specimen is defined by its homologous anatomical landmark coordinates, which are comprised of twenty-one landmarks for the humerus (Fig. 2, Table 2), nineteen landmarks for the ulna (Fig. 2, Table 3) and thirteen landmarks for the radius (Fig. 2, Table 4). Based on the homologous landmarks, the sliding semi-landmarks of the template are warped onto the new specimen while minimizing the bending energy. Next, the warped sliding semi-landmarks are projected onto the predefined curves and surfaces of the new specimen. The curves consist of the distal surface of the articulation of the humerus and the proximal and distal articulations surface of the radius and ulna (Fig. 2). Finally, spline relaxation must be performed allowing sliding semi-landmarks to slide along the curves and surfaces' tangent structures (Gunz et al., 2005). During the relaxation step, sliding semi-landmarks are projected onto the nearest curves and surfaces. Both sliding and relaxation are repeated iteratively until the bending energy is minimized. At the end of this procedure, 306 landmarks (21 homologous landmarks and 285 sliding semi-landmarks) for the humerus, 165 landmarks (13 homologous landmarks and 152 sliding semi-landmarks) for the radius and 330 landmarks (19 homologous landmarks and 311 sliding semi-landmarks) for the ulna describe the shape of each bone and their articulations. After this operation has been performed for each data set, the landmarks of all specimens can be compared using traditional morphometric methods.

Table 2. Definition of the landmarks on the humerus used for geometric morphometric analyses
LandmarkDefinition
1Most medio-distal point of the caudal part of the trochlea
2Most medio-proximal point of the caudal side of the trochlea
3Point of maximum of curvature of the olecranon fossa
4Most latero-proximal point of the caudal side of the trochlea
5Point of maximum of convexity of the lateral epicondylar crest
6Point of insertion of the lateral epicondylar crest on the diaphyse
7Most proximal tip of the medial epicondyle
8Most distal tip of the medial epicondyle
9Most medio-proximal point of the cranial side of the trochlea
10Point of maximum of curvature of the coronoid fossa
11Most proximo-anterior point of contact between the trochlea and the capitulum
12Point of maximum of curvature of the radial fossa
13Most latero-proximal point of the cranial side of the capitulum
14Most disto-lateral point of the capitulum
15Most distal point of contact between the trochlea and the capitulum
16Most distal point of the deltopectoral crest
17Tip of the lesser tuberosity
18Most proximo-medial point of the greater tuberosity
19Most disto-medial point of the greater tuberosity
20Most latero-distal point of the cranial side of the capitulum
21Point of maximum of concavity of the caudo-medio-distal part of the trochlea
Table 3. Definition of the landmarks on the ulna used for geometric morphometric analyses
LandmarkDefinition
1Most lateral point of contact between the trochlear notch and the radial notch
2Most proximo-lateral point of the incisure of the trochlear notch
3Point of maximum of concavity of the proximal part of the trochlear notch
4Most proximo-medial point of the incisure of the trochlear notch
5Most palmar-lateral point of olecranon process
6Most palmar-medial point of olecranon process
7Most dorsal-medial point of olecranon process
8Most dorsal-lateral point of olecranon process
9Point where the most medial part of the coronoid process meets the most medio-distal part of the trochlear notch
10Most anterior point of contact between the trochlear notch and the radial notch
11Point of maximum of concavity between the radial notch and the trochlear notch
12Most latero-distal point of insertion of the radial notch
13Tip of the styloid process
14Most distal point of the articular facet that articulates with the radius
15Most proximal point of the articular facet that articulates with the radius
16Point where the proximo-lateral part of the coronoid process meets the lateral part of the trochlear notch
17Most distal point of insertion of the medial epicondylar crest on the diaphysis
18Point of maximum of curvature of the medial epicondylar crest
19Most proximal point of insertion of the medial epicondylar crest on the diaphysis
Table 4. Definition of the landmarks on the radius used for geometric morphometric analyses
LandmarkDefinition
1Most disto-lateral point of anterior side of the ulnar facet
2Most proximo-lateral point of anterior side of the ulnar facet
3Point of maximum of concavity of the anterior part of the fovea
4Tip of the fovea
5Most disto-medial point of the distal articular facet with the ulna
6Most proximal point of curvature of the distal articular facet with the ulna
7Most disto-lateral point of the distal articular facet with the ulna
8Distal tip of the styloid process
9Medial tip of the styloid process
10Most disto-lateral point of the dorsal side of the radius
11Most proximal point of the groove for extensor digitorium and extensor indicis
12Most proximo point of groove for extensor carpi radialis longus and brevis
13Most disto-medial point of the anterior side of the ulnar facet
image

Figure 2. Landmarks used in analyses to quantify shape variation on the forelimb bones. (a) humerus; (b) ulna; (c) radius. Black crosses represent landmarks; red dashed lines represent outlines used for the surface analyses of the articulations of each bone.

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Once all landmark data were obtained, a generalized Procrustes superimposition (Rohlf & Slice, 1990) was performed on the point coordinates using the package Rmorph (Baylac, 2012) in R (R Development Core Team, 2011). A principal component analysis (PCA) on the shape data was performed to evaluate the distribution of species in morphospace. The visualizations of shapes change (conformation) at the extreme of each axis were performed in two ways: first, the Evan toolbox (http://www.evan.at) package was used to generate 3D thin-plate spline visualizations; and second, a visualization of conformation change using shapes coordinates at the extreme of each axis was obtained with the package Rmorph in R and reconstructed in Geomagic Studio (http://www.geomagic.com). A mean conformation was calculated separately for arboreal species having either well-developed or poorly developed grasping ability, as well as for all arboreal species, allowing visualization of the shape differences between these groups.

Statistical Analyses

As species share some part of their evolutionary history, they cannot be treated as independent data points. Thus, we conducted these analyses in a phylogenetic framework (Felsenstein, 1985; Harvey & Pagel, 1991) using the recently published phylogeny described above (Fig. 1) and with branch lengths proportional to time. To test whether grasping ability or lifestyle influences forelimb shape, we performed a phylogenetic manova and anovas (Garland et al., 1993) on the principal components that explain a significant proportion of the shape variation for each bone: the first four principal components of the humerus data set and the first three principal components of the ulna and radius data sets. We used the phy.manova and the phy.anova function in the R package ‘geiger’ (Harmon et al., 2008) for our analysis. To test whether animals with different lifestyles and grasping abilities differed in shape, simulation of new shapes variables on the tree was performed. We used Brownian motion as our model for evolutionary change and ran 1000 simulations to create an empirical null distribution against which the F-value from the original data could be compared. We considered differences among categories significant if the original P-value was higher than the P95-value derived from the empirical, simulated distribution. For the manova, we used a Wilks' statistic as a multivariate test. This gives an approximation of the F distribution by a transformation of the test statistic. Finally, standard Bonferroni corrected post hoc tests were calculated using the phylanova function in the R package ‘phytools’ (Revell, 2012). These corrected post hoc tests allow us to test for differences between each lifestyle and grasping ability of group and consist of a comparison of the means of each category in each group.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information

Ancestral Character State Reconstructions

The ancestral state reconstruction of lifestyle (Fig. 3) suggests that the character state of the common ancestor of musteloids and of the clade containing ailurids + procyonids + mustelids was equivocal. The basal node of the mustelids was either terrestrial or semi-arboreal, whereas procyonids were reconstructed as having an arboreal ancestor. Furthermore, our reconstructions suggest that a specialized arboreal lifestyle evolved on at least two separate occasions: once in the ailurids (Ailurus fulgens) and once in procyonids (Potos flavus, Bassariscus astutus, Bassaricyon alleni, Bassaricyon gabbii). Semi-arboreality evolved on three separate occasions: once in mustelids (Martes and Eira clades) and twice independently in procyonids (Procyon clade and Nasua clade).

image

Figure 3. Ancestral character state reconstructions for lifestyles on the left and grasping ability on the right.

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The ancestral state reconstruction of grasping ability (Fig. 3) suggests that the common ancestor of musteloids had a poorly developed prehensile ability. The common ancestor of the ailurid, procyonid and mustelid clades was also reconstructed as having poorly developed prehensile abilities. The base of procyonid node was also reconstructed as having a poorly developed prehensile ability. This reconstruction suggests that the character of intermediately developed grasping appeared independently twice: once in the ailurid clade and once in the Procyon clade. A well-developed grasping ability evolved on two separate occasions among procyonids: once in the Potos lineage and once at the base of the Bassaricyon clade.

Shape Variation Using 3D Geometric Morphometrics

Only axes and the associated conformations that were significantly different among groups, as determined by regular or phylogenetic anovas (Table 5), are described below.

Table 5. Results of anovas (F and P-values) and Phylogenitic anovas (Phyl P-value) for the first four principal shape components of the humerus, the first three principal shape components of the ulna and the first three principal shape components of the radius. Principal components showing significant differences are indicated in bold
 LifestyleGrasping ability
 F-valueP-valuePhyl P-valueF-valueP-valuePhyl P-value
  1. ‘***’0.001; ‘**’0.01; ‘*’0.05.

HumerusPC1 8.35 0.0037** 0.073 7.72 0.0049** 0.063
PC2 3.78 0.047* 0.27 9.63 0.002** 0.028*
PC32.280.140.480.680.520.78
PC43.40.060.3261.020.380.70
UlnaPC1 13.63 0.00042*** 0.025* 14.06 0.00036*** 0.006**
PC20.580.570.810.590.560.8
PC33.050.0770.361.680.210.56
RadiusPC1 11.70 0.00087*** 0.033* 8.445 0.0035** 0.048*
PC20.800.460.7351.820.1960.48
PC33.480.0570.313 4.78 0.025* 0.18
Influence of Locomotion and Grasping Ability on Humerus Shape

A standard and phylogenetic manova and anova were performed on the first four principal components representing 65% of the variation in humerus shape (Table 5). Results of the manova and phylogenetic manova were significant for lifestyle (manova: Wilks λ = 0.090, F2,15 = 7.01, < 0.001; manova Pphyl = 0.021) and grasping ability (manova: Wilks λ = 0.1269, F2,15 = 5.42, < 0.001; manova Pphyl = 0.053). Results of the anovas were significant for the first two axes for lifestyle (PC1 = 0.0037, PC2 = 0.047) and the first two axes for grasping ability (PC1 = 0.0049 and PC2 = 0.002). Results were not significant for other axes. Results of the phylogenetic anova were only significant for grasping ability on the second principal component (PC2: Pphyl = 0.028). These results indicate a strong influence of prehensile ability on the shape of the humerus as represented by the second axis when phylogeny is taken into account. The post hoc tests showed differences in prehensile ability between species displaying an intermediately developed and well-developed ability (PC2 = 0.032) and between species showing well-developed and poorly developed ability (PC2 = 0.024) on the second axis.

Shape Variation

The first three principal component (PC) axes accounted for 56.9% of the total shape variation. The overall distribution of the different taxa in the morphospace as defined by the first and second axes (Fig. 4) showed a gradient from terrestrial species to arboreal ones. Principal component 1 (Fig. 4) tended to differentiate arboreal species and semi-arboreal species able to grasp on the negative part of the axis from terrestrial species unable to grasp and some semi-arboreal species unable to grasp on the positive part of the axis. Shape changes associated with PC1 (Fig. S1) on the negative part of the axis encompass a more gracile humerus with a relatively small distal articulation with a capitulum that is relatively broader in comparison with the trochlea, a relatively narrow and concave trochlea, a relatively straight medial lip of the trochlea, a relatively short medial epicondyle, a relatively small lateral epicondylar crest and a greater tubercle oriented more vertically relatively to the diaphysis. In contrast, terrestrial and some semi-arboreal species falling on the positive part of the axis show a relatively more robust humerus with a relatively broad distal articulation with a smaller capitulum in comparison with the trochlea, a medial lip of the trochlea that is oriented more medially, a relatively large medial epicondyle, a relatively prominent lateral epicondylar crest and a greater tubercle that is oriented more horizontally relatively to the diaphysis.

image

Figure 4. Results of a principal component analysis performed on the morphometric data for the humerus. (a) scatter plot illustrating the position of different species on the first two principal components; (b) scatter plot illustrating the position of different species on axes one and three; (c) scatter plot illustrating the position of different species on the axes two and three. Shaded polygons represent lifestyles; black: terrestrial lifestyle, grey: semi-arboreal, white: arboreal. The prehensile ability of each species is represented by a dot for poorly developed, a triangle for intermediately developed and a star for a well-developed prehensile ability.

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The negative end of principal component 2 (Fig. 4) is occupied by terrestrial species, semi-arboreal weasels (Martes) and the tayra (Eira barbara), which are all unable to grasp, as well as the arboreal red panda (Ailurus fulgens) and the semi-arboreal raccoons (Procyon), which all display an intermediately developed ability to grasp. Arboreal olingos and kinkajous (Bassaricyon and Potos) with a well-developed ability to manipulate and semi-arboreal coatis (Nasua), which are unable to grasp, are positioned towards the positive part of the axis. Shape changes associated with PC2 (Fig. S1) on the negative part of the axis include characterized by a relatively short distal articulation with a relatively broad trochlea in comparison with the capitulum, a relatively narrow and concave trochlea, a relatively narrow and asymmetrical posterior part of the trochlea with a higher and asymmetrical olecranon fossa and a relatively smaller coronoid fossa in comparison with the radial fossa. In contrast, species falling on the positive part of the axis display the opposite morphology.

Influence of Locomotion and Grasping Ability on the Shape of the Ulna

Results of the manova and phylogenetic manova performed on the first three principal components of the ulna shape were significant for lifestyle (manova: Wilks λ = 0.081, F2,15 = 10.81, < 0.001; manova Pphyl = 0.004). Results of the manova of the ulna shape were significant for grasping ability, but the phylogenetic manova was not significant (manova: Wilks λ = 0.21, F2,15 = 5.02, < 0.001; manova Pphyl = 0.07). An anova performed on the first three principal components of the ulna shape (Table 5) showed significant results on the first axis for both lifestyle (PC1 < 0.001) and grasping ability (PC1 < 0.001). Results of the phylogenetic anova were also significant on the first principal component for lifestyle (Pphyl = 0.025) and grasping ability (Pphyl = 0.006). Results were not significant for all others axes. Results of the corrected post hoc tests show differences in prehensile ability between species with poorly and intermediately developed abilities (PC1 = 0.012), and in lifestyle between arboreal and terrestrial species (PC1 = 0.048) and between terrestrial and semi-arboreal species (PC1 = 0.048).

Shape Variation

The first three PC axes (Fig. 5) accounted for 67% of the overall shape variation. The morphospace as defined by the scatter plots of the first and second and of the first and third axes tended to separate terrestrial species from semi-arboreal and arboreal species. Furthermore, a gradient of prehensile ability can be observed along the first axis from intermediately developed to poorly developed ability.

image

Figure 5. Results of a principal component analysis performed on the morphometric data for the ulna. (a) scatter plot illustrating the position of different species on the first two principal components; (b) scatter plot illustrating the position of different species on axes one and three; (c) scatter plot illustrating the position of different species on axes two and three. Shaded polygons represent lifestyles; black: terrestrial lifestyle, grey: semi-arboreal, white: arboreal. The prehensile ability of each species is represented by a dot for poorly developed, a triangle for intermediately developed and a star for a well-developed prehensile ability.

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Principal component 1 (Fig. 5) tended to differentiate semi-arboreal and arboreal species (with the exception of Martes foina and Eira barbara) from terrestrial species. Species that display an intermediately developed to a well-developed prehensile ability fall on the negative end of the axis. In contrast, more terrestrial species occupy the positive part of the axis. Shape changes associated with the negative end of PC1 (Fig. S2) describe a relatively gracile and straight ulna with a relatively small proximal and distal articulations, an olecranon process that is relatively short and straight, a radial notch with a double and concave surface, a relatively narrow angle between radial notch and the coronoid process, a relatively short and flat medial epicondylar crest with a more proximal insertion on the diaphysis that is higher than the distal radial facet and a relatively narrow and concave anconeal process. Shape change associated with the positive part of PC1 displays a relatively robust ulna with the opposite morphology to that described above for the negative end of the axis.

Influence of Locomotion and Grasping Ability on the Shape of the Radius

Results of the manova performed on the first three principal components of the radial shape were significant for both lifestyle (manova: Wilks λ = 0.21, F2,15 = 5.12, < 0.001) and grasping ability (manova: Wilks λ = 0.169, F2,15 = 6.19, < 0.001). However, the results of the phylogenetic manova were only significant for the grasping ability (manova Pphyl = 0.025) and not for the influence of the lifestyle (manova Pphyl = 0.086). Both a traditional and a phylogenetic anova were performed on the first three principal components of the radius shape (Table 5) and revealed significant differences among groups on the first axis for lifestyle (PC1 < 0.001; Pphyl = 0.033) and on the first and third axes for grasping ability with results of the phylogenetic anova being significant only on the third axis (PC1 = 0.0035, Pphyl > 0.05; PC3 = 0.025, Pphyl = 0.048). Results were not significant for all other axes. Results of the post hoc tests were not significant.

Shape Variation

The first three PC axes accounted for 72% of the total shape variation. The overall distribution of taxa on the first and second axes and the first and third axes (Fig. 6) showed a cluster of terrestrial species that was generally differentiated from semi-arboreal and arboreal species. Species that display a well-developed prehensile ability tend to cluster in morphospace. Arboreal species with a degree of grasping ability tend to be separate from semi-arboreal and terrestrial species in the morphospace defined by the first and third axes.

image

Figure 6. Results of a principal component analysis performed on the morphometric data for the radius. (a) scatter plot illustrating the position of different species on the first two principal component; (b) scatter plot illustrating the position of different species on axes one and three; (c) scatter plot illustrating the position of different species on axes two and three. Shaded polygons represent lifestyles; black: terrestrial lifestyle, grey: semi-arboreal, white: arboreal. The prehensile ability of each species is represented by a dot for poorly developed, a triangle for intermediately developed and a star for a well-developed prehensile ability.

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The negative end of principal component 1 (Fig. 6) was occupied by arboreal species and semi-arboreal species with intermediately developed ability of grasping, as well as weasels (Martes) that have poorly developed ability to grasp, whereas terrestrial species and some semi-arboreal species that are unable to grasp fell along the positive part of the axis. The negative part of the PC1 (Fig. S3) was defined by a relatively gracile radius with a relatively small proximal and distal articulation, a circular proximal articular surface, a relatively flatter than convex fovea with a relatively flat tip, a posterior border of the proximal surface contacting the radial notch of the ulna which is circular and an anterior border which is round with a relatively narrow interruption of its rim, an antero-medial part of the proximal surface contacting the radial notch of the ulna which is relatively thin and a relatively narrow and asymmetrical distal epiphysis with a relatively small medial styloid process. Shape change associated with the positive part of the PC1 displays a relatively robust radius with a radial head that is oval-shaped, a relatively more concave anterior part of the fovea with a relatively prominent tip, a posterior border of the proximal ulnar facet which is oval, but an anterior border that is relatively concave with a relatively broad interruption of its rim, a antero-medial part of the proximal ulnar facet which is relatively broad, a distal articulation which is relatively broad, and a relatively large and symmetric distal epiphysis with a prominent medial styloid process.

Principal component 3 (Fig. 6) tends to separate the kinkajou (Potos flavus) on the negative part of the axis from all other species. Radial morphology associated with species on the negative part of PC3 (Fig. S3) consists of a rounded radial head, which is oriented postero-distally, a relatively broader posterior rim of the proximal ulnar facet, a tip of the fovea that is relatively flat, a relatively round and concave fovea, a proximal ulnar facet with a relatively equal antero-lateral surface in comparison with the antero-medial one, an antero-medial surface of the proximal ulnar facet that is relatively large and flat, a relatively low tip on the styloid process and a relatively convergent orientation of the groove of the extensor digitorum and extensor indicis to the groove of the extensor carpi radialis longus and brevis. Shape changes associated with species on the positive part of the axis involve the opposite morphology.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information

Our analyses of humerus shape (Fig. 4, Table 5) show that arboreal species tend to fall in the same part of morphospace as species having a well-developed grasping ability. Shapes associated with the humerus (Fig. 7, Fig. S1) of arboreal species and species displaying a well-developed grasping ability show mainly a narrow trochlea relative to the capitulum, which is broad and well-developed distally where the fovea of the radial head articulates. This kind of conformation has been suggested to facilitate forearm movements during pronation–supination, which is important during both arboreal locomotion and grasping (Sargis, 2002; Antón et al., 2006; Candela & Picasso, 2008; Flores & Díaz, 2009). The trochlea of arboreal species is relatively narrow with a shallow trochlear groove. It reflects the trochlear notch on the ulna, which is also small and narrow. Terrestrial species unable to grasp display the opposite morphology, and this pattern of form likely restricts movement and stabilizes the elbow joint. As such, it is likely efficient for load bearing and may help dissipate the load of the anterior part of the animal transferred to the front limbs during locomotion (Szalay & Sargis, 2001).

image

Figure 7. Mean shape of forelimb elements of arboreal species (orange) and species having a well (green) and poorly developed (black) grasping ability. (a) humerus: (a) posterior view; (b) anterior view; (c) close-up of the distal articulation in posterior view; (d) close-up of the distal articulation in distal view; (e) close-up of the distal articulation in anterior view. (b) ulna: (a) anterior view; (b) lateral view; (c) close-up of the proximal articulation in anterior view; (d) close-up of the proximal articulation in lateral view; (e), close-up of the distal articulation in anterior view. (c), radius: (a) anterior view; (b) lateral view; (c), close-up of the proximal articulation in anterior view; (d), proximal view; (e) close-up of the proximal articulation in posterior view. Dots and grey surfaces represent landmarks; lines represent real links between landmarks; dashed lines represent a schematic representation of the bone.

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The analyses of the shape of the ulna (Fig. 5, Table 5, and Fig. S2) and radius (Fig. 6, Table 5, and Fig. S3) show that arboreal and semi-arboreal species again fall in the same area of morphospace as do species able to grasp. Moreover, morphological differences between species with different degrees of grasping behaviour are evident in the distribution of taxa in the ulnar and radial morphospaces. Indeed, a cluster of species having a well-developed grasping ability is clearly differentiated from another cluster of semi-arboreal species having an intermediately developed grasping ability for both the ulna (Fig. 5A, Fig. S2) and the radius (Fig. 6A, Fig. S3). The ulnar and radial morphologies (Fig. 7, Fig. S2) of species with a well-developed grasping ability, as well as of arboreal species, correspond to gracile bones with a less developed medial epicondylar crest on the diaphysis of the ulna and a narrow and poorly developed distal end of the radius. The ulnae of arboreal species display a short olecranon process. This character has biomechanical consequences as it decreases the lever arm and consequently decreases the force during flexion-extension movements. However, this character appears to be related to an increase in the speed of movement (Rose, 1993; Argot, 2001) and was previously interpreted as an adaptation to arboreality observed in species able to perform rapid locomotion on thin branches (Rose, 1993; Argot, 2001). The ulnae of arboreal species display a straight diaphysis and olecranon process (Fig. 7, Fig. S2). This character is thought to facilitate the transmission of compressive loading (Lanyon, 1980; Flores & Díaz, 2009) and likely relates to the importance of this bone in load transfer and stability of the forelimb.

The orientations of the proximal and distal radial notches (Fig. 7, Fig. S2) of arboreal species are clearly different from those of species unable to grasp, which are mainly terrestrial. The proximal radial notch of the ulna is broad and laterally oriented, and the distal radial notch is antero-distally oriented. The proximal ulnar notch of the radius is broad around the fovea, and the distal one is broad and proximally oriented relative to the diaphysis. Both of these articular surfaces of the forearm seem to perfectly fit with each other, suggesting a strong degree of co-evolution. These configurations likely also facilitate the rotation of the radius around the ulna given the extent of the articulation and its orientation. Furthermore, the circular shape of the radial head together with a round and slightly concave fovea in arboreal species, and especially in species having a well-developed grasping ability, may allow the rotation of the radius on the ulna and also on the capitulum of the humerus. This configuration likely provides a wide range of pronation–supination movements and consequently a greater mobility to the forearm and the hand (MacLeod & Rose, 1993; Argot, 2001; Szalay & Sargis, 2001; Flores & Díaz, 2009). In contrast, terrestrial species and species showing poorly developed grasping ability display an oval-shaped radial head complemented by a sharp antero-medial fovea, which likely restricts the range of rotational movements.

Although our results thus show many similarities between arboreal species and those species with a well-developed grasping ability, shape differences do exist (Fig. 7). Species with a well-developed grasping ability appear to exhibit exaggerated arboreal characteristics, rather than novel attributes. In the humerus, they display a distal articulation with a relatively broader capitulum in comparison with the trochlea, a relatively flat trochlear groove and a relatively poorly developed lateral epicondylar crest. In the ulna, the mean shape of species with a well-developed ability to grasp (Fig. 7) involves a relatively straight olecranon process, a relatively narrow medio-distal trochlear notch, a relatively more distal insertion of the medial epicondylar crest on the diaphysis that is positioned at the same level as the distal radial facet, and a relatively narrow and oval-shaped distal radial facet. The radius of species having a well-developed grasping ability (Fig. 7) is a gracile element with a relatively small radial head, which is circular, a fovea with a skewed orientation relative to the diaphysis, an antero-medial part of the proximal surface contacting the radial notch of the ulna which is relatively thin, a distal ulnar articulation which is oriented more perpendicularly than parallel relative to the diaphysis, and a relatively short, narrow and asymmetrical distal part of the radius. Overall, the forelimb of species with a well-developed ability to grasp appears to provide a greater potential for rotation, yet this remains to be tested empirically.

Thus, our quantitative shape descriptions suggest differences in forelimb shape that reflect both the influences of lifestyle and grasping ability. The results of our manovas show that both lifestyle and grasping behaviour influence the shape of long bones of the forelimb. Nevertheless, our results of our phylogenetic manovas show that grasping behaviour appears to influence the radial shape more, whereas locomotion influences primarily the humeral and ulnar shapes. These results seem to suggest that the ulna plays a greater role in load transfer than mobility per se. The results of our anovas and phylogenetic anovas (Table 5) confirm this. Overall, the results of our shape analyses show that species having a well-developed grasping ability tend to fall in the same area of morphospace as do arboreal ones, and this pattern holds for all the long bones of the forelimb. This distribution of species in morphospace can be seen particularly clearly for the more distal elements (radius and ulna). Moreover, the radial and ulnar morphospaces were more similar to one other in comparison with those of the humerus, suggesting that these elements may play a functional role that is distinct from those of the humerus but more similar to each other during grasping and/or arboreal locomotion. Indeed, grasping and manipulation involve pronation–supination movements, which mainly occur at the elbow joint and primarily involve the lower arm bones. Pronation and supination consist of a rotational movement where the radius revolves medio-laterally around the ulna. These movements of rotation occur on the proximal part of the radius where the proximal ulnar notch of the radial head allows the rotational movements around the radial notch of the ulna and at the distal ulnar notch, which is a concave surface that allows rotation of the radius against the ulna. Interestingly, our shape analyses indicate that it is exactly these zones that show the largest differences between groups.

In addition to showing quantitative differences in the shape of the long bones of the forelimb, our ancestral character state reconstruction (Fig. 3) also showed that the evolution of an arboreal lifestyle in musteloids tends to precede the development of specializations for grasping ability. This may explain the observed similarity in shape between arboreal species and species with a well-developed grasping ability (Fig. 7), with the morphology of able graspers being an exaggerated version of that of arboreal species. Moreover, our results show multiple independent origins of a well-developed grasping ability among musteloids. These results suggest that arboreal lifestyle can confer an advantage in the development of complex grasping as suggested previously for ailurid carnivorans (Antón et al., 2006; Salesa et al., 2006) and primates (Godinot, 1991, 2007). Yet, whether these patterns are generally applicable to mammals remains to be seen, and a broader analysis of forelimb shape including taxa with other lifestyles such as aquatic or fossorial species is needed to more fully understand the evolution of grasping and the morphologies that underlie it.

In conclusion, our results confirm our predictions and suggest that the functional signal of grasping ability on forelimb shape is stronger for forelimb bones most implicated in the movement such as the radius. The humerus and ulna, on the other hand, appear to be influenced more by constraints for load bearing. The overall shape of the forelimb of both arboreal species and species showing a well-developed grasping ability suggests a potential wide range of pronation–supination movements that may confer a greater mobility to the forearm and the hand. Our results demonstrate the importance of using 3D surface methods to describe differences in morphology related to functional traits involving complex movements. The addition of quantitative and qualitative behavioural data of species during grasping and manipulation (such as rotational capacity and movement complexity) complemented by detailed information on muscular anatomy would contribute to further improving the ability to characterize forelimb morphology in the context of locomotion and grasping ability. Finally, despite the abundance of research focused on the evolution of grasping ability and forelimb shape in mammals, the complete lack of quantitative data for the majority of taxa prevents broader interpretations of evolutionary patterns. Thus, more quantitative data on shape and behaviour are needed to advance our understanding of the evolution this complex attribute.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information

We thank Jacques Cuisin, Géraldine Véron, Julie Villemain, Céline Bens and Tarik for access to specimens from the collections Mammifères et Oiseaux, MNHN, Paris. We also thank Loïc Costeur for allowing us to scan the material from the Naturhistorisches Museum, Basel; Judy Chupasko for allowing us to scan the material from the Harvard Museum of Comparative Zoology, Cambridge, Massachusetts; and Suzanne Peurach for allowing us to scan the material from the Smithsonian National Museum of Natural History, Washington, D.C. We thank the ‘plate-forme de morphométrie’ of the UMS 2700 (CNRS, MNHN) for access to the surface scanner. ACF thanks the doctoral school FdV, the Fondation Bettencourt-Schueller, and, Andrew Murray and Mary Collins to help her to obtain a UCL IMPACT scholarship for funding. We also thank Andrew Murray, Mary Collins, Anthony Herrel, Livia Bascher, Marcela Randau, Sybile Moulin and Céline Houssin for their helpful discussions and comments on this manuscript.

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  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information
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Supporting Information

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
  9. Supporting Information
FilenameFormatSizeDescription
jeb12161-sup-0001-Data1.docWord document68KData S1 Specimens used in analyses.
jeb12161-sup-0002-FigS1-S3.pdfapplication/PDF5382K

Figure S1 Shapes change of the humerus associated with each significant principal component. Shapes correspond to the positive (red) and negative (blue) extremes of each axis.

Figure S2 Shapes change of the ulna associated with each principal significant component axis. Shapes correspond to the positive (red) and negative (blue) extremes of each axis.

Figure S3 Shapes change of the radius associated with each principal component axis. Shapes correspond to the positive (red) and negative (blue) extreme of each axis.

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