Evolution of grasping among anthropoids

E. POUYDEBAT,* M. LAURIN,� P. GORCE* & V. BELS�*Handibio, Universite du Sud Toulon-Var, La Garde, France

�Comparative Osteohistology, UMR CNRS 7179, Universite Pierre et Marie Curie (Paris 6), Paris, France

�UMR 7179, MNHN, Paris, France

Introduction

Grasping behaviour is a key activity in primates to obtain

food. The hand is used in numerous activities of manip-

ulation and locomotion and is linked to several func-

tional adaptations (Godinot & Beard, 1993; Begun et al.,

1997; Godinot et al., 1997). In particular, the hand is

involved in prehension, such as gripping of static foods

(fruits, leaves) and dynamic foods such as insects or other

prey (frogs, rodents, small antelopes). Some primates

such as chimpanzees (Pan troglodytes) and capuchins

(Cebus apella) use their hands to manipulate tools, to

crack nuts, for example (Boesch & Boesch, 1990; Fraga-

szy et al., 2004), whereas gorillas (Gorilla gorilla) use their

hands to extract food from holes (Pouydebat et al., 2005).

The evolution of primates (humans included) is linked to

the development of those behaviours allowing organisms

to exploit the resources in their environment. A general

model of grasping in primates proposes an evolution from

a ‘power grip’ towards a ‘precision grip’, supposed to

have taken place in hominids; the precision grip has been

suggested to appear with Australopithecus afarensis (Mar-

zke, 1997) or with Homo (Napier, 1956, 1960). The power

grip is defined as a grasp with the palm, and is probably a

very old behaviour, as it occurs in anurans, crocodilians,

squamates and several therian mammals (Gray, 1997;

Iwaniuk & Whishaw, 2000). On the contrary, the

precision grip, in which an object is held between the

distal surfaces of the thumb and the index finger, is

usually viewed as a derived function, linked to tool use

and human morphological autapomorphies (Napier,

1956; Tuttle, 1965; Schultz, 1969; Susman, 1979, 1989;

Marzke et al., 1992; Clark, 1993). The precision grip has

been considered the most important hand function of all

prehensile movements (Napier, 1980).

Our aim is to reconsider this simple model of grasping

evolution in the light of morphometric data from

numerous species of primates and behavioural consider-

ations such as areas of contact between the fingers and

the food grasped by extant primates. Therefore, the

possible presence of a phylogenetic signal in the behavio-

ural and relevant morphometric characters is investi-

gated and the correlation between morphometric and

behavioural characters is also determined. We also

present models that enable inference of behaviours from

morphological characters, which we use to infer behav-

iours in three extinct primates: Proconsul africanus,

Oreopithecus bambolii and Australopithecus afarensis, three

species considered to have divergent grasping abilities.

Proconsul africanus and Australopithecus afarensis are from

Africa, which is probably the cradle of hominoid diver-

sification (Arnason et al., 2000; Folinsbee & Brooks,

Correspondence: Michel Laurin, Comparative Osteohistology, UMR CNRS

7179, Universite Pierre et Marie Curie (Paris 6), Paris, France.

Tel.: (33) 1 44 27 36 92; e-mail: michel.laurin@upmc.fr

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Keywords:

behaviour;

grasping;

hominids;

palaeobiology;

phylogeny;

precision grip;

primates;

variance partitioning with PVR.

Abstract

The prevailing hypothesis about grasping in primates stipulates an evolution

from power towards precision grips in hominids. The evolution of grasping is

far more complex, as shown by analysis of new morphometric and behavio-

ural data. The latter concern the modes of food grasping in 11 species (one

platyrrhine, nine catarrhines and humans). We show that precision grip and

thumb-lateral behaviours are linked to carpus and thumb length, whereas

power grasping is linked to second and third digit length. No phylogenetic

signal was found in the behavioural characters when using squared-change

parsimony and phylogenetic eigenvector regression, but such a signal was

found in morphometric characters. Our findings shed new light on previously

proposed models of the evolution of grasping. Inference models suggest that

Australopithecus, Oreopithecus and Proconsul used a precision grip.

doi: 10.1111/j.1420-9101.2008.01582.x

2007). Oreopithecus bambolii was found in Tuscany, Italy.

It is included here because its prehensile behaviour has

been inferred in the literature (Moya-Sola et al., 1999;

Susman, 2004).

Material and methods

Quantification of areas of contact

SubjectsThe data represented in this study are based on a wide

variety of primates observed in captivity (Appendix S1):

nine capuchins (C. apella), nine macaques (Macaca

fuscata), nine baboons (Papio papio), three gibbons

(Hylobates lar), seven orang-utans (Pongo pygmaeus), three

gorillas (G. gorilla) and 14 chimpanzees (P. troglodytes).

We also have observations from nine children, 2–5 years

of age (Homo sapiens), and nine adults (H. sapiens). Data

for three other species were collected from the literature

(Christel, 1993; Christel et al., 1998): black mangabey

(Cercocebus aterrimus), geladas (Theropithecus gelada) and

bonobos (Pan paniscus). These species represent a wide

array of body size, hand morphological traits and

anthropoid taxa. Indeed, capuchins do not possess an

opposable thumb and none of the studied primate species

except humans has morphological traits usually associ-

ated with precision grip.

Protocol of observationsThe observations of grasping of small and large objects

have been made in various groups of animals belonging

to zoological gardens in France. All individuals observed

in any given species belong to a single group and the

hierarchical position of each specimen was established.

The animals were observed without modification of their

social (within their group) or environmental (e.g. logs,

rocks, ropes) context to maintain: (i) all behavioural

interactions between the members of the group; (ii) all

constraints in relation to the environment; and (iii) all

possibility of opportunistic manipulation (Parker &

Gibson, 1977).

All observations of the animals were made for

7 months (Pouydebat, 2004). The duration of observa-

tion for each specimen was standardized following

the usual methods suggested in comparative ethology

(Lehner, 1996). A preliminary analysis was conducted by

‘ad libitum sampling’ (Altmann, 1974) that permits the

individual recognition of all subjects for each species and

the identification of a wide variety of areas of fingers in

contact with the presented objects. During the study,

each individual was observed according to the method of

‘focal animal sampling’ (Altmann, 1974). We filmed the

animals during two sessions of 2 h each for chimpanzees,

baboons, capuchins and macaques and six sessions of 2 h

each for orang-utans, gorillas and gibbons. Every 15 min,

sequences of grasping which lasted 5 min were analysed

to determine the area of the finger in contact with the

object by using frame-by-frame analysis in the labora-

tory. We obtained a minimum of 90 min of observation

of grasping behaviour for each chimpanzee, baboon,

macaque and capuchin, and 180 min for each orang-

utan, gorilla and gibbon.

Frame-by-frame analysis was performed with a Basler

camera (Basler, Ahrensburg, Germany), recording 250

images per second. Each prehension technique was

characterized by contacts between one or several lateral

or ventral areas of a minimum of two digits or the

complete palm. From this analysis, we determined five

categories of object prehension.

Size and nature of the objectsFor all primates except humans, the objects were small

and scattered on the ground; the objects involved

spherical cereals and fruits. In humans, the objects were

spherical pearls. It was necessary to standardize the

diameter and the volume in order to calibrate these

parameters according to the length of the hand of the

species studied. In this paper, we always presented

spherical objects to the animals and determined their

diameter. The diameter of the objects was calibrated

according to the length of the hand of the species. As we

knew the length of the hand of the smallest studied

species (76.2 ± 5.3 mm for capuchin) and the diameter

of the smallest object (3.0 ± 0.1 mm) grasped by this

species, we deduced the diameter of objects for other

species as follows (D = diameter, L = length, all units

in mm):

D object for species x¼L hand of the species x�3:0=76:2

For example, to calculate the diameter of objects to be

grasped by chimpanzees, we used the length of the

chimpanzee’s hand (235.0 mm) and that of the smallest

hand (the capuchins’ hand: 76.2 mm) and the diameter

of the smallest object (3.0 mm). In this example, Dxc

corresponds to the determined diameter of the small

object for chimpanzees (c). We calculated the following

value for objects in chimpanzees: Dxc is equal to 9.0 mm

(235.0 mm · 3.0 ⁄ 76.2). We followed the same method

to calculate the diameter of objects for each species

(Appendix S2).

Number of graspsA total of 5549 grasps were recorded for the eight studied

species (Table 1). The percentage of each prehension

category was calculated on the basis of the total number

of grasping observed in each species.

Morphometric dataMorphometric data were obtained from hand skeletons

belonging to the collection of the Museum National

d’Histoire Naturelle (Paris). Our sample consisted of 17

measurements of the hand of 26 taxa (Appendix S3). A

mean of 10 specimens per taxon (males and females) was

measured.

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Categories of contacts

Each of the six species of primates uses from 5 to 21 of 26

different modes of contacts between areas of digits and

the objects. This large number of contacts can be

classified into five main categories of grasping behaviour

(Table 1). In order to facilitate our comparison with the

previous literature, each category is named (Fig. 1) as

suggested by Napier (1956) and Jones-Engel & Bard

(1996):

Category 1: contact between the distal phalanx of the

thumb, the distal part of the index finger and

the object (precision).

Category 2: contact between the distal phalanx of at

least three fingers and the object (thumb-

distals).

Category 3: contact between the distal part of the thumb,

the lateral side of the middle and proximal

phalanges of the index finger and the object

(thumb-lateral).

Table 1 Use of the grasps from all categories in anthropoid species.

Species N Mean

Category 1

Precision

Category 2

Thumb-distals

Category 3

Thumb-lateral

Category 4

Without thumb

Category 5

Power

Homo sapiens (adults) 600 50.0 ± 0.0 81 ± 3.5 19 ± 2.2 0 ± 0 0 ± 0 0 ± 0

Homo sapiens (child) 450 50.0 ± 0.0 59 ± 4.3 34 ± 1.4 0 ± 0 0 ± 0 7 ± 1.5

Pan troglodytes 804 57.4 ± 4.9 32 ± 2.6 7 ± 0.7 38 ± 2.2 22 ± 3.1 1 ± 0.5

Pan paniscus * * 15 ± 1.7 1 ± 0.2 45 ± 4.0 39 ± 3.2 0 ± 0

Gorilla gorilla 600 200.0 ± 6.7 67 ± 4.4 2 ± 1.1 17 ± 2.0 12 ± 1.9 2 ± 0.3

Pongo pygmaeus 624 89.1 ± 4.7 29 ± 1.3 3 ± 1.3 33 ± 3.1 34 ± 2.0 1 ± 0.4

Hylobates lar 546 182.0 ± 5.3 5 ± 1.2 0 ± 0 95 ± 2.1 0 ± 0 0 ± 0

Papio papio 581 64.6 ± 5.9 71 ± 5.2 3 ± 2.0 24 ± 2.8 0 ± 0 2 ± 0.6

Macaca fuscata 667 74.1 ± 6.2 76 ± 3.9 1 ± 0.3 22 ± 2.4 0 ± 0 1 ± 0.4

Theropithecus gelada * * 77 ± 3.3 2 ± 1.2 18 ± 1.1 0 ± 0 3 ± 1.2

Cercocebus aterrimus * * 70 ± 4.6 0 ± 0 28 ± 1.7 0 ± 0 2 ± 0.6

Cebus apella 677 75.2 ± 7.0 80 ± 4.1 13 ± 2.1 2 ± 0.4 4 ± 1.6 1 ± 0.3

N, Number of grasps of small objects.

The mean number of observed grasps per individual for each species is also given. All other columns represent percentages.

*Data derived from the literature (Christel, 1993; Christel et al., 1998).

(e)

(a)

(c) (d)

(b)

Fig. 1 Definition of contacts (drawings modified from Schultz, 1969). (a) Precision (two digits). (b) Thumb-distal (3, 4 or 5 digits).

(c) Thumb-lateral. (d) Without thumb. (e) Power. The arrows indicate the possible contact between the thumb and the other digits (a–c), and

between the index and middle fingers (d). In the last prehension mode (e), the palm completely covers the object and the ventral surface of the

digits is also implicated in the grasping action. These surfaces are presented in black and the arrows indicate possible modes of contact

between the object and the digit surfaces. In the first example (a), the pad of the thumb and the pad or the extremity of the index can be

simultaneously in contact with the object (photographs: E. Pouydebat).

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Category 4: contact between one or several fingers,

except the thumb, and the object (without

thumb).

Category 5: contact between the palm, one or several

fingers and the object (power).

Data distribution and transformation

The length of the manus (LM) is used in the analyses

below to remove some of the body size effect on the

remaining characters. For all analyses, this character

(LM) was log-transformed because body size usually

follows a log-normal, rather than normal, distribution.

All other morphometric characters were divided by LM

before all the analyses below (Appendix S3).

Detection of phylogenetic signal

To determine whether or not the phylogeny needed to be

incorporated into the analyses, and whether or not

squared-change parsimony could be used to study char-

acter evolution, we performed two types of tests of

phylogenetic signal. The first one consists of comparing

the squared length of a character over the reference tree

to the squared length of multiple (in this case 10 000)

random trees. For quantitative characters optimized

through squared-change parsimony, branch length data

are critical. Thus, the most appropriate way to create

random trees is to reshuffle the terminal taxa on a tree of

fixed topology and branch lengths (Laurin, 2004; Laurin

et al., 2004). However, squared-change parsimony opti-

mization requires the same assumptions as independent

contrast analysis; thus, we checked if these assumptions

were met using the PDAP (Phenotypic Diversity Analysis

Programs) module for MESQUITEESQUITE (Midford et al., 2003).

This module performs four relevant tests. The first three

regress the absolute value of standardized contrast

against: (i) their expected standard deviation (the square

root of the sum of corrected branch lengths); (ii) the

estimated value of the base node; and (iii) the corrected

height of the base node. The fourth and last test is a

regression of the estimated value of the base node against

the corrected height of the base node. We performed all

these tests (four) for all characters (21) for all trees (five).

No corrections for multiple tests were made, which

makes our procedure more stringent by rejecting trees

which yield artefactual relationships which are signifi-

cant when taken in isolation, but which might no longer

be significant if such corrections were made. Further-

more, it is not clear if such corrections should be made

because these four tests evaluate different statistical

artefacts, and results for one character have no bearing

on other characters. Deviations from the assumptions

were detected in several cases; this prevented analyses of

the relevant characters on a given tree. To maximize the

number of tests that could be performed and to test the

presence of a phylogenetic signal, we produced four

alternative trees (trees 2–5 in Appendix S4) that derive

from our main tree. Tree 2 differs from tree 1 in having

older divergence dates for some nodes, especially among

hominoids (Fig. 2, grey). Tree 3 was produced by a

natural logarithmic transformation of the branch lengths

of tree 1. Tree 4 was produced by setting all branch

lengths to 1. Tree 5 is ultrametricized from tree 4. For the

behavioural data, the same trees were used, but taxa

with missing data were pruned from the trees. These

trees deviate increasingly from the starting tree that, we

believe, includes plausible divergence times; thus, for all

analyses, we used the tree with the lowest designator

possible (tree 1, and if not possible, tree 2, and so on). All

these trees can be used to the extent that ‘the statistical

adequacy of any proposed branch lengths should be

viewed as an empirical issue’ and ‘In general, any trans-

formation of possible use for tip data…might also be tried

for branch lengths’ (Garland et al., 1992: pp. 23–24).

A second set of tests of phylogenetic signal was

performed using phylogenetic eigenvector regression

(PVR) analysis (Diniz-Filho et al., 1998). This method

relies on a principal coordinate analysis of the phylo-

Fig. 2 Time-calibrated supertree of primates used in this study. Tree

1 is in black; tree 2, with older divergence dates in Catarrhini, is in

grey. This figure was produced from a pdf file generated by

MESQUITEESQUITE (Maddison & Maddison, 2006) and showing the tree in a

stratigraphic time scale displayed by Stratigraphic Tools (Josse et al.,

2006). The numbers next to the tree indicate the age (Ma); those

next to the stage names indicate their duration (Ma). [A colour

version of this figure is available online.]

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genetic distance matrix to extract eigenvectors that are

used in a standard linear regression against the character

of interest. The eigenvectors represent the position of the

taxa on the various principal coordinate axes. However,

for n taxa, n – 1 principal coordinate axes are produced,

and they cannot all be used in a linear regression analysis

or there would be no degrees of freedom left. The axes

we used were selected using a broken-stick model

(Diniz-Filho et al., 1998), because it would have taken

too long to test for a significant relationship between all

axes and all characters separately (21 characters and up

to 26 taxa yield 546 tests). Furthermore, none of the

behavioural characters exhibits a phylogenetic signal

according to the squared-change parsimony analysis (see

below), and that method is usually more powerful than

PVR (Cubo et al., 2005). Thus, the broken-stick model

was the only method applicable to all of our data. In all

our analyses of phylogenetic signal, only the first two

axes were used. They represent 60.7% of the phylo-

genetic variance.

The phylogenetic distance matrix was obtained from

tree 1 using the Stratigraphic Tools module (Josse et al.,

2006). The principal coordinate analysis was performed

in PROGICIELROGICIEL R (Casgrain et al., 2004). Linear regressions

were tested for statistical significance using 9999 per-

mutations of the dependent variables (here, the mor-

phometric or behavioural data) in PERMUTEERMUTE! (Casgrain,

2005). A regression is significant (at a 0.05 threshold

value) if fewer than 5% of the data sets have an R2

value at least as large as the original data set (the

original, unpermuted set is included). The advantage of

using permutations to test the significance of the

relationship is that this method requires far fewer

assumptions about the distribution of the data. Thus,

contrary to the other method, this test could be applied

to all characters.

Phylogenetically independent contrasts

We assessed correlations between the behavioural

(dependent) and morphometric (independent) charac-

ters using phylogenetically independent contrasts

(Felsenstein, 1985), whenever the assumptions of

that method were met on at least one of our trees. These

tests were performed using the PDAP module for

MESQUITEESQUITE (Midford et al., 2003). As for the test a

phylogenetic signal using squared-change parsimony,

we performed this test on the tree with the lowest

designator (tree 1 if possible; if not, tree 2, etc.) that gave

adequate contrast standardization for both characters

analysed.

Variance partitioning with phylogenetic eigenvectorregression

Correlations between the behavioural (dependent) and

morphometric (independent) characters were also tested

using variance partitioning with a PVR analysis (Diniz-

Filho et al., 1998; Desdevises et al., 2003). This method

incorporates the phylogeny into the analysis in the form

of principal coordinate axes, as explained in the section

on phylogenetic signal detection (above). We performed

some exploratory analyses (results not shown) in

PERMUTEERMUTE (Casgrain, 2005) to choose the characters to

analyse through PVR. Correlation between these char-

acters was then tested through variance partitioning with

PVR, using principal coordinate axes that were signi-

ficantly correlated with the dependent (behavioural)

characters. These axes were selected by performing a

simple regression of all axes against the relevant

behavioural characters, because in this case only three

characters are involved.

Linear regression models

Simple or multiple linear regressions were used to

produce inference models of the behavioural characters.

These models are based on the morphometric characters

that are significantly correlated with the behavioural

characters according to the variance partitioning analysis

with PVR (Appendix S5) or according to linear regres-

sions, but they were constructed without incorporation

of the phylogeny. This is unavoidable because principal

coordinate axes have no absolute meaning (they differ

when a taxon is added or removed, or if the topology or

branch length is changed), so incorporating them into

predictive models would preclude their use in palaeobi-

ological inference, which is self-defeating. These models

could not be used on some of the extinct taxa included in

our study because the relevant morphometric characters

are not known. To maximize the number of inferences

which could be drawn about these taxa, we built

additional inference models for several combinations of

these taxa and available osteological characters (Appen-

dix S6). For this purpose, we used a forward selection

procedure in PERMUTEERMUTE to select the characters, among

those that were significantly correlated with each other

according to the variance partitioning or the indepen-

dent contrast analyses. In two cases, to produce the

models, we had to extend character selection to other

characters (because extinct taxa are incompletely

known); in such cases, we used a forward selection

procedure in PERMUTEERMUTE (with p to enter of 0.1) to build

the model.

Results

Taxon-specific distribution of categories

The platyrrhine and all catarrhines were able to modulate

their grasping behaviour for small food items. However,

some clusters of species emerge for all categories of

contact. These groups can be compared on the basis of

the mean percentage (Table 1).

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From these data, five main conclusions can be drawn.

First, great apes (except humans) and capuchins use

grasping category 4 (without thumb), whereas humans

and other primates never do. All primates except

humans use the lateral part of their index (category 3,

thumb-lateral), whereas capuchins hardly ever do and

humans never do. Secondly, adult humans and capu-

chins are similar as regards a majority of grasping

categories. Thirdly, human children do not show clear

similarities with other primate species for any of the

grasping categories. Fourthly, cercopithecids (i.e. maca-

ques and baboons), capuchins and humans use the

precision grip most often (Table 1). Fifthly, humans

present some unique characteristics in their selection of

grasping categories. Human adults are the only primates

to use exclusively the tips of the fingers (precision and

thumb distals). Human children and capuchins are more

similar behaviourally to human adults than to other

primates in our sample, because they mainly use the tips

of their fingers (93%). One key result from our data is

that all species were able to grasp small objects with the

precision grip corresponding to the contact between the

tips of thumb and index finger. This applies even to

capuchins, although their thumb is only pseudo-oppos-

able.

Detection of phylogenetic signal

Globally, about 40% of the characters display a phylo-

genetic signal (Appendix S4). This proportion holds

when using both tests, but is affected by taxonomic

sampling; when only the 11 taxa for which behavioural

data are available are tested, this proportion decreases to

20%. This may explain why no phylogenetic signal was

found in the behavioural data using random taxon

reshuffling and squared-change parsimony or PVR

analysis using the first two principal coordinate axes

selected by the broken-stick model (Appendix S4).

However, when each axis was regressed separately

against the behavioural characters, axis 1 had a signif-

icant effect for precision, without thumb and power

grasp frequency.

Character correlation assessed using phylogeneticindependent contrasts

Only three of the behavioural characters were analysed

using independent contrasts because for the others, the

assumptions of that method were not met (Appendix S7).

Some of the morphometric characters are clearly corre-

lated with behavioural data. The behavioural character

‘precision’, involving the contact of the distal phalanges

of the thumb and the index, and the character ‘thumb-

lateral’, involving contact of the distal phalanx of the

thumb and the lateral side of the index, are correlated

with the length of the carpus and the first ray (the thumb

and its metacarpal). Power grasping is linked with second

and third digit length.

Character correlation assessed using variancepartitioning with PVR

The forward selection test in PERMUTEERMUTE (with a p to enter

of 0.1) resulted in only one or two morphometric

characters being selected for each behavioural character

(results not shown), which implies that grasping behav-

iour can be inferred fairly precisely using few morpho-

metric data. No principal coordinate axis was selected. An

additional (non-phylogenetic) test using simple linear

regressions confirms that all the selected characters are

correlated with behavioural characters and explain more

than 50% of the variance in the behavioural characters

(results not shown). In addition, variance partitioning

analyses of the characters which were correlated with at

least one of the phylogenetic principal coordinate axes

indicate that most of the explained variance is genuinely

explained by morphometry rather than by covariation

with the phylogeny (Table 2).

Linear regression models of inference

Inference models obtained through linear regressions

include one or two morphometric characters (Appendix

S5). Inferences were obtained from these models for

extant species in which morphometric data (but no

Table 2 Variance partitioning with PVR showing the correlation between behavioural (dependent) and the morphometric (independent)

characters that were selected by the forward selection procedure using linear regressions with permutations (Appendix 5) and the phylogenetic

principal coordinate axes (we included those that were correlated with behavioural characters based on several simple regressions with

permutations).

Dependent

character

Morphometric characters Phylogenetic axes

Identity

Portion of variance

explained (probability)

Variance explained by covariation

of morphometry and phylogeny Identity

Portion of variance

explained (probability)

Unexplained

variance

Precision 2, 4 0.4364 (0.103) 0.3125 1 0.0528 (0.509) 0.1984

Without thumb 5 0.3544 (0.017) 0.3682 1 0.0268 (0.307) 0.2506

Power 15 0.3404 (0.061) 0.3132 1 0.0540 (0.488) 0.2923

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behavioural data) are available (Appendix S8), and for

three extinct species (Table 3).

Discussion

Compilation of a time-calibrated tree

For many of the analyses performed below, a phylogeny

incorporating an estimate of branch lengths is needed.

Thus, we compiled a time-calibrated tree (branch lengths

reflect estimated evolutionary time). The topology fol-

lows Goodman et al. (2005). Divergence time estimates

are much more contentious because the affinities of

several primate species based on fragmentary material

are poorly constrained (Ross et al., 1998), and because

divergence time estimates based on molecular data are

often considerably older than the minimal times of

divergence based on fossils (see Marjanovic & Laurin,

2007; for a review). Estimates of divergence times based

on molecular data also often differ substantially between

studies; for instance, Arnason et al. (2000) estimated that

the divergence between strepsirhines and haplorhines at

about 90 Ma (in the Turonian, in the Early Upper

Cretaceous) and that the anthropoid radiation started at

70 Ma, whereas Yoder & Yang (2004) estimated these

events to have occurred at about 80 and 50 Ma, respec-

tively. Yoder & Yang (2004) furthermore estimate the

divergence between Lorisiformes and Lemuriformes at

70–75 Ma, but Roos et al. (2004) estimate it at about

60 Ma, although the oldest fossil in that clade dates from

the Priabonian (Stucky & McKenna, 1993: p. 757), no

more than 37.2 Ma, according to the geological time

scale of Gradstein et al. (2004). Given the poor fossil

record of (crown group) strepsirhines (Stucky &

McKenna, 1993: p. 757), the paleontological date here

is likely to seriously underestimate the actual divergence

dates within Strepsirhini. Considerable differences be-

tween molecular dates are not unexpected because

several methods can be used to obtain molecular dates.

The choice of the calibration date also influences the

results (Brochu, 2004a, b; Poux & Douzery, 2004;

Marjanovic & Laurin, 2007), and there are many other

pitfalls in such analyses (Shaul & Graur, 2002; Graur &

Martin, 2004; Marjanovic & Laurin, 2007). Furthermore,

evolutionary rates are quite variable in primates (Gross-

man et al., 2004; Steiper et al., 2004), which makes

molecular dating more difficult.

For all clades, we have adopted a compromise that uses

minimal divergence ages from the fossil record in the

taxa where this record is reasonably abundant, and

molecular ages for taxa such as Strepsirhini, for which

the fossil record is poor. When using molecular data, we

have tried to use studies that obtained ages compatible

with the fossil record. We assembled the tree in

MESQUITEESQUITE (Maddison & Maddison, 2006) using the

Stratigraphic Tools module (Josse et al., 2006). To facil-

itate comparisons with palaeontological literature, when-

ever molecular dates fall close to geological stage

boundaries, we used the age of the boundary itself

(Fig. 2); this also facilitates tree manipulation in Strati-

graphic Tools (Josse et al., 2006). More information about

individual divergence ages can be found in Appendix S9.

Ontogenetic and taxonomic distribution ofgrasping behaviours

The data presented above show that precision grasping

can be used by all arboreal and terrestrial primate species

in our study. Indeed, the precision grip was recently

reported in capuchins (Spinozzi et al., 2004). However,

according to that report, this grasping technique was less

frequently used by immature individuals. In our study,

all individuals were observed in their social groups, and

we did not observe any obvious effect of ontogenetic age

for this behaviour (data not shown).

Comparisons between great apes and human children

refute the idea that they have similar sensorimotor

organization (Parker & Gibson, 1977). In our study, this

similarity is not great. Categories of grasping used for

small objects differ strongly between human children and

great apes. Great apes use precision grips and the distal

phalanges of their digits less often than children. In

addition, they use the lateral side of their index and the

grip without thumb, contrary to children. These differ-

ences between great apes and children may be explained

by the neural and morphological variability existing

between humans and the other species, regardless of

their age. Finally, the comparison between great apes and

human adults does not show strong similarities. Human

adults use precision grips with small objects and the distal

phalanges of their digits to grasp large objects much more

often.

Relationship between morphometry and graspingbehaviour

The results of this study refute some well-established

ideas about the relationship between morphometry and

Table 3 Inferred behaviour frequency (%) of extinct primate taxa

based on linear regression inference models (Appendix 5).

Taxon Precision

Thumb-

distals

Thumb-

lateral

Without

thumb Power

Australopithecus 58 2 35 )9 (0) 1

Oreopithecus 46 26 18 5 2

Proconsul 76 7 28 13 1

As frequency of a behaviour cannot exceed the interval 0–100%,

values outside this interval represent modelling errors and should be

interpreted as implying values close to the nearest bound (given in

parentheses). Note that as these are inferences, the sums of

percentages on a given line do not necessarily add up to 100% (the

difference between the total and 100% represents modelling errors).

1738 E. POUYDEBAT ET AL.

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prehensile behaviour. Our data show that great apes

use precision grips less often than cercopithecoids when

handling small objects and that the contrary pattern is

observed when handling large objects (Pouydebat et al.,

2006a). Furthermore, Pongo and Pan use the grip

without the thumb, contrary to cercopithecoids. These

differences are partly explained by morphometrical data

such as the shorter thumb of great apes (Marzke et al.,

1992), as shown by our analyses (Appendix S7,

precision and characters 3 and 5; Table 2, without

thumb and character 5). Therefore, the length of the

thumb, including the first metacarpal, is an important

morphometrical character in the behaviour of precision

grasp, as previously suggested (Napier, 1956; Schultz,

1969; Susman, 1989). These morphometrical parame-

ters are also negatively correlated with the behavioural

character ‘thumb-lateral’ (Appendix S7), involving the

contact of the distal phalanx of the thumb and the

lateral side of the index. Therefore, the length of the

first ray does not reflect precision grasping only.

Other morphometrical data are specifically correlated

with a single behavioural character. For instance,

the power grasping behaviour, involving the palm of

the hand during the grasp, is strongly correlated with the

lengths of the digits one to three (Appendix S7, power vs.

characters 7–9, 12, 15). The length of digits 2 and 3 is

correlated only with power-grasping (among the behav-

iours studied here); short index and third digits seem to

favour power-grasping.

A few species show prehensile patterns which could

not have been inferred from their hand morphology. For

instance, gorillas show a high percentage of use of the

precision grip in spite of their short thumb (Pouydebat

et al., 2006a). This reflects the fact that the length of the

thumb does not explain all the variance in use of the

precision grip. A quantitative, statistical approach is

required because of the complexity of the relationship

between morphometry and prehensile behaviour.

Finally, we wonder why carpus length is correlated

with precision and thumb-lateral grips. It would be

interesting to test if this can be explained by soft

anatomy, such as muscle or tendon morphology, or by

locomotory behaviour (such as arboreality).

Unexpected similarities between capuchin andhuman prehensile behaviours

Our study reveals similarities in prehensile behaviours

between capuchins and humans. Capuchins use preci-

sion and thumb-distal grips as often as human adults.

Similar to humans, capuchin monkeys almost exclusively

used the distal phalanges of their digits to grasp small

objects. These results can be compared with those of

Spinozzi et al. (2004), who observed a wide variety of

grasping patterns in capuchins. These include various

forms of precision and power grips. Contrary to our

results, Spinozzi et al. (2004) reported that capuchins use

precision and power grips with the same frequency to

grasp small food items. We found that they opted more

often for precision grips (almost 80%). This difference

between our results could be due to the population and

individual variability or the protocol of observation

which was not the same. Capuchins display a wide

variety of prehensile abilities that confirm their capacity,

apparently atypical among New World monkeys, to use

their hands dexterously during extractive foraging and

object manipulation (Fragaszy et al., 1991; Fragaszy &

Boinski, 1995; Christel & Fragaszy, 2000; Pouydebat

et al., 2006b), although they do not possess the true

opposable thumb typical of catarrhine primates.

Inferences about the grasping behaviour of extinctprimates

The inference of grasping behaviour from morphological

analyses of the hands of fossils is a complex problem.

Some authors opposed the hand of extant apes to the

hand of humans and argued that extant apes are unable

to grasp objects with a precision grip or pad-to-pad

gripping. However, many extant ape species use preci-

sion gripping (Christel, 1993; Pouydebat, 2004) without

meeting all the morphological criteria usually considered

to be linked with precision gripping. We have shown that

precision gripping can be performed by hands showing a

greater morphological diversity than previously thought.

Our sampling of behavioural characters in anthropoids

largely restricts our discussion of their possible evolution

within this clade, as suggested by the extant phylogenetic

bracket principle (Witmer, 1995), which was extended

into the context of continuous characters by Laurin et al.

(2004). The absence of a phylogenetic signal in the

behavioural characters (Appendix S4, characters 17–21)

precludes tracing their history over the tree using

optimization procedures because the results would not

be reliable (Laurin, 2004). This limitation may reflect the

relatively low number of taxa for which behavioural data

are available as analyses of our data with the same

taxonomic sampling show a similar absence of a phylo-

genetic signal in most morphometric characters (Appen-

dix S4, central columns). Thus, it might be possible to

reconstruct the evolution of these behavioural characters

by sampling the same clade more densely.

Another possibility is to use the linear regression

inference models that we have produced (Appendix S5)

to infer the behaviour of extinct primate species (Table 3):

A. afarensis, O. bambolii and P. africanus (Fig. 3). Thus, we

can infer that the Plio-Pleistocene hominin A. afarensis

(3–4 Ma old) from Hadar (Ethiopia) exhibited frequent

precision behaviour (Table 3). The linear regression

inference for thumb-distals behaviour in A. afarensis

suggests the infrequent occurrence of this behaviour.

Results about precision behaviour are close to those

obtained by Marzke (1997) and Panger et al. (2002); on

the contrary, several authors suggested that A. afarensis

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use power grasping most often (Bush et al., 1982; Stern &

Susman, 1983; Susman, 1991, 1994), which we infer to

have occurred infrequently. Australopithecus may share

with humans the absence of without-thumb behaviour,

which may be a synapomorphy of Australopithecus and

Homo among hominoids (although cercopithecoids show

a convergent similarity).

The Miocene ape Oreopithecus may have exhibited

slightly less precision behaviour than Australopithecus, but

like the latter, it resorted to that behaviour much more

often than the power grip, which was rarely displayed.

This result is congruent with the assessment of Moya-

Sola et al. (1999). On the other hand, Susman (2004)

suggested that O. bambolii emphasized the power grip

over the precision grip. Similar to most extant hominoids

and Proconsul, but unlike Homo and Australopithecus,

Oreopithecus may have displayed the without-thumb

behaviour (Table 3).

The linear regression inference models suggest that the

Early Miocene (Burdigalian) stem-hominoid P. africanus

(16–18 Ma) from Kenya used the precision grip fre-

quently (Table 3) and thumb-distals grip more rarely.

P. africanus resorted to thumb-lateral grip relatively

infrequently and used the without-thumb grip even less

frequently. These results about P. africanus are very

different from those published in the literature, which

suggest that P. africanus did not use a precision grip

(Napier & Davis, 1959; McHenry, 1983; Walker & Pick-

ford, 1983; Begun et al., 1994). The widespread distribu-

tion of the precision grip in the primate species sampled in

this study support our palaeobiological inferences.

The evolution of grasping behaviour

The classical model proposes a late appearance of

precision grasping, often considered unique to hominids.

Napier (1956, 1960) suggested that grasping objects with

precision requires opposability of the thumb and favour-

able relative lengths of digits I and II. Furthermore, some

authors suggest that precision grasping is linked with

brain organization and the development of cognitive

processes (Napier, 1960; Jones-Engels & Bard, 1996).

Under such hypotheses, hominoid fossils presenting

morphological characters associated with precision grasp-

ing have been argued to be able to use tools (Susman,

1989; Marzke, 1997). The data presented in this paper

refute this evolutionary scenario because species with

highly different hand morphologies and brain structure

use a precision grip. The evolution of grasping abilities in

platyrrhines and catarrhines is much more complex than

a simple trend from power to precision grasping. Indeed,

several species (i.e. P. troglodytes, P. pygmaeus, M. fuscata,

P. papio and C. apella) use the tips of their thumb and

index finger for grasping small objects, demonstrating

that morphological criteria previously used for deducing

grasping ability are not reliable (Susman, 1998). Fur-

thermore, in our quantitative analysis based on the

percentages of use of five simplified categories of grasp-

ing, capuchins are similar to humans (mainly adult

humans) even though they possess a pseudo-opposable

thumb (rather than a truly opposable thumb, capable of

adduction and rotation of its carpo-metacarpus joint).

This functional similarity of two species which diverged

about 34 Ma (Fig. 2) is surprising.

Our findings are in concordant with the evolutionary

model according to which a primitive power grasp was

subsequently modified into a derived precision grasp

(Susman, 1979), although this transition occurred before

the appearance of hominoids. Our data suggest that both

behaviours were already present in the first anthropoids.

It would be interesting to obtain some data on Tarsius and

strepsirhines to determine when precision grasping

appeared.

All our results suggest that grasping has evolved in a

more complex manner than previously realized. Our

observations show that precision grip is far more wide-

spread than previously thought. This is coherent with the

findings that skilled forelimb movements are also present

in other mammals (Ivanco et al., 1996; Whishaw et al.,

1998) and even in amphibians (Gray, 1997). These

movements may not be homologous and represent

convergent evolution of motor patterns that superficially

resemble reaching (Bracha et al., 1990). However, the

similarities in reaching among different mammalian taxa

suggest that the movements are homologous within

mammals. It would be interesting to apply comparative

methods to a far greater range of taxa to assess broader-

scale evolutionary patterns of various grip patterns.

Acknowledgments

We would like to thank the Foundation Singer-Polignac

for their financial support, P. Piras for helping us with

Fig. 3 Time-calibrated supertree of extant and extinct hominoids

represented in this study. The numbers next to the tree indicate the

age (Ma); those next to the stage names indicate their duration (Ma).

For more information, see Fig. 2. [A colour version of this figure is

available online.]

1740 E. POUYDEBAT ET AL.

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some statistical analyses, D. Marjanovic for numerous

stylistic corrections, and all the staff of the Zoo of Beauval

and of the Monkey Valley (France).

References

Altmann, G. 1974. Observational study of behavior. Sampl.

Methods Behav. 49: 227–267.

Arnason, U., Gullberg, A., Burguete, A. S. & Janke, A. 2000.

Molecular estimates of primate divergences and new hypo-

theses for primate dispersal and the origin of modern humans.

Hereditas 133: 217–228.

Begun, D. R., Teaford, M. F. & Walker, A. 1994. Comparative

and functional anatomy of Proconsul phalanges from the

Kaswanga Primate Site, Rusinga Island, Kenya. J. Hum. Evol.

26: 89–165.

Begun, D. R., Ward, C. V. & Rose, M. D. 1997. Function, Phylogeny

and Fossils: Miocene Hominoid Origins and Adaptations. Plenum

Press, New York.

Boesch, C. & Boesch, H. 1990. Tool use and tool making in wild

chimpanzees. Folia Primatol. 54: 86–99.

Bracha, V., Zhuravin, I. A. & Burges, J. 1990. The reaching

reaction in the rat: a part of the digging pattern? Behav. Brain

Res. 36: 53–64.

Brochu, C. A. 2004a. Calibration age and quartet divergence

date estimation. Evolution 58: 1375–1382.

Brochu, C. A. 2004b. Patterns of calibration age sensitivity with

quartet dating methods. J. Paleontol. 78: 7–30.

Bush, M., Lovejoy, C., Johanson, D. & Coppens, Y. 1982.

Hominid carpal, metacarpal, and phalangeal bones recovered

from the Hadar Formation: 1974–1977 collections. Am. J. Phys.

Anthrop. 57: 651–677.

Casgrain, P. 2005. Permute! [www document]. URL http://www.

bio.umontreal.ca/Casgrain/en/labo/permute/index.html.

Casgrain, P., Legendre, P. & Vaudor, A. 2004. The R Package for

Multidimensional and Spatial Analysis [www document]. URL

http://www.fas.umontreal.ca/BIOL/Casgrain/en/labo/R/v4/

progress.html.

Christel, M. 1993. Grasping techniques and hand preference in

Hominoidea. In: Hands of Primates (H. Preuschoft & D. Chivers,

eds), pp. 91–108. Springer, Berlin.

Christel, M. I. & Fragaszy, D. 2000. Manual function in Cebus

apella. Digital mobility, preshaping, and endurance in repet-

itive grasping. Int. J. Primatol. 21: 697–719.

Christel, M., Kitzel, S. & Niemitz, C. 1998. How precisely do

bonobos (Pan paniscus) grasp small objects? Int. J. Primatol. 19:

165–194.

Clark, J. D. 1993. Stone artifact assemblages from Members 1–3

Swartkrans Cave. In: Swartkrans: A Cave’s Chronicle of Early

Man (C. K. Brain, ed.), pp. 167–194. Transvaal Museum,

Pretoria.

Cubo, J., Ponton, F., Laurin, M., de Margerie, E. & Castanet, J.

2005. Phylogenetic signal in bone microstructure of saurop-

sids. Syst. Biol. 54: 562–574.

Desdevises, Y., Legendre, P., Azouzi, L. & Morand, S. 2003.

Quantifying phylogenetically structured environmental vari-

ation. Evolution 57: 2467–2652.

Diniz-Filho, J. A. F., de Sant’Ana, C. E. R. & Bini, L. M. 1998. An

eigenvector method for estimating phylogenetic inertia.

Evolution 52: 1247–1262.

Felsenstein, J. 1985. Phylogenies and the comparative method.

Am. Nat. 125: 1–15.

Folinsbee, K. E. & Brooks, D. R. 2007. Miocene hominoid

biogeography: pulses of dispersal and differentiation. J. Bio-

geogr. 34: 383–397.

Fragaszy, D. M. & Boinski, S. 1995. Patterns of individual

diet choice and efficiency of foraging in wedge-capped capuchin

monkeys (Cebus olivaceus). J. Comp. Psychol. 109: 339–348.

Fragaszy, D. M., Baer, J. & Adams-Curtis, L. 1991. Behavioral

development and maternal care in tufted capuchins (Cebus

apella) and squirrel monkeys (Saimiri sciureus) from birth

through seven months. Dev. Psychobiol. 24: 375–93.

Fragaszy, D., Visalberghi, E. & Fedigan, L. 2004. The Complete

Capuchin. The Biology of the Genus Cebus. Cambridge University

Press, Cambridge, UK.

Garland, T. Jr, Harvey, P. H. & Ives, A. R. 1992. Procedures for

the analysis of comparative data using phylogenetically

independent contrasts. Syst. Biol. 41: 18–32.

Godinot, M. & Beard, K. C. 1993. A survey of fossil primate

hands. In: Hands of Primates (H. Preuschoft & D. J. Chivers,

eds), pp. 335–378. Springer-Verlag, Vienna.

Godinot, M., Laneque, L., Verdier, R. & Apriletti, K. 1997.

Quantitative morphology of Eocene primates compared to

living primates: examples of current studies. Geobios 30: 271–

281.

Goodman, M., Grossman, L. I. & Wildman, D. E. 2005. Moving

primate genomics beyond the chimpanzee genome. Trends

Genet. 21: 511–517.

Gradstein, F. M., Ogg, J. G. & Smith, A. G. (eds) 2004. A Geologic

Time Scale 2004. Cambridge University Press, Cambridge.

Graur, D. & Martin, W. 2004. Reading the entrails of chickens:

molecular timescales of evolution and the illusion of precision.

Trends Genet. 20: 80–86.

Gray, L. A. 1997. Evolution of forelimb movement patterns

for prey manipulation in anurans. J. Exp. Zool. 277: 417–424.

Grossman, L. I., Wildman, D. E. & Schmidt, T. R. 2004.

Accelerated evolution of the electron transport chain in

anthropoid primates. Trends Genet. 20: 578–585.

Ivanco, T. L., Pellis, S. M. & Whishaw, I. Q. 1996. Skilled

forelimb movements in prey catching and reaching by rats

(Rattus norvegicus) and opossums (Monodelphis domestica): rela-

tions to anatomical differences in motor systems. Behav. Brain

Res. 79: 163–181.

Iwaniuk, A. N. & Whishaw, I. Q. 2000. On the origin of skilled

forelimb movements. Trends Neurosci. 23: 372–376.

Jones-Engel, L. & Bard, K. A. 1996. Precision grips in young

chimpanzees. Am. J. Primatol. 39: 1–15.

Josse, S., Moreau, T. & Laurin, M. 2006. Stratigraphic Tools for

Mesquite. [Computer program]. URL http://www.mesquite

project.org/packages/stratigraphicTools/.

Laurin, M. 2004. The evolution of body size, Cope’s rule and the

origin of amniotes. Syst. Biol. 53: 594–622.

Laurin, M., Girondot, M. & Loth, M.-M. 2004. The evolution of

long bone microanatomy and lifestyle in lissamphibians.

Paleobiology 30: 589–613.

Lehner, P. N. 1996. Handbook of Ethological Methods. Cambridge

University Press, Cambridge, UK.

Maddison, W. P. & Maddison, D. R. 2006. Mesquite: a modular

system for evolutionary analysis, Version 1.1. [Computer

program]. URL http://www.mesquiteproject.org.

Marjanovic, D. & Laurin, M. 2007. Fossils, molecules, divergence

times, and the origin of lissamphibians. Syst. Biol. 56: 369–388.

Marzke, M. W. 1997. Precision grips, hand morphology and

tools. Am. J. Phys. Anthrop. 102: 91–110.

Evolution of grasping among anthropoids 1741

ª 2 0 0 8 T H E A U T H O R S . J . E V O L . B I O L . 2 1 ( 2 0 0 8 ) 1 7 3 2 – 1 7 4 3

J O U R N A L C O M P I L A T I O N ª 2 0 0 8 E U R O P E A N S O C I E T Y F O R E V O L U T I O N A R Y B I O L O G Y

Marzke, M. W., Wullstein, K. L. & Viegas, S. F. 1992. Evolution

of the power grip and its morphological correlates in homi-

nids. Am. J. Phys. Anthrop. 89: 283–298.

McHenry, H. M. 1983. The capitate of Australopithecus afarensis

and A. africanus. Am. J. Phys. Anthrop. 62: 187–198.

Midford, P., Garland, T. J. & Maddison, W. P. 2003. PDAP Package

for Mesquite. [Computer program]. URL http://mesquiteproject.

org/pdap_mesquite/index.html.

Moya-Sola, S., Kohler, M. & Rook, L. 1999. Evidence of

hominid-like precision grip capability in the hand of the

Miocene ape Oreopithecus. Proc. Natl. Acad. Sci. USA 96: 313–

317.

Napier, J. R. 1956. The prehensile movements of the human

hand. J. Bone Joint Surg. 38B: 902–913.

Napier, J. R. 1960. Studies of the hands of living primates. Proc.

Zool. Soc. London 134: 647–657.

Napier,J.R.1980.Hands.PrincetonUniversityPress,Princeton,NJ.

Napier, J. & Davis, P. 1959. The forelimb skeleton and

associated remains of Proconsul africanus. Fossil Mam. Afr. 16:

1–70.

Panger, M., Brooks, A. & Richmond, B. 2002. Wood, older than

the Oldowan? Rethinking the emergence of hominin tool use.

Evol. Anthrop. 11: 235–245.

Parker, S. T. & Gibson, K. R. 1977. Object manipulation, tool

use, and sensorimotor intelligence as feeding adaptations in

cebus monkeys and great apes. J. Hum. Evol. 6: 623–641.

Poux, C. & Douzery, E. J. P. 2004. Primate phylogeny,

evolutionary rate variations, and divergence times: a contri-

bution from the nuclear gene IRBP. Am. J. Phys. Anthrop. 124:

1–16.

Pouydebat, E. 2004. La prehension chez les Primates: approches

ethologique, biomecanique et morphometrique. Ph.D. Thesis, at the

Museum National d’Histoire Naturelle, Paris, 300 p.

Pouydebat, E., Berge, C., Gorce, P. & Coppens, Y. 2005. Use and

manufacture of tools to extract food by captive Gorilla

gorilla gorilla: experimental approach. Folia Primatol. 76: 180–

183.

Pouydebat, E., Berge, C., Gorce, P. & Coppens, Y. 2006a. La

prehension chez les Primates: precision, outils et perspectives

evolutives. C. R. Palevol. 5: 597–602.

Pouydebat, E., Gorce, P., Coppens, Y. & Bels, V. 2006b. Substrate

optimisation in nut cracking by capuchin monkeys. Am. J.

Primatol. 68: 1017–1024.

Roos, C., Schmitz, J. & Zischler, H. 2004. Primate jumping genes

elucidate strepsirrhine phylogeny. Proc. Natl Acad. Sci. USA

101: 10650–10654.

Ross, C., Williams, B. & Kay, R. F. 1998. Phylogenetic analysis of

anthropoid relationships. J. Hum. Evol. 35: 221–306.

Schultz, A. H. 1969. The Life of Primates. Weidenfeld and

Nicolson, London, 341 p.

Shaul, S. & Graur, D. 2002. Playing chicken (Gallus gallus):

methodological inconsistencies of molecular divergence date

estimates due to secondary calibration points. Gene 300: 59–61.

Spinozzi, G., Truppa, V. & Lagana, T. 2004. Grasping behavior in

tufted capuchin monkeys (Cebus apella): grip types and manual

laterality for picking up a small food item. Am. J. Phys. Anthrop.

125: 30–41.

Steiper, M. E., Young, N. M. & Sukarna, T. Y. 2004. Genomic

data support the hominoid slowdown and an Early Oligocene

estimate for the hominoid-cercopithecoid divergence. Proc.

Natl Acad. Sci. USA 101: 17021–17026.

Stern, J. & Susman, R. 1983. The locomotor anatomy of

Australopithecus afarensis, Am. J. Phys. Anthrop. 60: 279–317.

Stucky, R. K. & McKenna, M. C. 1993. Mammalia. In: The Fossil

Record 2 (J. M. Benton, ed.), pp. 739–771. Chapman & Hall,

London.

Susman, R. L. 1979. Comparative and functional morphology of

hominoid fingers. Am. J. Phys. Anthrop. 50: 215–236.

Susman, R. L. 1989. New hominid fossils from the Swartkrans

formation: postcranial specimens. Am. J. Phys. Anthrop. 79:

451–474.

Susman, R. L. 1991. Who made the Oldowan tools? Fossil

evidence for tool behavior in Plio-Pleistocene hominids.

J. Anthrop. Res. 47: 129–149.

Susman, R. L. 1994. Fossil evidence for early hominid tool use.

Science 265: 1570–1573.

Susman, R. L. 1998. Hand function and tool behavior in early

hominids. J. Hum. Evol. 35: 23–46.

Susman, R. L. 2004. Oreopithecus bambolii: an unlikely case of

hominidlike grip capability in a Miocene ape. J. Hum. Evol. 46:

105–117.

Tuttle, R. H. 1965. A Study of the Chimpanzee Hand with Comments

on Hominoid Evolution. University of California, Berkeley, CA,

526 p.

Walker, A. C. & Pickford, M. 1983. New postcranial fossils of

Proconsul africanus and Proconsul nyanzae. In: New Interpretations

of Ape and Human Ancestry (R. L. Ciochon & R. S. Corruccini,

eds), pp. 325–351. Plenum Press, New York.

Whishaw, I. Q., Sarna, J. R. & Pellis, S. M. 1998. Rodent-typical

and species-specific limb use in eating: evidence for specialized

paw use from a comparative analysis of ten species. Behav.

Brain Res. 96: 79–91.

Witmer, L. M. 1995. The extant phylogenetic bracket and the

importance of reconstructing soft tissues in fossils. In:

Functional Morphology in Vertebrate Paleontology, Vol. 1 (J. J.

Thomason, ed.), pp. 19–33. Cambridge University Press, New

York.

Yoder, A. D. & Yang, Z. 2004. Divergence dates for Malagasy

lemurs estimated from multiple gene loci: geological and

evolutionary context. Mol. Ecol. 13: 757–773.

Received 28 March 2008; revised 18 June 2008; accepted 23 June 2008

Supporting information

Additional supporting information may be found in the

online version of this article:

Appendix S1 Animals observed.

Appendix S2 Diameter of the objects for the studied

species.

Appendix S3 Matrix of morphometric (1–16) and

behavioural (17–21) characters used in this study.

Appendix S4 Phylogenetic signal in the characters.

Appendix S5 General linear regression inference mod-

els for the behavioural characters.

Appendix S6 Specific linear regression inference mod-

els for the behavioural characters.

Appendix S7 Correlation between behavioural (depen-

dent) and morphometric (independent) characters

assessed using independent contrasts.

1742 E. POUYDEBAT ET AL.

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Appendix S8 Inferred behavioural character values

for extant primate taxa for which such data are unavailable

but for which relevant morphometric data are known.

Appendix S9 Notes about the divergence dates used to

compile the time-calibrated supertree.

Please note: Wiley-Blackwell are not responsible for

the content or functionality of any supporting materials

supplied by the authors. Any queries (other than missing

material) should be directed to the corresponding author

for the article.

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