Early Origin for Human-Like Precision Grasping: A
Comparative Study of Pollical Distal Phalanges in Fossil
Hominins
Sergio Almécija1*, Salvador Moyà-Solà2, David M. Alba1
1 Institut Català de Paleontologia, Universitat Autònoma de Barcelona, Cerdanyola del Vallès (Barcelona), Spain, 2 ICREA at Institut Català de Paleontologia and Unitat
d’Antropologia Biològica (Dept. BABVE), Universitat Autònoma de Barcelona, Cerdanyola del Vallès (Barcelona), Spain
Abstract
Background: The morphology of human pollical distal phalanges (PDP) closely reflects the adaptation of human hands for
refined precision grip with pad-to-pad contact. The presence of these precision grip-related traits in the PDP of fossil
hominins has been related to human-like hand proportions (i.e. short hands with a long thumb) enabling the thumb and
finger pads to contact. Although this has been traditionally linked to the appearance of stone tool-making, the alternative
hypothesis of an earlier origin—related to the freeing of the hands thanks to the advent of terrestrial bipedalism—is also
possible given the human-like intrinsic hand proportion found in australopiths.
Methodology/Principal Findings: We perform morphofunctional and morphometric (bivariate and multivariate) analyses of
most available hominin pollical distal phalanges, including Orrorin, Australopithecus, Paranthropous and fossil Homo, in order
to investigate their morphological affinities. Our results indicate that the thumb morphology of the early biped Orrorin is
more human-like than that of australopiths, in spite of its ancient chronology (ca. 6 Ma). Moreover, Orrorin already displays
typical human-like features related to precision grasping.
Conclusions: These results reinforce previous hypotheses relating the origin of refined manipulation of natural objects–not
stone tool-making–with the relaxation of locomotor selection pressures on the forelimbs. This suggests that human hand
length proportions are largely plesiomorphic, in the sense that they more closely resemble the relatively short-handed
Miocene apes than the elongated hand pattern of extant hominoids. With the advent of terrestrial bipedalism, these hand
proportions may have been co-opted by early hominins for enhanced manipulative capabilities that, in turn, would have
been later co-opted for stone tool-making in the genus Homo, more encephalized than the previous australopiths. This
hypothesis remains may be further tested by the finding of more complete hands of unequivocally biped early hominins.
Citation: Almécija S, Moyà-Solà S, Alba DM (2010) Early Origin for Human-Like Precision Grasping: A Comparative Study of Pollical Distal Phalanges in Fossil
Hominins. PLoS ONE 5(7): e11727. doi:10.1371/journal.pone.0011727
Editor: David S. Strait, University at Albany, State University of New York (SUNY), United States of America
Received May 5, 2010; Accepted June 27, 2010; Published July 22, 2010
Copyright: ß 2010 Almécija et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This research has been supported by the Generalitat de Catalunya (predoctoral fellowship 2006 FI 00065 and travel grant 2008 BE1 00370 to S.A., and
2009 SGR 754 GRC), the U.S. National Science Foundation under NSF Award #BCS-0321893, the European Commission’s Research Infrastructure (SYNTHESYS
project grant to S.A.), and the Spanish Ministerio de Ciencia e Innovación (CGL2008-00325/BTE, and RYC-2009-04533 to D.M.A.). The funders had no role in study
design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: sergi.almecija@icp.cat
[3–4]. These include the pronounced insertion for the flexor pollicis
longus (FPL), with a marked asymmetry towards the radial side; the
presence of an ungual fossa; and the occurrence of dissymmetric
ungual spines, with a prominent ulnar one (Figure 1). The
asymmetries of the FPL insertion and the ungual spines are the
osteological correlates of the interphalangeal joint configuration of
the human thumb, in which flexion is accompanied by pronation,
so that the pulp of the thumb faces that of the remaining fingers.
This provides the maximum contact surface with the objects being
manipulated. The presence in humans of ungual spines and
ungual fossa are indicative of a fully compartmentalized digital
pulp, with a fatty and mobile proximal portion (related to the
ungual fossa) as well as a large and more or less static distal part
(related to the distal tuberosity; [3–4]). The presence of these two
different pulps, each with distinctive properties, ensures an
adequate friction and accommodation of the object between the
Introduction
One of the hallmarks of humankind is the possession of a
complex repertoire of manual grips [1–2]. In humans, the thumb
always plays a central role, being involved in almost all possible
prehensile typologies [1–4]. This is possible thanks to human
intrinsic manual proportions, i.e. a long thumb relative to the rest
of the hand. On the contrary, extant apes possess relatively long
hands with a short thumb, in which the musculature is poorly
developed [1–2,5]. The most refined expression of human
manipulation is attained during pad-to-pad precision grasping,
which consists in the opposition of the proximal pulp of the thumb
against that of one or more fingers ([3]; see Figure 1). This
capability is reflected in the morphology of the distal phalanges,
especially in the pollical distal phalanx (PDP), which shows specific
features related to the soft tissues involved in precision grasping
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Origin of Precision Grasping
Figure 1. Modern human thumb and index finger (right hand) during pad-to-pad precision grasping in ulnar view. The box shows the
anatomy of the pollical distal phalanx and its relationship with soft structures related to refined manipulation: a huge proximopalmar fossa (orange),
associated with a palmarly protruding ridge (red) for insertion of the flexor pollicis longus; a compartmentalized digital pulp to accommodate the
shape of the object being manipulated; this is reflected in the presence of an ungual fossa (green), associated to the large and mobile proximal pulp,
as well as a wide apical tuberosity associated with the smaller and less mobile distal pulp; and finally, the ungual spines (yellow), where the collateral
intraosseous ligaments that sustain the nail bed insert.
doi:10.1371/journal.pone.0011727.g001
In order to test this hypothesis, and given the tight relationship
between the anatomy of the PDP and refined manipulation in
modern humans, we provide a morphofunctional analysis of this
bone in selected fossil hominins—including the early biped Orrorin
tugenensis (ca. 6 Ma; [16–17])—as compared to extant apes and
humans. A principal components analysis (PCA) based on shape
variables of the PDP is further provided in order to compare the
main proportions of this bone in extant great apes, humans and
fossil hominins, as well as ratios of relative phalangeal robusticity.
The presence of anatomical traits functionally related to pad-topad precision grasping in the PDPs of early hominins would
suggest that these taxa also displayed human-like hand length
proportions for enabling the contact between the pulps (or pads) of
the thumb with those of one ore more of the remaining fingers [4].
However, more complete fossil hands of these early hominins
would be required in order to unequivocally confirm this
prediction. On the contrary, the latter would be falsified if fossil
taxa displaying the refined manipulation traits on their PDPs
together with relatively long hands and short thumbs were found
in the future.
pulp of the thumb and those of the fingers during precision
grasping (Figure 1). Furthermore, the possession of a wide apical
tuberosity is correlated with the presence of pulp that is also wide
[6].
Humans also display a characteristic FPL insertion, which
protrudes palmarly as a distinct bony element that is visible in
lateral view (Figures 1 and 2; [7] his Figure 4). Exclusively among
extant primates, humans display the complete set of anatomical
traits in their PDPs, which have been related to the presence of a
relatively long and powerful thumb, able to contact the proximal
pulp of the other fingers ([4]; Figure 1). Most previous studies
have focused on the functional relationship between the
anatomical traits discussed above and stone tool-making in PlioPleistocene hominins [3–4,8–9]. Furthermore, some studies
equated precision grasping—inferred from PDP anatomy— with
stone tool-making, thus favoring the view that the evolution of the
human hand was mainly related the selective pressures posed by
the latter behavior [7,10–11]. However, the human-like manual
proportions displayed by australopiths [12–13], well before the
advent of stone tool-making, would contradict the former
hypothesis. In fact, ever since Darwin [14] it has been
hypothesized that the origin of bipedalism was related to the
freeing of the hands for manipulative purposes. Alternatively,
manual proportions might have been optimized for manipulation
once the hands became freed from locomotion thanks to the
advent of terrestrial bipedalism [12,15].
PLoS ONE | www.plosone.org
Results
Precision grasping morphology
Extant great-ape PDPs lack all the features related to
precision grasping (Figure 2); as such, they display a smooth
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Figure 2. Morphological comparisons of pollical distal phalanges in African apes, extant humans and selected hominins. Specimens
are showed in palmar (top), oblique proximopalmar (middle) and lateral (bottom) views, and scaled to the same length to easily visualize the
morphological differences. The main features related to human-like precision grasping are indicated in the middle row (same colors as in Figure 1),
whereas the palmarly protruding insertion for the flexor pollicis longus has been further signaled in lateral view (red arrows in the lower row). Note
that, although with several morphological differences, all the features related to refined manipulation in modern humans are already present in the
late Miocene Orrorin. By the way, the OH 7 specimen, besides its odd overall proportions, neither shows a distinctive insertion for the flexor muscle,
nor a compartmentalized digital pulp. All the phalanges belong to a right thumb. Scale bars represent 5 mm.
doi:10.1371/journal.pone.0011727.g002
apical tuft (instead of a developed apical tuberosity with ungual
spines), and further lack well-developed basal tubercles, which
in humans reflect the presence of collateral intraosseous
ligaments for sustaining the nail bed ([3–4]; see Figures 1 and
2 and Videos S1, S2, S3, S4, S5 for renderings of the PDPs in
Figure 2).
Interestingly, the PDP of Orrorin, being the earliest pollical
specimen in the hominin fossil record (ca. 6 Ma; [16–17]) displays
an overall human-like morphology (Video S3). The latter even
includes the most significant features related to precision grasping
(Figure 2), although some of them (such as the ridge for insertion of
the FPL and the apical tuberosity) are stouter as compared to later
hominins and modern humans [17].
The Olduvai Hominid 7 (OH 7) specimen—originally attributed to Homo habilis [17]—differs from that of extant apes and
humans (Video S5). This PDP does not display ungual spines [3],
and there is no ridge for insertion of the FPL, but a huge palmar
fossa that extends until the large apical tuberosity (Figure 2).
Furthermore, the lack of a distinctive ungual fossa and spines
would be indicative of limited palmar pad compartmentalization
and, as such, of a restricted precision-grip capability [3].
PLoS ONE | www.plosone.org
PCA
A PCA based on PDP shape variables allow us to discriminate
the several extant genera being analyzed between each other
(Figure 3, see Materials and Methods and Table 1). Positive values
on the PC 1 (68% variance) are related to phalanges with
mediolaterally narrow tufts and shafts, and with dorsopalmarly
high midshafts and bases, thus having an overall rod-like
appearance. Negative values, on the contrary, are related to
phalanges with a flat appearance due to high breadths at midshaft
and at the distal end (i.e. with apical tuberosities instead of tufts).
Positive values on the PC 2 (13% variance) mainly separate
phalanges with a relatively large base, in both mediolateral and
dorsopalmar diameters (i.e., with a relatively small shaft and apical
tuft), from phalanges that are very long relative to other
dimensions (see Figures 2 and 3 and Videos S1, S2, S3, S4, S5).
To this respect, extant great apes display relatively narrow PDPs
with a dorsopalmarly high midshaft, while the apical tuft is not
well developed, conferring them a rod-like shape. This is especially
true concerning Pan and Pongo, which can be roughly distinguished
from each other thanks to the highest loads on PC 2 of orangs,
which display very small shafts and apical tufts relative to the base
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Figure 3. Principal components analysis (PCA) based on six shape variables of the pollical distal phalanx. Blue, Papio; red, Pongo;
yellow, H. sapiens; green, Gorilla; grey, Pan. The PC 1 largely reflects the proportions of the tuft and shaft, while the PC 2 is more related to the
proportions of the base. The Orrorin PDP overlaps with modern humans in both principal components, and later hominins also resemble modern
humans in both components—although to a lesser degree. Paranthropus robustus and OH 7 constitute an exception, because they fall within the
human range across the PC 2, but depart from the remaining taxa on the PC 1 by showing exceptionally wide PDPs (Figures 2 and 3). See text for
further explanation. Figures at the corners represent the outline of these phalanges in palmar and lateral views.
doi:10.1371/journal.pone.0011727.g003
Table 1. Main results of the principal components analysis (PCA) based on the six shape variables of the pollical distal phalanx,
including the variable loadings from the rescaled component matrix for the five principal components.
PC 1
PC 2
PC 3
PC 4
PC 5
% variance
68.668
13.344
8.072
7.149
2.768
% cumulative variance
68.668
82.012
90.084
97.232
100
Eigenvalue
0.67
0.13
0.08
0.07
0.03
PC 1
PC 2
PC 3
PC 4
PC 5
Variable loadings
Variables
L
0.837
20.483
0.111
0.230
20.027
MLT
20.912
20.006
20.320
0.256
0.000
DPS
0.847
0.042
20.393
20.347
0.077
MLS
20.886
20.275
0.201
20.307
20.064
DPB
0.520
0.744
0.181
0.074
20.372
MLB
20.114
0.602
0.553
0.149
0.544
The more significant values across PC 1 and 2 (in bold) are discussed in the text.
Abbreviations: PC = principal component; L = length; MLT = mediolateral width at the tuft; DPS = dorsopalmar height at midshaft; MLS = mediolateral width at
midshaft; DPB = dorsopalmar height at the base; MLB = mediolateral width at the base. The sixth component was not included because the first five components
almost explained the 100% of the total variance.
doi:10.1371/journal.pone.0011727.t001
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Concerning the fossil hominins, Orrorin (BAR 1901901) most
closely resembles modern humans in both components (Figure 3).
Neandertals (La Ferrassie I and Kebara 2) and Stw 294 (cf. A.
africanus) also fall close to modern humans in both components,
although both La Ferrassie I and Stw 294 display slightly highest
values on the PC 2. However, both Paranthropus robustus (SKX
5016) and OH 7 depart in PC 1 by having an extremely robust (i.e
mediolaterally broad) shaft and apical tuberosity in the PDP.
(Figure 3). On this basis, gorillas occupy a central position on the
scatter plot, because their PDPs overall resemble a somewhat
flatter version of chimps’ (see also Figure 2).
Extant humans display PDPs with relatively wide shafts and
apical tuberosities (see Figure 2), as indicated by the low loads on
the PC1. Moreover, they show low values on the PC2, which are
also correlated to a significantly long PDP (Table 2). This
combination of relatively long and wide PDP is exclusive of
humans among the extant taxa analyzed (Figure 3). It is interesting
to point out that, although humans and gorillas overlap in both PC
1 and PC 2, they occupy different regions in the morphospace.
The position of baboons (Papio) in the scatter plot indicates that
they show overall proportions on PDPs more similar to those of
humans than to great apes, although being relatively shorter and
displaying a larger base (Figure 3).
Ratios
Here we provide additional morphometric evidence regarding
the robusticity of the distal phalanges, by comparing the first (DP1)
and third (DP3) manual rays of extant taxa, together with OH 7,
Paranthropus robustus and Neandertals (Figure 4 and Table 2). In
orangutans, the PDP is only slightly more robust than the third
Table 2. Descriptive statistics for the ratios of distal phalangeal robusticity.
DP1 MLT/L
DP3 MLT/L
DP1MLT/L - DP3MLT/L
Taxon
N
Mean
SD
95% CI
Pan
33
0.268
0.039
0.254
0.281
0.197
0.336
Gorilla
15
0.335
0.032
0.317
0.353
0.276
0.392
Pongo
23
0.273
0.030
0.260
0.286
0.227
0.359
Homo
35
0.407
0.045
0.391
0.422
0.316
0.515
Papio
22
0.478
0.050
0.456
0.501
0.391
0.571
Macaca
18
0.494
0.084
0.453
0.536
0.354
0.620
OH 7
1
0.611
P.robustus
1
0.566
La Ferrassie I
1
0.485
Kebara 2
1
0.456
Taxon
N
Mean
SD
95% CI
Pan
32
0.313
0.056
0.292
0.333
0.187
0.421
Gorilla
15
0.385
0.047
0.359
0.410
0.316
0.480
Pongo
26
0.229
0.024
0.219
0.239
0.184
0.268
Homo
21
0.403
0.050
0.380
0.426
0.300
0.470
Papio
22
0.323
0.033
0.309
0.338
0.253
0.371
Macaca
14
0.294
0.069
0.254
0.334
0.218
0.423
OH 7
1
0.437
P.robustus
1
0.397
La Ferrassie I
1
0.467
Kebara 2
1
0.426
Taxon
N
Mean
SD
95% CI
Pan
32
20.043
0.043
20.059
20.028
20.134
Gorilla
12
20.052
0.049
20.084
20.021
20.145
0.028
Pongo
21
0.045
0.036
0.028
0.061
0.005
0.175
Homo
20
0.004
0.037
20.014
0.021
20.072
0.057
Papio
22
0.155
0.052
0.132
0.178
0.067
0.301
Macaca
14
0.205
0.081
0.158
0.252
0.077
0.347
OH 7
1
0.174
P.robustus
1
0.169
La Ferrassie I
1
0.017
Kebara 2
1
0.030
Range
Range
Range
0.049
The more important values of relative robusticity (in bold) are discussed in the text.
Abbreviations: DP1 = pollical distal phalanx; DP3 = middle finger distal phalanx; L = length; MLT = mediolateral width at the tuft; SD = standard deviation; CI =
confidence interval for the mean.
doi:10.1371/journal.pone.0011727.t002
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Figure 4. Boxplots of distal phalangeal robusticity in selected extant taxa, Neandertals, OH 7 and Paranthropus robustus. Robusticity
refers to apical tuft width (a) in relation to maximum length (b) of the distal pollical and middle finger phalanges (left and right, respectively; see
Materials and for further details). Horizontal lines represent the median values, whereas the boxes represent the 25% and 75% percentiles, the
whiskers the maximum-minimum ranges and circles are outliers. OH 7, like Paranthropus robustus, display a robusticity pattern convergent with
quadrupedal monkeys (Macaca and Papio), in which the pollical distal phalanx is disproportionally robust relative to that from the middle finger. Note
that the pollical and nonpollical distal phalanges attributed to P. robustus may not belong to the same individual.
doi:10.1371/journal.pone.0011727.g004
According to this, the hallux would have been extremely reduced
because of locomotor selection pressures, whereas the reduction of
the pollex would not have proceeded to the same extent due to
contradictory, manipulatory selection pressures favoring instead
the possession of a longer thumb [23]. In orangutans, the
reduction of the hallux has also affected the long flexor tendon
[22]. This condition that can be also found in the thumb of all
extant great apes, especially in Pongo and Pan, in which locomotor
selection pressures have probably favored the lengthening and
increased strength of digits II-V [18].
Thus, although extant great apes display diminished thumbs,
especially concerning extrinsic muscle insertions, they do have
well-developed intrinsic muscles that enable efficient power and
precision grips, the latter being used during food manipulation
[1,2,5,18,24]. Chimps and gorillas do efficiently manipulate small
object between their thumb and index finger using different
precision grip combinations (e.g. tip-to-tip and pad-to-side), but a
human-like, pad-to-pad precision grip is precluded due to the
disproportionate length of their digits II-V relative to that of the
thumb [1,2,5,24]. Chimps and orangs mostly rely on arboreal
foraging by directly putting the foods from branch to mouth,
whereas gorillas spend many hours on the ground, where they
carefully select, manipulate and hold the food with their hands
[18]. Increased terrestriality in such a large ape might have
resulted in longer thumbs relative to the rest of the hand [12,25],
as a by-product of their shorter hands relative to body mass [26].
The Gorilla hand therefore displays more balanced proportions
distal one, whereas in African apes the reverse condition is found.
The 95% confidence intervals (CI) for DP1 and DP3 robusticity
between extant great apes do not overlap, suggesting that
differences are significant. In modern humans the degree of distal
phalanx tuft robusticity for the first and third manual rays is very
similar, although it is somewhat higher in the thumbs of
Neandertals, with both La Ferrassie I and Kebara II having
robusticity values above the 95% CI of extant humans. In
monkeys, on the contrary, the distal pollical phalanx is much more
robust than the distal third one, with both macaques and baboons
showing values well above the 95% CI to that of the third digit.
This odd condition is also found in both OH 7 and P. robustus,
which the difference between the robusticity of the two digits (DP1
- PD3) falling within the 95% CI displayed by monkeys (see
Figure 4 and Table 2).
Discussion
Functional analysis
Extant great apes do not significantly use the thumb during
locomotion: it does not participate in below-branch suspensory
behaviors, and it does not support body weight during knucklewalking in African apes [18–21]. However, it can participate
during terrestrial palmigrady and fist-walking in orangutans [18].
In the latter, the hallux is reduced [22], and in some cases the
distal phalanx may not be present at all [23]. This is explained by
the specialized, four-digit hook grasp of orangs’ hands and feet.
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Origin of Precision Grasping
talized digital pulp (Figure 2)—is not found among non-human
primates, being indicative of a stable and powerful pad-to-pad
contact during refined manipulation [3–4]. The similar position
occupied by the PDPs of modern humans and those of fossil
hominins (including Neandertals), together with the possession of
morphological features functionally-related to pad-to-pad precision grasping [17,30–31], is highly indicative of shared functional
similarities. Apart from Neandertals, this is evident in Stw 294 (cf.
A. africanus) and, particularly, in BAR 190191 (Orrorin), the latter
showing, among early hominins, the greatest resemblance to
extant humans (Figures 2–3). On the contrary, SKX 5016 (P.
robustus) and OH 7, although more closely resembling extant
humans than any other taxa examined, display extremely broad
shafts and apical tuberosities (Figures 3–4). Although the phalanx
attributed to P. robustus has been described as displaying some traits
related to pad-to-pad precision grasping [17], this is not the case of
OH 7 [3–4], which lacks some of these features (Figure 2 and
Video S5; see next section). These results agree with previous ones,
according to which both OH 7 and SKX 5016 are extremely
broad phalanges, unlike those of humans or apes, thus having a
narrow base relative to these dimensions [32].
All the evidence reported above suggests that the morphological
differences found between the PDPs of extant taxa seem to be also
correlated to functional differences in hand function, particularly
involving the thumb. It would be of utmost interest to discern
whether the subtle morphological differences found amongst the
fossil hominins being analyzed—particularly concerning SKX
5016 and OH 7—are also correlated to differences in function, or
whether they are alternatively correlated to different overall body
types [32]. This cannot be definitively settled until more
postcranial remains of these hominins are available. However,
given the apparently convergent morphological similarities
between these fossil taxa and baboons, both in the middle [33]
and distal phalanges [this study], we favor the view that some kind
of functional differences as compared to other hominins are likely.
between the thumb and index finger (presumably related to
somewhat advanced manipulatory capabilities) than chimps and
especially orangs [5].
Our results show that extant great apes exhibit rod-like PDPs
with barely discernible muscular impressions on the palmar side,
further lacking developed tufts and associated palmar pads
(Figures 2–4; see also [4,6,22]). The lack of dorspalmar flattening
in the PDP, especially in Pan and Pongo, would be related to the
lack of a developed flexor apparatus (usually without receiving
extrinsic muscular component). The overall reduced PDP of
orangs, especially referring the shaft and apical tuft, obviously
stems from their rudimentary thumbs, which are diminished like in
Colobus and Procolobus [22]. In the latter taxa, the PDP, when
present, is usually confined to its proximal portion, the base (S.A.
personal observation). Gorillas, being the most terrestrial great
apes and displaying relatively short and skillful hands with
relatively long thumbs, possess a somewhat flatter PDP than the
other great apes (Figures 2–3). Furthermore, gorillas also exhibit
more barely evidence of muscular insertion scars on the palmar
side of the PDP shaft than them (Figure 2). Since the thumbs of
gorillas do not participate in locomotion, this morphology should
be correlated with an increased use of the thumb for manipulation
as compared to Pan and Pongo [18].
Terrestrial monkeys, in its turn, exhibit proportionally short
fingers in relation to their thumbs, thereby enabling an efficient
precision grip [27–28]. This is particularly evident in gelada
baboons, which display enhanced manual feeding capabilities [29]
thanks to displaying the highest opposability index among extant
primates, including humans [28]. Other baboons (Papio spp.) show
the same capabilities, although to a lesser degree [28]. These
baboons are digitigrade, and only the tip of the thumb contacts the
substrate during the touchdown phase [21]. A huge long flexor
tendon is inserted onto the distal part of the shaft and tuberosity of
their PDP [4], although it does not correspond to the FPL, but to
the radial portion of the flexor digitorium profundus [21]. Moreover,
during the tip-weight support, their PDPs can be hyperextended,
so that, like in humans, their pollical interphalangeal joint displays
well-developed sesamoid bones [4]. There are also other
similarities between baboon and human PDPs [4], such as a
broad distal pad, tuberosity (sometimes with spines) and nail, a
large palmar fossa (but not a distinct ridge for insertion of the FPL
and ungual fossa), and similar ratios concerning both bone and
long flexor tendon dimensions. These similarities can be related to
the enhanced manipulative capabilities displayed by these
monkeys [27–29].
Our results agree with previous findings showing that baboons
display PDPs more similar in overall proportions to those of extant
humans rather than those of extant great apes, although being
shorter and displaying a larger base (Figure 3). This morphology
might be an adaptation to frequent weight bearing, during which
the tip of the thumb contacts the ground in hyperextended
postures. According to this, the enhanced manipulative capabilities
displayed by baboons could be merely a by-product of an
adaptation of the hand to digitigrady, resulting in a long thumb
relative to the rest of the hand that would be suitable for pad-topad precision grasping (see Fig. 8a–b in [28]). The precision
grasping displayed by these monkeys, in any case, is much less
developed than that of humans, which is further reflected by the
lack in the former of many PDP traits that are functionally related
to human-like precision grasping (Figures 1–2; [3–4]).
The morphology displayed by the PDP of modern humans—
including a relatively long bone, dorsopalmarly flat and wide at the
shaft and apical tuberosity (Figure 3), together with several
morphological traits related to a powerful FPL and compartmenPLoS ONE | www.plosone.org
The attribution of the OH 7 hand remains
The original attribution of the partial hand from Olduvai Bed I
to the holotype of H. habilis (OH 7, consisting in the parietals and
mandible of a subadult; [34]) has been subsequently accepted by
most authors [e.g. 2–3,35–36], mainly due to its subadult status.
However, due to its overall robusticity—especially concerning the
PDP—and curved middle phalanges, an alternative attribution to
Paranthropus—contemporary to Homo in that region [37]—was also
suggested long ago [18,38]. More recently, this alternative
attribution has been further favored on the basis of morphometric
and morfofunctional analyses, particularly concerning middle
phalangeal morphology [33]. The later study found that the OH 7
remains are more similar to those from South Africa attributed to
P. robustus than to earlier Australopithecus and later and contemporary humans [33]. It is also noteworthy that other bones from the
OH 7 hand, such as the trapezium, also suggests a taxonomic
attribution different than Homo [9].
Be that as it may, the odd morphology of OH 7 PDP led some
authors to consider an alternative anatomical identification as a
hallucial distal phalanx [35]. This would be supported by the
strong muscular attachments and, especially, the slight axial
torsion at the apical tuft (functionally related to bipedalism).
However, a discriminant analysis by the same authors indicated
‘‘that the fossil is closer to human distal phalanges than to those of
any other hominoid and is somewhat more like a pollical than a
hallucial phalanx’’ [35, p. 325]. We concur with this anatomical
identification, especially given that there are no differences in axial
torsion as compared to modern humans or extant apes (Figure 2),
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July 2010 | Volume 5 | Issue 7 | e11727
Origin of Precision Grasping
in which the apical tuft is slightly twisted, so that it faces the rest of
the fingers. It is also noteworthy that the PDP of OH 7 does not
display a human-like morphology related to precision grasping
([3]; Figure 2 and Video S5). This includes its odd overall
proportions, which like in SKX 5016 (P. robustus) are characterized
by a high degree of apical and midshaft robusticity, as it is found
here (Figure 3) and in many previous works [10,32–33,39].
Furthermore, our results regarding relative distal phalangeal
robusticity show that, when non-pollical manual rays are also taken
into account, the pattern of robusticity of OH 7, like that of
Paranthropus, resembles that of quadrupedal monkeys and does not fit
either the great-ape or the human pattern (Figure 4). These results
agree with a previous study of this partial hand, which interpreted the
morphology of the middle phalanges as showing convergent
adaptations with gelada baboons [33]. Alternatively, it would be
necessary to conclude that early Homo was more similar to Paranthropus
than to Australopithecus and Orrorin regarding several aspects of
phalangeal morphology, which in evolutionary terms would imply
a reversion regarding, among others, the robusticity of the PDP.
Thus, although the late Miocene Orrorin is somewhat ape-like in
dorsopalmar dimensions, it approaches a human-like profile in
mediolateral dimensions. Moreover, it is most remarkable that
although Plio-Pleistocene australopiths also show the morphological features related to precision grip [17], the 6-million-years-old
PDP of Orrorin is more human-like in overall proportions and
morphology than these later hominins. To this respect, both OH 7
and SKX 5016 display a degree of mediolateral broadening that
highly surpasses the human condition. This is consistent with the
femoral morphology of this taxon, which more closely resembles
australopiths than later Homo, but among early hominins it is the
one that most closely resembles humans [43]. All this evidence
suggests that australopiths—especially Paranthropus—are derived by
displaying a robusticity pattern on the distal phalanges that is
convergent with that of quadrupedal monkeys (Figure 4), as
previously suggested for the middle phalanges [33], and also
suggested to some degree by the trapezial morphology [9,36].
Be that as it may, the highest resemblance between the late
Miocene Orrorin and modern humans, with the exclusion of
australopiths, is an unexpected result that bears important
implications for the understanding of the selective pressures
originally involved in the evolution of human manual skills. Extant
great apes are highly committed to arboreal locomotion (including
vertical climbing and suspensory behaviors), their manipulative
capabilities being limited by their relative short thumbs [1–2,5], and
especially by their absolutely long hands [12]. Because Miocene
apes displayed absolutely long thumbs, it has been suggested that
their hands were more suitable for manipulative purposes than
those of extant hominoids [44–47]. The same condition can also be
inferred for the stem hominid Pierolapithecus, which displays relatively
short manual phalanges—like other early and middle Miocene
apes—as well as a relatively long PDP [48–49].
From the evidence presented above, it can be suggested that the
hand length proportions of humans are plesiomorphic to a large
extent. If Orrorin was an early biped hominin with a PDP adapted
to refined manipulation, it follows that the whole thumb would be
long relative to the hand, thus enabling an efficient pad-to-pad
contact. Thus, this leads us to hypothesize that the manual
proportions of Orrorin might have more closely resembled those of
early and middle Miocene apes than those of extant apes, which
would have diverged towards a different direction from the same
ancestral morphotype. This idea is similar to that presented by
Tuttle [18], who suggested that ‘‘By the time early hominids had
assumed a bipedal gait, the hand was probably well on its way
toward modern human configuration’’ [18; p. 203]. We therefore
favor the hypothesis that human hand proportion enabling a padto-pad precision grasping are an exaptation, co-opted by early
bipedal hominins for manipulative purposes, but originally evolved
within a locomotor selective context as an adaptation to powerfulgrasping—assisted by the thumb— within an arboreal setting in
Miocene apes. This would explain why early bipedal hominins,
such as A. afarensis [12] and A. africanus [13], already displayed
human-like hand length proportions prior to the appearance of
stone tools in the archeological record. It seem likely that the
acquisition of habitual bipedalism—which largely freed the upper
extremities from locomotor demands [14]—would have facilitated
the refining of the manipulative capabilities displayed by all
primates [e.g. 1–2,5,12,28,33]. Furthermore, bipedalism could
also affect the hand morphology by means of correlated
developmental responses dues to changes in the feet morphology
[12,39]. Thus, most probably ‘‘early hominoids [and hominins]
[…] evidently employed behaviors resulting from the addition of a
number of functional morphological innovations to a relatively
conservative body plan, including those underlying a more
The attribution of BAR 1901901
Hallucial distal phalanges do not display the set of features
present in all the human PDPs, which are related to the pad-topad contact. Thus, they do show a large proximoplantar fossa,
which is further accompanied by plantarly protruding basal
tubercles. In proximal view, these structures configure a very wide
and shallow channel for the pass and/or insertion of the flexor
hallucis longus, which can act as a ‘‘supporting muscle’’ during
terrestrial progression in both apes and humans [40].
Thus, besides morphometric similarities, the PDP of the late
Miocene Orrorin displays the typically human set of morphological
features functionally related to human pad-to-pad precision
grasping (Figure 2 and Videos S3–S4; [4]). The presence of these
features, among others, indicates that BAR 190191 does not
belong to the hallux. The other features indicating an anatomical
attribution to the pollex include: its degree of elongation, overall
flatness, and round dorsal surface [17]; the orientation of the
apical tuberosity, which does not face distally (such is the case in
distal phalanges that support weight stresses in hyperextended
positions; see Fig. 1 in [41] for the case of OH 10); and the lack of
axial torsion, which is present in the hallucial phalanges of both
humans [41] and apes [42].
The evolution of refined manipulation
The presence of precision grip features in the PDP of Orrorin
indicates that this bone was fully prepared to accommodate objects
between the palmar aspect of its pulp and that of the fingers. Some
of these precision-grasping features in the Orrorin specimen had
been previously reported, although they were interpreted as an
adaptation to arboreal locomotion reflecting ‘‘the precision grip
essential for climbing and balancing, different from that of apes’’
([17], p. 372). However, given the fact that no arboreal primate
displays this set of features, we favor the hypothesis that
functionally relates the striking and detailed similarities between
Orrorin and extant human PDPs to refined object manipulation.
Admittedly, although the Orrorin phalanx mostly looks like a
human PDP, it also displays some primitive features that are
further retained by the later australopiths, such as a small ungual
fossa and a proximally protruding median eminence of the
articular surface. Moreover, some other features, like the ridge for
insertion of the FPL, and the dorsopalmar height of the shaft and
apical tuberosity, are stouter than in later hominins and modern
humans (Figure 2). The latter display relatively flat PDPs,
especially at midshaft and distal tuberosity levels (Figures 2–3).
PLoS ONE | www.plosone.org
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July 2010 | Volume 5 | Issue 7 | e11727
Origin of Precision Grasping
sophisticated manipulative and grasping use of the hand than used
before’’ [50, p. 264].
Most likely, these hand capabilities would have not been coopted until much later for a regular use in stone tool-making,
coinciding with the encephalization increase that took place in
hominins with the advent of the genus Homo ca. 2.5 Ma [51–53].
Thus, stone tool-making would not have played a significant role
until the latter part of human hand evolution, and especially after
the advent of the Acheulian culture [54], as already suggested by
Tuttle [18]. On the basis of the evidence provided by modern
human hands, the fine tuning of manipulative adaptations during
the evolution of Homo would have involved an increase of overall
robusticity at the several manual joints, an increase in robusticity
of the whole thumb, and especially the development of distinct
palmar pads on the distal phalanges.
More complete fossil hands from the African Mio-Pliocene
transition would be necessary to clarify this issue, especially regarding
of the selection pressures underpinning the remarkable human-like
features of the Orrorin PDP. For the moment being, the most complete
fossil hand around this time corresponds to the 4.4 million-years-old
putative hominin Ardipithecus ramidus [55]. Although its hand is not as
elongated as in extant apes [55], its thumb seems to be relatively
short, and its PDP looks more ape-like than that of Orrorin, in spite of
the older chronology of the latter. Thus, although A. ramidus has been
claimed to be an early hominin close to the last common ancestor
with Pan [56], it could be alternatively interpreted as one of the apes
‘‘among the tangled branches that constitute the basal hominine
bush’’ [57, p 533]. Only future comparative studies would help to
bring some light onto this question.
SKX 27504 (attributed to P. robustus), La Ferrassie I and Kebara 2.
Measurements for fossil specimens were taken from originals, good
quality casts or from the literature [31,58–59].
PCA
A principal components analysis (PCA) based on the covariance
matrix was employed to perform morphometric comparisons
between the pollical distal phalanges (PDP) of selected fossil
specimens and those of other hominins and extant primates,
including modern humans. This analysis, which does not assume
group membership on a priori grounds, was based on six shape
variables of the PDP, in its turn computed on the basis of the
following six metrial variables: length (L); mediolateral width at the
apical tuft (MLT), midshaft (MLS) and the base (MLB); and
dorsopalmar height at midshaft (DPS) and the base (DPB). These
measurements were transformed into shape variables by dividing
each of them by the geometric mean (GM) of all the six phalangeal
measurements (the GM being taken as a variable of overall
phalangeal size) and then applying a logarithmic transformation
(on the basis of natural logarithms, ln), following [43].
Ratios
Distal phalangeal robusticity was analyzed by means of a ratio
between apical tuft width and maximum length, separately for
both the distal pollical and middle finger phalanges. We further
calculated the difference between both ratios, in order to quantify
the relative robusticity of the pollical distal phalanx in relation to
that of the middle finger. Summary statistics for extant and fossil
taxa are reported in Table 2.
Conclusions
Supporting Information
The pollical distal phalanx of the early bipedal hominin Orrorin
(BAR 1901901) unequivocally shows precision grasping capabilities
in spite of its ancient chronology, most closely resembling modern
humans than some later Plio-Pleistocene hominins—which show a
derived robusticity pattern. This indicates that refined manipulation is an ancient acquisition already present by the late Miocene.
This is consistent with the hypothesis that habitual terrestrial
bipedalism and the possession of skillful hands do constitute a
single adaptive complex. Both types of behaviors might have been
simultaneously selected, by synergistically favoring each other.
From the evidence reported by BAR 1901901, it is reasonable to
assume that human hand length proportions (i.e. short hands and
relatively long thumbs) are plesiomorphic to some degree, thus
more closely resembling the short hands with relatively long
thumbs of Miocene apes, rather than the elongated hands of
extant apes, which seem to be secondarily derived. These ancient
proportions, suitable for refined manipulation, would not have
been co-opted for stone tool-making until much later, coinciding
with a significative increase in encephalization in the genus Homo.
Video S1 360u video render of Pan troglodytes pollical distal
phalanx.
Found at: doi:10.1371/journal.pone.0011727.s001 (3.31 MB AVI)
Video S2 360u video render of Gorilla gorilla pollical distal
phalanx.
Found at: doi:10.1371/journal.pone.0011727.s002 (2.96 MB AVI)
Video S3 360u video render of Orrorin tugenensis pollical distal
phalanx.
Found at: doi:10.1371/journal.pone.0011727.s003 (3.72 MB AVI)
360u video render of Homo sapiens pollical distal
phalanx.
Found at: doi:10.1371/journal.pone.0011727.s004 (3.46 MB AVI)
Video S4
Video S5 360u video render of Olduvai Hominid 7 pollical distal
phalanx.
Found at: doi:10.1371/journal.pone.0011727.s005 (4.32 MB AVI)
Acknowledgments
Materials and Methods
We are indebted to the following curators and scholars for granting access
to collections under their care: Wim van Neer, Burkart Engesser,
Assumpció Malgosa, Lars van den Hoek Ostende, Eileen Westwig and
Eric Delson. Marta Palmero assisted us with Figure 1 and Diana Cózar
provided with the nice video renderings. We are especially grateful to
Soledad De Esteban-Trivigno for her ideas and to Brigitte Senut for
making us available the cast of the Orrorin PDP.
The primate sample
The comparative extant sample includes the following taxa:
chimpanzees and bonobos (Pan; N = 29), gorillas (Gorilla; N = 13),
orangutans (Pongo; N = 19), baboons (Papio; N = 22) and modern
humans (Homo sapiens; N = 22). The fossil sample includes the PDPs
of Orrorin tugenensis from the Lukeino Formation (BAR 1901901),
Australopithecus africanus from Sterkfontein (Stw 294), the hand from
Olduvai (OH 7 A), Paranthropus robustus from Swartkrans (SKX
5016), and H. neanderthalensis from La Ferrassie I and Kebara 2.
Apart of the above-mentioned extant taxa, we further employed the
following fossil third distal phalanges for computing ratios: OH 7 B,
PLoS ONE | www.plosone.org
Author Contributions
Conceived and designed the experiments: SA SMS DMA. Performed the
experiments: SA SMS DMA. Analyzed the data: SA SMS DMA. Wrote
the paper: SA SMS DMA.
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Origin of Precision Grasping
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