Journal of Human Evolution 63 (2012) 64e78
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Journal of Human Evolution
journal homepage: www.elsevier.com/locate/jhevol
Evolution and homologies of primate and modern human hand and forearm
muscles, with notes on thumb movements and tool use
Rui Diogo a, *, Brian G. Richmond b, c, Bernard Wood b, c
a
Department of Anatomy, Howard University College of Medicine, 520 W St. NW, Washington, DC 20059, USA
Center for the Advanced Study of Hominid Paleobiology, Department of Anthropology, George Washington University, DC 20052, USA
c
Human Origins Program, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA
b
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 21 January 2012
Accepted 5 April 2012
Available online 27 May 2012
In this paper, we explore how the results of a primate-wide higher-level phylogenetic analysis of muscle
characters can improve our understanding of the evolution and homologies of the forearm and hand
muscles of modern humans. Contrary to what is often suggested in the literature, none of the forearm
and hand muscle structures usually present in modern humans are autapomorphic. All are found in one
or more extant non-human primate taxa. What is unique is the particular combination of muscles.
However, more muscles go to the thumb in modern humans than in almost all other primates, reinforcing the hypothesis that focal thumb movements probably played an important role in human
evolution. What makes the modern human thumb myology special within the primate clade is not so
much its intrinsic musculature but two extrinsic muscles, extensor pollicis brevis and flexor pollicis
longus, that are otherwise only found in hylobatids. It is likely that these two forearm muscles play
different functional roles in hylobatids and modern humans. In the former, the thumb is separated from
elongated digits by a deep cleft and there is no pulp-to-pulp opposition, whereas modern humans
exhibit powerful thumb flexion and greater manipulative abilities, such as those involved in the
manufacture and use of tools. The functional and evolutionary significance of a third peculiar structure,
the intrinsic hand structure that is often called the ‘interosseous volaris primus of Henle’ (and which we
suggest is referred to as the musculus adductor pollicis accessorius) is still obscure. The presence of
distinct contrahentes digitorum and intermetacarpales in adult chimpanzees is likely the result of prolonged or delayed development of the hand musculature of these apes. In relation to these structures,
extant chimpanzees are more neotenic than modern humans.
Ó 2012 Elsevier Ltd. All rights reserved.
Keywords:
Phylogenetic analysis
Morphology
Extensor pollicis brevis
Flexor pollicis longus
Adductor pollicis accessorius
Introduction
An understanding of comparative myology is crucial for developing hypotheses about the functional morphology of the modern
human forearm and hand, and particularly their involvement in the
manufacture and use of tools (e.g., Day and Napier, 1961, 1963;
Napier, 1962; Tuttle, 1969; Lewis, 1989; Marzke, 1992, 1997;
Susman, 1994, 1998; Marzke et al., 1998; Susman et al., 1999;
Tocheri et al., 2008). The relatively few publications that have
included myological information in discussions of the evolution of
the primate and modern human forearm and hand can be divided
into two groups. Publications prior to the 1950s were mainly the
work of comparative vertebrate, tetrapod or mammalian anatomists who, with the exception of authors such as Howell and Straus
* Corresponding author.
E-mail addresses: [email protected], [email protected] (R. Diogo).
0047-2484/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jhevol.2012.04.001
(1932) and Straus (1941a, b), usually investigated a wide range of
non-primate species but only a few primate taxa (e.g., Brooks, 1886;
Parsons, 1898; McMurrich, 1903a, b; Forster, 1917; Howell, 1936a, b;
Haines, 1939, 1946, 1950; Straus, 1942a, b). This pattern contrasts
with most of the reports published since the 1950s that have
mainly focused on primates, or even more narrowly, on hominoids
or on modern humans (Hominina: see Fig. 1), and when they did
provide a non-primate comparative context it was a relatively
narrow one (e.g., Abramowitz, 1955; Day and Napier, 1963;
Dylevsky, 1967; Tuttle, 1969; Dunlap et al., 1985; Aziz and Dunlap,
1986; Susman, 1994, 1998; Marzke et al., 1998; Susman et al.,
1999). A notable exception is Lewis' (1989) book that includes
detailed information based on his own dissections of a wide range
of non-primate tetrapods.
These studies have generated hypotheses regarding the evolution of primate forearm and hand anatomy, among them that
modern humans are derived relative to other extant primates in
possessing a true flexor pollicis longus, a deep head of flexor pollicis
R. Diogo et al. / Journal of Human Evolution 63 (2012) 64e78
LEMURIFORMES
Lemur (Lemuridae)
Propithecus (Indriidae)
Loris (Lorisidae)
STREPSIRRHINI
Nycticebus (Lorisidae)
1,2
LORISIFORMES
Tarsius (Tarsiiformes; Tarsiidae)
PRIMATES
Pithecia (Pitheciidae)
Aotus (Aotidae)
Callithrix (Callitrichinae)
Saimiri (Saimiriinae)
3,4,5
CEBIDAE
CEBIDAE+AOTIDAE
HAPLORRHINI
PLATYRRHINI
Colobus (Colobinae)
Cercopithecus (Cercopithecini)
Macaca (Macanina)
Papio (Papionina)
6
PAPIONINI
ANTHROPOIDEA
CERCOPITHECINAE
7,8,9
CERCOPITHECIDAE
CATARRHINI
HOMINOIDEA
Hylobates (Hylobatidae)
10,11,
12,13 14,15,
Pongo (Ponginae)
16,17 18,19,
Gorilla (Gorillini)
20
Pan (Panina)
Homo (Hominina)
HOMINIDAE
HOMININAE
HOMININI
21,22,23,
24,25
Figure 1. Single most parsimonious primate tree (L 301, CI 58, RI 73) obtained from the
cladistic analysis of 166 characters of the head, neck, pectoral and forelimb musculature (Diogo and Wood, 2011, 2012), showing the unambiguous transitions (homoplasic: regular font; non-homoplasic: bold) of the forearm and hand musculature that
occurred in the branches leading to modern humans: 1) Opponens pollicis is a distinct
muscle (this muscle became secondarily undifferentiated in Callithrix); 2) Opponens
digiti minimi is a distinct muscle (also found in a few other mammals, e.g., Rattus); 3)
Flexor carpi radialis inserts onto the metacarpals II and III (also found in a few other
mammals, e.g., Tupaia); 4) There are more than two contrahentes digitorum (reverted
in some haplorrhines, e.g., modern humans); 5) Adductor pollicis has slightly differentiated transverse and oblique heads; 6) Supinator has ulnar and humeral heads
(independently acquired in Lorisiformes); 7) Adductor pollicis further differentiated
into distinct transverse and oblique heads; 8) Opponens pollicis reaches the distal
portion of metacarpal I (feature independently acquired in Lorisiformes); 9) Opponens
digiti minimi is slightly differentiated into superficial and deep bundles; 10) Flexor
digitorum superficialis originates from the radius; 11) Flexor digitorum superficialis
originates from the ulna; 12) Epitrochleoanconeus is not a distinct muscle (this muscle
became undifferentiated in Lorisiformes and in hominoids, and then became
secondarily differentiated in Pan); 13) Pronator teres often (but not usually, i.e., in
<50% of the cases) originates from the ulna; 14) Flexor digitorum profundus is not
originated from the medial epicondyle of the humerus or from the common flexor
tendon (feature also found in Macaca); 15) Tendon of flexor digitorum profundus to
digit 1 is vestigial or absent (this feature was independently acquired in Colobus and it
was secondarily reverted - i.e., the tendon is not atrophied - in modern humans); 16)
Pronator teres is usually (50% of the cases) originated from the ulna; 17) Contrahentes digitorum are missing (this feature was secondarily reverted in Pan, i.e., alone
among the Hominidae, Pan has distinct contrahentes digitorum); 18) Palmaris longus
is absent in >5% of the cases; 19) Adductor pollicis accessorius (or ‘interosseous volaris
primus of Henle’ of modern human anatomy) is often (i.e., in <50% of the cases)
present; 20) Extensor indicis usually inserts onto digit 2 only; 21) Flexor pollicis longus
is a distinct muscle (independently acquired in hylobatids); 22) Reversion of ‘Tendon of
flexor digitorum profundus to digit 1 is vestigial or absent’ (see above); 23) Reversion
of ‘Flexor carpi radialis originates from the radius’ (the muscle originates from the
radius in gorillas, chimpanzees and orangutans, but it is not clear which is the usual
condition for hylobatids, and, thus, whether a radial origin constitutes a synapomorphy
of hominoids or of hominids); 24) Adductor pollicis accessorius (or ‘interosseous
volaris primus of Henle’ of modern human anatomy) is usually (i.e., in >50% of the
cases) present; 25) Extensor pollicis brevis is a distinct muscle (independently
acquired in hylobatids) [for more details, see text].
brevis, a volar interosseous of Henle, and an extensor pollicis brevis.
However, with a few noteworthy exceptions, the authors of most of
these publications relied on reports in the literature for their
comparative information. This is problematic because the
65
nomenclature of the forearm and hand muscles of primate and
non-primate tetrapod taxa has been the subject of some confusion
and controversy (see Diogo, 2007, 2009; Diogo and Abdala, 2007,
2010; Diogo et al., 2009; Diogo and Wood, 2011, 2012). For example,
statements that some non-hominoid primates have a separate
flexor pollicis longus (e.g., Marzke, 1997; Shrewsbury et al., 2003)
refer to older publications that often used the name ‘flexor pollicis
longus’ for the tendon of the flexor digitorum profundus that
inserts onto digit 1 and not for a separate flexor pollicis longus that
has a distinct belly and tendon (see below).
In recent papers (Diogo and Abdala, 2007; Diogo et al., 2009;
Abdala and Diogo, 2010; Diogo and Wood, 2011) and monographs
(Diogo, 2007; Diogo and Abdala, 2010; Diogo and Wood, 2012),
Diogo and colleagues have reported the results of their long-term
dissection-based study of the comparative anatomy, homologies
and evolution of the pectoral and forelimb muscles of all major
groups of non-primate vertebrates and representatives of all of the
major primate higher taxa. Diogo and Wood (2011, 2012) combined
data from these dissections with carefully validated information
from the literature to undertake the first comprehensive parsimony
and Bayesian cladistic analyses of the order Primates based on
myological data (Fig. 1) and for a range of outgroups (tree-shrews,
dermopterans and rodents). A goal of the project was to establish
the homologies of the pectoral and forelimb muscles of vertebrates
and to provide the comparative context for more detailed evolutionary and taxon-based analyses.
The present paper uses data from these dissections to test
hypotheses about the evolution of the hand musculature of modern
humans. Because we have dissected members of all of the major
primate groups and the major non-primate vertebrate taxa, we can
better understand the descriptions of authors that use different
nomenclatures for these muscles. This has allowed us to clarify
much of the nomenclatural confusion involved in the descriptions
of the forearm and hand muscles of primates (see above). We also
use these data to critically examine the proposition that modern
humans are derived in having a flexor pollicis longus, deep head of
flexor pollicis brevis, a ‘volar interosseous’ or ‘interosseous volaris
primus’ of Henle, and an extensor pollicis brevis.
Materials and methods
We dissected representatives of each major extant nonhominoid primate clade (Strepsirrhini, Tarsiiformes, New World
monkeys and Old World monkeys) and of each of the five main
groups of living hominoids (i.e., hylobatids, orangutans, gorillas,
chimpanzees, and modern humans) (Fig. 1). With a few exceptions,
we use the same taxonomic nomenclature as Diogo and Wood
(2011). Data included in the analysis come from four strepsirrhine
genera, two from the infraorder Lemuriformes (Lemur, family
Lemuridae; Propithecus, family Indriidae) and two from the infraorder Lorisiformes (Loris and Nycticebus, family Lorisidae); the
single extant genus of the infraorder Tarsiiformes, Tarsius; representatives of three of the four extant platyrrhine families: Saimiri
and Callithrix (Cebidae, subfamilies Saimiriinae and Callithrichinae,
respectively), Pithecia (Pitheciidae), and Aotus (Aotidae; the other
platyrrhine family being the Atelidae); the two extant subfamilies
of Old World monkeys (family Cercopithecidae) represented by
Colobus (Colobinae), Papio, Macaca and Cercopithecus (Cercopithecinae; the two former genera represent the tribe Papionini, while
the latter genus represents the other extant tribe of the subfamily,
the Cercopithecini); and five extant hominoid genera: Hylobates
(Hylobatidae), Pongo (Hominidae, Ponginae), Gorilla (Hominidae,
Homininae, Gorillini), Pan (Hominidae, Homininae, Panini, Panina),
and Homo (Hominidae, Homininae, Hominini, Hominina) (Fig. 1).
We use the traditional classification that recognizes a single extant
66
R. Diogo et al. / Journal of Human Evolution 63 (2012) 64e78
hylobatid genus (Hylobates; including species such as Hylobates
syndactylus, Hylobates lar, Hylobates gabriellae and Hylobates hoolock, among others: for more details see Diogo and Wood, 2011).
Apart from the primates dissected for this study, we have dissected
specimens from all of the major groups of vertebrates. A list of the
dissected non-primate vertebrate specimens is given in Diogo and
Abdala (2010).
The nomenclature for the forearm and hand muscles follows
that of Diogo and Abdala (2010) (see Table 1). We addressed the
problem of inconsistent usage of some specific taxonomic names in
older systematic and anatomical studies, particularly those prior to
Osman Hill’s studies in the 1950s (e.g., Hill, 1953, 1955, 1957, 1959,
1960, 1962, 1966, 1970, 1974; see References) by carefully reviewing
all of the names and synonyms used in those studies (see Diogo and
Wood, 2011). Discussions of the evolutionary changes occurring in
each of the major primate branches are based on the phylogenetic
results of Diogo and Wood (2011) (Fig. 1). The primate specimens
were mainly dissected by RD, and were obtained from the following
institutions: the Primate Foundation of Arizona (PFA), the Department of Anatomy (GWUANA) and the Department of Anthropology
(GWUANT) of the George Washington University, the Department
of Anatomy of Howard University (HU), the Department of
Anatomy of Valladolid University (VU), the Cincinnati Museum of
Natural History (CMNH), the San Diego Zoo (SDZ) and the Canadian
Museum of Nature (CMN). For each taxon, we provide the Linnean
binomial, its source, its unique identifier, the number of specimens
from that source and the state of the specimens. Regarding the
sample size used in the cladistic study of Diogo and Wood (2011)
and in the discussions of the present paper, two points should be
stressed. First, it is difficult to find primate, and particularly ape,
specimens in circumstances where careful dissection can take
place. During this project, we made a considerable effort to establish connections with the major museums and zoos in the United
States and beyond. This effort resulted in us being able to dissect,
for example, two fresh gorillas, one fresh and one formalin
embalmed Pongo, and six fresh and three formalin embalmed
chimpanzees. The second point is that the sample size used in that
cladistic study and in the discussions provided here refers to the
specimens dissected by us and the total number of specimens
reported in the numerous publications that were analysed in the
extensive review of the literature undertaken by Diogo and Wood
(2011) and particularly Diogo and Wood (2012). Thus, when we
code and discuss each character we take into account all of the
information available, and in numerous cases the total sample size
is substantial when compared with cladistic studies of other animal
species that were based on muscles (see, e.g., Diogo, 2007). For
example, for character. 118 (the presence/absence of the palmaris
longus) Diogo and Wood (2011) took into account information
obtained from dissections of more than 20 hylobatid, 19 orangutan,
25 gorilla, and 39 chimpanzee specimens. For this character, the
sample size just for apes was >103 specimens.
Primate specimens dissected
Aotus nancymaae: GWUANT AN1, 1 (fresh; adult female). Callithrix jacchus: GWUANT CJ1, 1 (fresh; adult male). Cercopithecus
diana: GWUANT CD1, 1 (fresh; adult female). Colobus guereza:
GWUANT CG1, 1 (fresh; adult male). Gorilla gorilla: CMS GG1, 1
(fresh; adult male); VU GG1, 1 (fresh; adult female). Homo sapiens:
GWUANA HS1-16, 16 (formalin); HU D43, 1 (formalin); HU D45
(formalin). Hylobates gabriellae: VU HG1, 1 (fresh; infant male).
Hylobates lar: HU HL1, 1 (formalin; adult male). Lemur catta:
GWUANT LC1, 1 (fresh; adult male). Loris tardigradus: SDZ LT53090,
1 (fresh; adult male). Macaca fascicularis: VU MF1, 1 (fresh; adult
male). Macaca mulatta: HU MM1, 1 (formalin; adult male). Macaca
silenus: VU MS1, 1 (fresh; adult male). Nycticebus coucang: SDZ
NC41235, 1 (fresh; adult female); SDZ NC43129, 1 (fresh; adult
female). Nycticebus pygmaeus: VU NP1, 1 (fresh; adult female); VU
NP2, 1 (fresh; adult male); SDZ NP40684, 1 (fresh; adult female);
SDZ NP51791, 1 (fresh; adult female). Pan troglodytes: PFA 1016, 1
(fresh; adult female); PFA 1009, 1 (fresh; adult female); PFA 1051, 1
(fresh; infant female); PFA 1077, 1 (fresh; infant female); PFA UNC
(uncatalogued), 1 (fresh; infant male); HU PT1, 1 (formalin; infant
male); GWUANT PT1, 1 (formalin; adult female); GWUANT PT2, 1
(formalin; adult female); VU PT1, 1 (fresh; adult male). Papio anubis
GWUANT PA1, 1 (fresh; adult female). Pithecia pithecia: VU PP1, 1
(fresh; adult male); GWUANT PP1, 1 (fresh; adult female). Pongo
pygmaeus: HU PP1, 1 (formalin; neonate male); GWUANT PP1, 1
(formalin; adult male). Propithecus verreauxi: GWUANT PV1, 1
(fresh; adult female); GWUANT PV2, 1 (fresh; infant female). Saimiri
sciureus: GWUANT SC1, 1 (fresh; adult female). Tarsius syrichta:
CMNH M-3135, 1 (alcohol; adult female).
Results
For each group of muscles (ventral forearm muscles, dorsal
forearm muscles and intrinsic hand muscles), we discuss the results
working from the more inclusive synapomorphic features (e.g.,
Primates, Haplorhini, Anthropoidea, etc.) to those apomorphies
that are only found within H. sapiens (Fig. 1). Detailed tables that
describe and use photographs to illustrate each muscle of each of
the taxa included in the cladogram of Fig. 1 are included in Diogo
and Wood (2012). Detailed descriptions of the phylogenetic characters used and of the synapomorphies obtained in our phylogenetic analyses are given there and in Diogo and Wood (2011).
Ventral forearm musculature
Among the synapomorphic features of the ventral forearm
muscles, the most inclusive is the insertion of the flexor carpi
radialis onto metacarpals II and III (e.g., Fig. 2), which was acquired
in the Haplorhini (Fig. 1, feature 3). In most non-primate eutherian
mammals, the flexor carpi radialis inserts onto metacarpal III (e.g.,
in rats), onto metacarpal II (as is usually the case in e.g., Lemur and
Propithecus), or, in a few cases (e.g., in flying lemurs), onto other
structures, but it does not attach onto both metacarpals II and III, as
it usually does in haplorrhines (and in a few non-primate
mammals, e.g., Tupaia). Two of the synapomorphies of hominoids
concern the flexor digitorum superficialis. In non-hominoid
primates, this muscle originates exclusively from the arm (medial
epicondyle of humerus, common flexor tendon, and/or capsule of
the elbow joint), but in hominoids the muscle usually also originates from the ulna and the radius (Fig. 1, features 10, 11). Another
synapomorphy of hominoids is the loss of the epitrochleoanconeus,
a small muscle that connects the medial epicondyle of the humerus
to the olecranon process of the ulna. This muscle is usually present
(presumably due to a secondary reversion) in chimpanzees (Fig. 1,
feature 12). Plesiomorphically in primates the pronator teres has
a bony origin from the humerus only. In hylobatids, this muscle
originates from the humerus and often, but not usually (i.e., <50%
of the cases), from the ulna (Fig. 1, feature 13). In hominids, the
muscle originates from the humerus and usually (i.e., 50% of the
cases) also from the ulna (Fig. 1, feature 16).
Plesiomorphically, in primates the flexor digitorum profundus
originates from the forearm (ulna, radius, and/or interosseous
membrane) and arm (medial epicondyle and/or common flexor
tendon). In hominids (and also in Macaca as a homoplasy), this
muscle does not originate from the medial epicondyle nor from the
common flexor tendon (Fig. 1, feature 14). In our dissections, the
flexor pollicis longus was present in modern humans and
R. Diogo et al. / Journal of Human Evolution 63 (2012) 64e78
67
Table 1
Scheme illustrating the authors’ hypotheses regarding the homologies of the arm and hand muscles of adults of representative primate taxa; the flexor brevis profundus 2
(which corresponds to the ‘deep head of the flexor pollicis brevis’ of human anatomy) is listed here (and counted) as a distinct muscle, following the works done on numerous
other mammals.
APPEND.: DORSAL FOREARM
APPEND.: VEN. AND DORSAL HAND
APPEND.: VEN. FOREARM
Muscle names
Homo
Lemur
Tarsius
Aotus
Macaca
Hylobates
Pongo
Gorilla
Pan
(49 mus.: 19
(51-55 mus.: 19
(41 mus.: 19
(46 mus.: 19 forearm;
(46 mus.: 19
(38 mus.: 18
(38 mus.: 18
(45 mus.: 19 forearm; (41 mus.: 20
forearm; 30 hand)
forearm; 32-36 hand)
forearm; 22 hand)
27 hand)
forearm; 27 hand)
forearm; 20 hand)
forearm; 20 hand)
26 hand)
Pronator quadratus
P
P
P
P
P
P
P
P
forearm; 21 hand)
P
Flexor dig. profundus
P
P
P
P
P
P
P
P
P
Flexor pollicis longus
---
---
---
---
P
---
---
---
P
Flexor dig. superficialis
P
P
P
P
P
P
P
P
P
Palmaris longus
P
P
P
P
P
P
P
P
P
Flexor carpi ulnaris
P
P
P
P
P
P
P
P
P
Epitrochleoanconeus
P
P
P
P
---
---
---
P
---
Flexor carpi radialis
P
P
P
P
P
P
P
P
P
Pronator teres
P
P
P
P
P
P
P
P
P
Palmaris brevis
P
P
P
P
P
P
P
P
P
Lumbricales 1-4
P
P
P
P
P
P
P
P
P
Contrahentes dig.
P (2mus.)
P (8mus.)
P (3mus.)
P (3mus.)
P (3mus.)
---
---
P (2mus.)
Adductor pollicis
P
P
P
P
P
P
P
P
P
Adductor pollicis access.
---
---
---
---
---
---
---
---
P
Flexor brevis prof. 2
P
P
P
P
P
P
P
P
Fbp. / Int. pal.
Fbp. 3-9 (7 mus.)
Int. dor. 1-4
---
Fbp. 3-9 (7 mus.)
---
Flexor pollicis brevis
P
Opponens pollicis
P
--Int. pal.1-3 (fbp 4,7,9)
Fbp.3-9 (7 mus.)
P
---
P
P
P
P
P
P
Int. pal.1-3 (fbp 4,7,9)
P
P
P
Int. pal.1-3 (fbp 4,7,9)
P
Int. pal.1-3 (fbp 4,7,9)
Fbp.3-9 (7 mus.)
---
Int. pal.1-3 (fbp 4,7,9)
P
---
P
P
P
P
P
P
P
P
P
Flexor digiti mi. brevis
P
P
P
P
P
P
P
P
P
Opponens digiti mi.
P
P
P
P
P
P
P
P
P
Abductor pollicis brevis
P
P
P
P
P
P
P
P
P
Abductor digiti mi.
P
P
P
P
P
Intermetacarpales 1-4
P
P
Int. accessorii (4 mus.)
P
Extensor carpi ra. longus
P
P
Extensor carpi ra. brevis
P
P
P
P
P
---
---
P
---
P
---
---
P
P
P
P
P
P
P
P
P
P
P
---
P
---
---
P
P
P
P
?
---
---
---
Brachioradialis
P
P
P
P
P
P
P
P
P
Supinator
P
P
P
P
P
P
P
P
P
Extensor carpi ulnaris
P
P
P
P
P
P
P
P
P
Anconeus
P
P
P
P
---
P
P
P
P
Extensor digitorum
P
P
P
P
P
P
P
P
P
Extensor digiti mi.
P
P
P
P
P
P
P
P
P
Extensor indicis
P
P
P
P
P
P
P
P
P
Extensor pollicis longus
P
P
P
P
P
P
P
P
P
Abductor pollicis longus
P
P
P
P
P
P
P
P
P
Extensor pollicis brevis
---
---
---
---
P
---
---
---
P
The nomenclature of the muscles follows that of Diogo and Abdala (2010) and Diogo and Wood (2011, 2012). Data from evidence provided by our own dissections and comparisons and by a
review of the literature. The black arrows indicate the hypotheses that are most strongly supported by the evidence available; the grey arrows indicate alternative hypotheses that are supported by
some of the data, but overall they are not as strongly supported by the evidence available as are the hypotheses indicated by black arrows. APPEND. = appendicular; P = muscle present; VEN.
= ventral; --- = muscle absent; access. = accessorius; dig. = digitorum; dor. = dorsales, fbp. = flexores breves profundi; mi. = minimi; mus. = muscles; pal. = palmares; pre. =
present in; prof. = profundus; ra. = radialis; int. = interossei.
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R. Diogo et al. / Journal of Human Evolution 63 (2012) 64e78
Figure 3. Hylobates gabriellae (VU HG1, infant male): ventral view of the left flexor
digitorum profundus (to digits 2e5) and flexor pollicis longus (to digit 1); note that the
tendon of the former muscle to digit 2 also receives a small contribution from the
tendon of the latter muscle to digit 1.
Figure 2. Hylobates lar (HU HL1, adult male): ventral view of the left forearm
musculature. Note the distinct muscle flexor pollicis longus. In this and the following
figures, PRO, MED, LAT and DIS mean proximal, medial, lateral and distal, respectively.
hylobatids (Table 1, Fig. 1, feature 21; Figs. 2e4), confirming
observations by previous researchers (e.g., Deniker, 1885;
Hartmann, 1886; Kohlbrügge, 1890-1892; Hepburn, 1892; Keith,
1894b; Chapman, 1900; McMurrich, 1903a, b; Sonntag, 1924b;
Howell, 1936a, b; Straus, 1942a; Jouffroy and Lessertisseur, 1960;
Tuttle, 1969; Jouffroy, 1971; Van Horn, 1972; Lorenz, 1974; Marzke,
1992, 1997; Susman, 1994, 1998; Stout, 2000; Tocheri et al., 2008).
This is a potential example of parallelism in that from a similar
ancestral configuration (i.e., the flexor digitorum profundus going
to the distal phalanges of digits 1e5), there is an independent
acquisition of a similar derived feature (differentiation of the belly
of the flexor digitorum profundus going to digit 1, to form a separate flexor pollicis longus muscle). The belly of the flexor pollicis
longus is distinct from the flexor digitorum profundus in all of the
modern humans and the two hylobatids dissected by us (Fig. 2), but
in the H. gabriellae (VU HG1) male infant there is a distal tendinous
connection between the tendon of the former muscle and the
tendon of the latter muscle that goes to digit 2 (Fig. 3; N.B., Fig. 2
shows some tissue that appears to run distally from the most
lateral flexor digitorum profundus tendon to the flexor pollicis
longus tendon just proximal to the wrist, but careful dissection
established that there is no fleshy or tendinous connection between
these two muscles in the photographed specimen). This connection
reflects the ancestral, and probably embryonic, condition where
these two muscles form a single structure (Diogo and Wood, 2011).
In the 18 modern humans dissected by us, we did not see as strong
a tendinous distal connection between the two muscles as we
found in the gibbon infant, but according to Lindburg and Comstock
(1979) 31% of modern humans display some type of connection
between these two muscles (see below). In the great apes, the
tendon of the flexor digitorum profundus to digit 1 is often either
a very thin, vestigial structure or it is absent (Fig. 5). According to
the results of our cladistic analysis, it is more parsimonious to infer
that this tendon became reduced in the last common ancestor
(LCA) of hominids and became fully developed again in the Hominina (two steps) than to conclude that it became reduced independently in orangutans, gorillas and chimpanzees (three steps)
(Fig. 1, features 15 and 21). However, in this case there are reasons
to suggest that the cladistically less parsimonious hypothesis may
be the most likely evolutionary hypothesis (see Discussion below).
Apart from the presence of a distinct flexor pollicis longus,
modern humans also show a reversion of the character state ‘Flexor
carpi radialis originates from the radius’ (Fig. 1, feature 23). Unlike
the condition in modern humans (i.e., the only bony origin is from
the medial epicondyle of the humerus), in great apes the flexor
carpi radialis muscle also originates from the radius. However, it is
not clear which is the usual condition for hylobatids, and, thus,
whether a radial origin constitutes a synapomorphy of hominoids
or of hominids. Hepburn (1892) and Kohlbrügge (1890-1892) noted
a partial origin of flexor carpi radialis from the radius in various
hylobatid species, as we did in our H. gabriellae and H. lar specimens, but other authors (e.g., Michilsens et al., 2009) have reported
an exclusive origin from the humerus in species such as H. pileatus,
H. moloch and H. syndactylus.
R. Diogo et al. / Journal of Human Evolution 63 (2012) 64e78
69
Figure 4. Homo sapiens. A) HU D43 (adult female): ventral view of the right hand, showing that some branches of the deep branch of the ulnar nerve run mainly distally to
innervate the dorsal and palmar interossei, while other branches run mainly laterally to innervate the oblique head of the adductor pollicis and then the adductor pollicis
accessorius (or ‘interosseous volaris primus of Henle’ of modern human anatomy; see Fig. 4B). Note that in this hand, as well as in all the other modern human hands dissected
exhibiting an adductor pollicis accessorius, the oblique head of the adductor pollicis, the so-called ’deep head of the flexor pollicis brevis’ (flexor brevis profundus 2 sensu the
present work) and the adductor pollicis accessorius are all present, so the adductor pollicis accessorius should clearly not be confused with the so-called ’deep head of the flexor
pollicis brevis’, as it is sometimes done in the literature (see also Discussion). B) HU D45 (adult female): dorsal view of the right hand showing the innervation of the adductor
pollicis accessorius from the branches of the deep branch of the ulnar nerve that innervate the oblique head of the adductor pollicis.
All of the non-Homininae (non-African ape and modern human)
primates, as well as the non-primate mammals dissected by us,
have a palmaris longus (e.g., Fig. 2). In gorillas, chimpanzees and
modern humans, the palmaris longus is missing in at least 5% of the
cases (Fig. 1, feature 18). The reviews of Keith (1899), Loth (1931),
Sarmiento (1994) and Gibbs (1999) indicate that a palmaris longus
is present in 64%, 15%, 36% and 31% of gorillas, respectively, and in
75%, 95%, 91% and 68% of chimpanzees, respectively, and more
recent literature indicates that the muscle is present in 85% of
modern humans (e.g., Gibbs, 1999; Gibbs et al., 2000, 2002).
Dorsal forearm musculature
With respect to the dorsal forearm muscles, an inclusive synapomorphy of anthropoids is the presence of both ulnar and
humeral heads of the supinator (Fig. 1, feature 6). The
plesiomorphic state in mammals (e.g., Tupaia, Rattus and Cynocephalus) and in primates (e.g., Lemur, Propithecus and Tarsius) is
a single humeral head. Lorisiformes have independently acquired
an ulnar head and thus they resemble anthropoids in that they have
both humeral and ulnar heads. The other two forearm extensor
apomorphies are much less inclusive. One, which characterizes the
Homininae, is the exclusive insertion of the extensor indicis onto
digit 2 (Fig. 1, feature 20). In other primates and in most other
mammals, this muscle usually goes to more than one digit (e.g.,
Fig. 7; N.B., other authors use names such as ‘extensor indicis et
tertius’ when the muscle goes e.g., to digits 2 and 3, but we follow
the nomenclature of Diogo and Wood, 2012, who pointed out that
the muscle should still be designated as extensor indicis in those
cases in order to stress the homology of the muscle, whether it goes
to a single digit or not). The other forearm extensor apomorphy,
which characterizes the extant Hominina (and also the
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R. Diogo et al. / Journal of Human Evolution 63 (2012) 64e78
Figure 5. Gorilla gorilla (CMS GG1, adult male): ventral view of the oblique and
transverse heads of the right adductor pollicis, as well as of the adductor pollicis
accessorius (or ‘interosseous volaris primus of Henle’ of modern human anatomy).
Hylobatidae, likely due to an independent acquisition; Table 1 and
Fig. 1, feature 25) is the presence of a distinct extensor pollicis
brevis (e.g., Fig. 7). The presence of this muscle in both modern
humans and the Hylobatidae is another example of a parallelism in
that a similar ancestral configuration (i.e., the abductor pollicis has
two distal tendons in most other primates; see Fig. 8 and below)
results in a similar, homoplasic, derived configuration (in which the
abductor pollicis longus gives rise to a new distinct muscle, the
extensor pollicis brevis: see below).
Intrinsic hand musculature
Regarding the intrinsic hand muscles, inclusive synapomorphies
include the presence of an opponens pollicis and an opponens digiti
minimi (Table 1) that were acquired in the node leading to the
Primates (Fig. 1, features 1, 2). The opponens pollicis became
secondarily undifferentiated in a few primates (e.g., Callithrix) and
one, or both, of these muscles may be present in some non-primate
mammals such as rats. Strepsirrhines and most non-primate
mammals have an undivided adductor pollicis. In the node
leading to haplorrhines, this muscle became partly divided into
transverse and oblique heads (Fig. 1, feature 5), and then in the node
leading to catarrhines the muscle became further divided into wellseparated transverse and oblique heads (Fig. 1, feature 7) (e.g.,
Figs. 4and 5). Another synapomorphy of haplorrhines is the presence of more than two contrahentes digitorum (i.e., other than the
adductor pollicis, which derives evolutionary from the ancestral
contrahens to digit 1; Table 1, Fig. 1, feature 4). The plesiomorphic
condition for primates (e.g., Lemur, Propithecus, Loris and Nycticebus)
Figure 6. Pan troglodytes (GWUANT PT2, adult female): ventral view of the right
flexores breves profundi 3e9 (pulled back) and the intermetacarpales 1e4; contrary to
other hominoids, in Pan the flexores breves profundi 3, 5, 6 and 8 and the intermetacarpales 1, 2, 3 and 4 usually do not fuse in order to form the interossei dorsales 1,
2, 3 and 4 (as in other hominoids, the flexores breves profundi 4, 7 and 9 correspond to
the interossei palmares 1, 2 and 3).
as well as in non-primate taxa such as Rattus, Tupaia and Cynocephalus, is to have only two contrahentes digitorum (usually to
digits 2 and 5; Table 1). A synapomorphy of the Hominidae is the
absence of contrahentes digitorum (Fig. 1, feature 17), but in the
node leading to Pan there was a reversion to the plesiomorphic
primate condition (i.e., adult chimpanzees usually have two contrahentes digitorum, but unlike in strepsirrhines these muscles
usually go to digits 4 and 5: Table 1; N.B., the chimpanzees dissected
by us have contrahentes, although in some cases the fleshy part of
these muscles was markedly reduced: for more details see, e.g.,
Diogo and Wood, 2012, in press). Another reversion that differentiates Pan from the other members of the Hominidae, as well as from
hylobatids and New World monkeys is the presence of four intermetacarpales (i.e., the flexor brevis profundi and intermetacarpales
do not fuse to form the dorsal interossei) each connecting adjacent
metacarpals (Table 1, Fig. 6; see Discussion below).
Apart from the presence of well-separated oblique and transverse heads of the adductor pollicis (see above) catarrhines are
characterized by two synapomorphies. First, contrary to the plesiomorphic primate condition in which the opponens pollicis
inserts onto the proximal and/or middle surfaces of the metacarpal
I, in catarrhines (and homoplasically also in the Lorisiformes) the
opponens pollicis reaches the distal margin of this bone (Fig. 1,
feature 8). Second, in catarrhines the opponens digiti minimi is
divided into superficial and deep bundles, while in other primates
and most other mammals this muscle is undivided (Fig. 1, feature 9).
According to our comparative and phylogenetic analyses, one of
the synapomorphies of the Homininae (African great apes and
modern humans) is that the ‘volar interosseus of Henle’ (or ‘interosseous volaris primus of Henle’), which very likely derives from
R. Diogo et al. / Journal of Human Evolution 63 (2012) 64e78
71
Figure 8. Gorilla gorilla (CMS GG1, adult male): dorsal view of the two tendons of the
left abductor pollicis longus, one going to the proximo-lateral margin of the proximal
phalanx of digit 1 (thus probably corresponding to the tendon of the extensor pollicis
brevis of humans), the other going to the proximo-lateral margin of metacarpal I (thus
probably corresponding to the tendon of the abductor pollicis longus of humans).
interosseous of Henle’ and the extensor pollicis brevis) have been
considered to be uniquely, or almost uniquely, found in modern
humans. Below we provide a discussion of these structures and of
the other forearm and hand structures to which they are anatomically and functionally associated, and consider their functional and
evolutionarily significance in light of evidence from the fossil
record and from biomechanical analyses.
Flexor pollicis longus
Figure 7. Hylobates lar (HU HL1, adult male): dorsal view of the left forearm musculature; note the distinct muscle extensor pollicis brevis.
a thin deep additional slip of the adductor pollicis (Diogo and
Wood, 2011), is often (c. < 50% of cases) present (Fig. 1, feature
19), whereas in other primates and other mammals this muscle is
nearly always, or always, absent. This synapomorphic Homininae
condition where the muscle is often but not usually present (i.e.,
c. < 50% of cases) is seen in chimpanzees and gorillas (e.g., Fig. 5).
Modern humans display an autapomorphic condition within the
Homininae because the muscle is found in most (50%) of the cases
(see Table 1; Fig. 1, feature 24; Fig. 4).
Discussion
Four forearm and hand muscles (flexor pollicis longus, the socalled ‘deep head of the flexor pollicis brevis’, the so-called ‘volar
In modern humans, the flexor pollicis longus is innervated by
the anterior interosseous nerve and it usually runs from the ventral
surface of the radius and the interosseous membrane to the distal
phalanx of the thumb. The different nomenclatures used to
describe this muscle have resulted in some confusion. Day and
Napier (1963) suggested that the flexor pollicis longus is present
in Loris, Nycticebus, Tarsius, Aotus, Callithrix, Saimiri, Macaca, Cercopithecus, Colobus, Papio and Homo, and this was the view that
informed the cladistic studies of Groves (1986) and Shoshani et al.
(1996). However, Day and Napier (1963) intended the term’s
traditional usage (e.g., Barnard, 1875; Duckworth, 1904, 1915; Wood
Jones, 1920; Sonntag, 1924a, b), which is to indicate the presence of
a tendon of the flexor digitorum profundus to digit 1. They did not
necessarily imply the presence of a distinct flexor pollicis longus
muscle (i.e., separated from the flexor digitorum profundus, with
a tendon exclusive to the thumb). In the Loris, Nycticebus and Tarsius specimens dissected by Burmeister (1846), Mivart and Murie
(1865), Murie and Mivart (1872), Keith (1894a, b), Allen (1897),
Woollard (1925), Miller (1943), Schultz (1984) and by us, the Aotus,
Callithrix and Saimiri specimens studied by Senft (1907), Beattie
(1927), Hill (1957, 1960, 1962) and by us, the Macaca specimens
examined by Haughton (1864, 1865), Howell and Straus (1932,
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R. Diogo et al. / Journal of Human Evolution 63 (2012) 64e78
1933), Patterson (1942), Jacobi (1966), Kimura and Tazai (1970),
Jouffroy (1971) and Landsmeer (1986) and by us, the Cercopithecus
specimens investigated by Hill (1966) and Lewis (1989) and by us,
the Colobus specimens dissected by Brooks (1886), Polak (1908),
Jouffroy and Lessertisseur (1960) and by us, and in the Papio
specimens studied by MacDowell (1910), Hill (1970), Swindler and
Wood (1973), Tocheri et al. (2008) and by us there is no distinct
flexor pollicis longus going exclusively to digit 1 (Table 1). Thus, the
apparently contradictory statements in the literature about the
presence/absence of a flexor pollicis longus in non-hominoid
primates are mainly the result of nomenclatural pluralism and
they should not be used as the basis of cladistic character states
without additional clarification.
Our dissections confirm previous reports that in most nonhominoid primates the flexor digitorum profundus sends
a tendon to digit 1. However, it is not independent of the tendons
going to the other digits even though, when it is present, it flexes
the distal phalanx of the thumb in the same way that the flexor
pollicis longus does in modern humans. In the great apes, the flexor
digitorum profundus tendon to digit 1 is usually either vestigial or
even absent (e.g., Fig. 5). Straus (1942b) showed, using evidence
from both his own dissections and from data available to him in the
literature, that among 47 chimpanzees such a tendon was absent in
14 individuals (30%), too small/thin to have had any useful function
in 10.5 individuals (22%), and was in direct functional continuity
with the radial muscle belly of the flexor digitorum profundus in 22
individuals (48%). Likewise, among 16 gorillas Straus (1942b)
showed that this tendon was absent in five individuals (31%),
rudimentary in six individuals (41%), and present in four individuals (28%). Among 27 orangutans, the tendon was absent in 24
individuals (89%), rudimentary and functionless in two individuals
(7%) and only completely developed in one individual (4%). Thus,
there is no functioning tendon in c. 95% of orangutans, in c. 72% of
gorillas and in c. 50% of chimpanzees.
In hylobatids, the anatomy of the flexor pollicis longus is more
complex. Our de novo dissections (Table 1; Figs. 2e4) confirm that
both modern humans and hylobatids have a flexor pollicis longus
distinct from the flexor digitorum profundus, unlike the
extensively-connected muscle bellies seen in other primates
(corroborating the descriptions of authors such as Deniker, 1885;
Hartmann, 1886; Kohlbrügge, 1890-1892; Hepburn, 1892; Keith,
1894b; Chapman, 1900; McMurrich, 1903a, b; Sonntag, 1924b;
Howell, 1936a, b; Straus, 1942a; Jouffroy and Lessertisseur, 1960;
Tuttle, 1969; Jouffroy, 1971; Van Horn, 1972; Lorenz, 1974; Marzke,
1992, 1997; Susman, 1994, 1998; Stout, 2000; Tocheri et al., 2008).
However, a few authors (e.g., Payne, 2001) suggest that in the
Hylobates specimens dissected by them the flexor pollicis longus
blends with, and is thus not really separate from, the flexor digitorum profundus.
In an influential paper about the evolution of tool use in the
Hominina, Susman (1994: 1573, Fig. 3) stated that contrary to the
condition in modern humans, chimpanzees and other primates
have only a tendon that mimics the flexor pollicis longus and lacks
a separate muscle belly; “in lesser apes (gibbons and siamang)
there is a muscle belly, but it is functionally coupled with the flexor
digitorum produndus.electromyography experiments on an adult
female gibbon (H. lar) did not elicit flexion of the thumb separate
from flexion of the fingers, as is the case in humans”. The apparent
inconsistency between Susman’s interpretation and the interpretations of researchers who have described the hylobatid flexor
pollicis longus as distinct (e.g., Marzke, 1992) is likely due to the
variable presence of a connective tissue ‘shunt’ (Tuttle, 1969) that
connects the tendons of the flexor digitorum profundus and flexor
pollicis longus (Tuttle (1969) referred to it as the ‘radial component
of the flexor digitorum profundus musculature’) often at the level of
the carpus in hylobatids. This shunt, which is commonly less
substantial than the tendons it connects, is a slender flat (4e5 mm
wide) structure that passes obliquely inferomedially from the
tendon of the flexor pollicis longus to the lateral edge of the
common flexor digitorum profundus tendons to digits 2e5.
According to Tuttle, the ’flexor shunt’ probably serves different
functions during the various activities undertaken by hylobatids.
For instance, he suggested that when the hand is used as an
anatomical hook during vigorous arm-swinging, the ‘shunt’ probably transfers some of the contractile force of flexor pollicis longus
to the flexor digitorum profundus tendons and thereby helps to
stabilize the wrist. In contrast, when the hand is used for fine
manipulation, particularly when the metacarpophalangeal joints of
digits 2e5 are flexed, the ‘shunt’ is probably somewhat slack,
allowing the flexor pollicis longus to independently flex the distal
phalanx of the thumb. When the thumb is abducted to grasp large
branches, the ‘shunt’ is probably also stretched to the extent that
the distal phalanges of the thumb and the medial four digits are
flexed synchronously to produce secure grips. As a result, and
contrary to what occurs in Pan, Pongo and Gorilla, in hylobatids the
pollex normally plays an active role in maintaining a suspended
posture and in facilitating the distinctive locomotion of these
hominoids. After observing living animals, Van Horn (1972) suggested that the flexor pollicis longus of hylobatids is important
during the arm-pull phase of climbing, in which the terminal
phalanx of the thumb is flexed as the animal lifts its weight from
a previous support (i.e., this muscle is an important component of
the power used to grasp). Stout (2000) found that the tendon of the
flexor pollicis longus of hylobatids does not flex the distal phalanx
of the thumb, but instead it adducts the thumb, flexes the pollical
metacarpophalangeal joint and stabilizes the pollical interphalangeal joint. Further functional studies of hylobatids are needed to
test these hypotheses, particularly because even among modern
humans there is significant variation with respect to the presence of
a fully independent flexor pollicis longus. For instance, as explained
above according to an extensive review undertaken by Lindburg
and Comstock (1979), only c. 70% of modern humans have
a flexor pollicis longus that is anatomically entirely independent
from the flexor digitorum profundus. Shrewsbury et al. (2003)
posited that evidence of restrictive thumb/index tendosynovitis
and pain in modern humans is usually associated with connections
between the flexor pollicis longus and the flexor digitorum profundus. In some cases, the condition can be relieved by removing
the connection between these muscles and occasionally the
thickened flexor pollicis longus must be removed as well. According
to Shrewsbury et al. (2003), the repetitive force used in a precision
grip in concert with habitual repetitive behaviours associated with
precision handling might have favoured independence of these two
muscles as modern humans became increasingly dependent on the
dexterity required to make and use tools.
There are reasons to consider that the tendon of the flexor
digitorum profundus to digit 1 became independently reduced in
orangutans, gorillas and chimpanzees, while the presence of
a separate, robust flexor pollicis longus in hylobatids and modern
humans may be associated with having a well-developed and/or
functionally more independent thumb. The first hypothesis is
supported by the fact that the tendon of the flexor digitorum profundus to digit 1 is highly variable in great apes. In a few cases it is
fully developed, in others it is atrophied, in others it is ‘rudimentary’ and may no longer attach to the main body of the flexor digitorum profundus muscle, and in others it is completely missing
(see above and also, e.g., Shrewsbury et al., 2003, Fig. 5). Straus
(1942b) included those cases where there is no continuity with
the main body of the flexor digitorum profundus in the category of
rudimentary, vestigial or functionless tendon to digit 1. However, it
R. Diogo et al. / Journal of Human Evolution 63 (2012) 64e78
is important to note that, as stressed by Shrewsbury et al. (2003),
the tendon is not necessarily functionless in all of those cases.
Within the specimens dissected by them, the tendon had an
attachment pattern that was ligament-like in all four specimens of
orangutan, two of the chimpanzees, and the two juvenile hamadryas baboons. The tendon attached distally to the pollical distal
phalanx and laterally to the radial and ulnar basal tubercles. Tendon
fibres in the hamadryas baboons had distal attachments to the
ungual pulp over the distal phalangeal tuberosity. However, the
proximal radial and ulnar bands of the tendon both sent branches
to the metacarpophalangeal joint in the region of the adductor
pollicis insertion, and also (in the apes) in the region of the flexor
pollicis brevis insertion. No fibres were found continuing further
proximally over the wrist to the radial aspect of the flexor digitorum profundus tendon. According to Shrewsbury et al. (2003),
this distal tethering of the tendon to digit 1 to bone on both sides of
the distal interphalangeal joint probably helps to stabilize the joint.
The hypothesis that the presence of a separate, robust flexor
pollicis longus in hylobatids and modern humans may be associated with having a well-developed and/or functionally more
independent thumb is in line with the results of electromyography
(Marzke et al., 1998) and hand pressure studies (Rolian et al., 2011;
Williams et al., 2012) when various modern human subjects were
manufacturing and using Oldowan tools as well as other objects.
The recruitment of the flexor pollicis longus and the extensor
pollicis brevis allowed the subjects to maintain the metacarpophalangeal joint in extension (using the extensor pollicis
brevis, which in modern humans usually attaches onto the proximal phalanx of the thumb: see below), while simultaneously using
the flexor pollicis longus to flex the distal phalanx of the thumb at
the pollical interphalangeal joint. The results from experiments
documenting hand pressure during stone tool making underscore
the importance of hand posture on the distribution of pressure
across the thumb and other digits (Williams et al., 2012),
supporting the suggestions of Marzke et al. (1998) suggestion that
the differentiation of these two muscles needed to have occurred
for early members of the human lineage to be able to habitually
make effective stone tools.
Evidence from the fossil record also lends some support to the
hypothesis that a well-developed tendon to digit 1, whether as part
of flexor digitorum profundus or as a separate flexor pollicis longus,
was the primitive condition for the Hominoidea and probably the
Pan-Homo LCA. While some (Shrewsbury et al., 2003; Marzke and
Shrewsbury, 2006; Tocheri et al., 2008) have noted that the flexor
pollicis longus (or flexor digitorum profundus to digit 1) does not
insert onto the distal phalanx’s volar pit, or ‘proximal volar fossa’
(Shrewsbury et al., 2003), it is clear that the tendon inserts on the
ridge that is, when present, just distal to the fossa (Susman, 1998;
Shrewsbury et al., 2003). The presence of an attachment (ridge) to
the distal pollical phalanx is seen in all of the fossil hominoid taxa
known to date, including Proconsul (Begun et al., 1994) and Oreopithecus (Moyà-Solà et al., 1999). Similarly, all fossil pollical thumb
distal phalanges attributed to (pre-modern) Homo show evidence
of a volar ridge, with an accompanying proximal volar fossa
(Shrewsbury et al., 2003) that marks the attachment of a tendon
(Susman, 1998). The attachment site is also present on the distal
pollical phalanges of both early and potential fossil taxa of the
subtribe Hominina, including Orrorin tugenensis (Gommery and
Senut, 2006; Almécija et al., 2010), Ardipithecus ramidus (Lovejoy
et al., 2009), and. Australopithecus afarensis (Ward et al., in press).
Whether Orrorin is a member of the subtribe Hominina (Senut
et al., 2001; Richmond and Jungers, 2008) or not (e.g., Wood and
Harrison, 2011), the clear indication of a tendon insertion on the
distal pollical phalanx at almost six million years ago suggests
that either 1) the presence of tendon to digit 1 was present in the
73
Pan-Homo LCA, is retained in the Hominina, and independently lost
in the evolution of Pan and Gorilla (and possibly Pongo), or 2) that
the Pan-Homo LCA lacked the tendon insertion, and that it evolved
rapidly at the base of the Hominina clade independently of its
evolution in hylobatids. In either scenario, the evolution of the
flexor pollicis longus in hominoids involves homoplasy. In a recent
paper, Almécija et al. (in press) strongly support the idea that the
plesiomorphic hominoid, hominid and hominin condition is very
likely a moderately long thumb, longer than the thumb of modern
great apes, thus indirectly supporting the idea that the tendon of
the flexor digitorum profundus to digit 1 became independently
reduced in orangutans, gorillas and chimpanzees.
Some time between the late Pliocene and early Pleistocene, the
thumb of the members of the subtribe Hominina evolved significantly greater robusticity, the thumb of modern humans being more
robust than that of any other extant hominoids, including hylobatids (Susman, 1994). However, the hypothesis remains untested
regarding whether other derived muscular features of the modern
human hand occurred with the evolution of thumb robusticity.
Deep head of the flexor pollicis brevis and the ‘volar interosseous of
Henle’
In modern humans, the so-called ‘deep head of the flexor pollicis brevis’ usually runs from the carpal region (e.g., capitate,
occasionally from trapezoid) to the medial side of the palmar
surface of proximal phalanx of digit 1 and/or an adjacent sesamoid
bone (e.g., Fig. 4) and it is normally innervated by the deep branch
of the ulnar nerve (and/or occasionally by the median nerve). The
so-called ‘volar interosseous of Henle’ usually runs from the base of
metacarpal I to the ‘wing tendon’ of the extensor apparatus of digit
1 (e.g., Susman et al., 1999). In the specimens examined by us, this
latter structure, which is normally innervated by the deep branch of
the ulnar nerve, may also originate from the carpal bones adjacent
to metacarpal I and its insertion onto digit 1 may extend onto the
proximal phalanx and/or sesamoid bone of the thumb (e.g., Fig. 4).
Susman (1994; Fig. 3) suggested that the ’deep head of the flexor
pollicis brevis’ and the ’interosseous volaris primus of Henle’ (as
described above) are derived in modern humans. However, our
comparative investigation suggests that the ‘deep head of the flexor
pollicis brevis’ is present in most primates, while the volar interosseous of Henle is seen in <50% of a few primates including
gorillas and chimpanzees (e.g., Fig. 5). Lewis (1989) embraced the
hypothesis of Forster (1917) who suggested that the plesiomorphic
condition for eutherian mammals is to have ten flexores breves
profundi, each inserting onto the lateral and medial sides of each
digit, and four intermetacarpales (see, e.g., Fig. 6) connecting the
adjacent metacarpal bones. In primates, the plesiomorphic condition is the same, but two of the 14 muscles have differentiated, each
forming two muscles: the flexor pollicis brevis and the opponens
pollicis from flexor brevis profundus 1, and the flexor digiti minimi
brevis and the opponens digiti minimi from flexor brevis profundus
10 (Fig. 1, Table 1). In hominoids other than chimpanzees, as well as
in New World monkeys, the flexores breves profundi 3, 5, 6 and 8
usually fuse with the intermetacarpales 1, 2, 3 and 4 to form the
dorsal interossei 1, 2, 3 and 4, respectively, whereas the palmar
interossei 1, 2 and 3 are derived directly from the flexores breves
profundi 4, 7 and 9, respectively. The model of Lewis (1989), model,
which explains why the dorsal interossei muscles are bipennate
whereas the palmar interossei are unipennate, is supported by the
developmental studies of authors such as Cihák (1972), which point
out that at least some flexores breves profundi effectively become
fused ontogenetically with the most dorsal intrinsic muscles of the
hand (the intermetacarpales), forming the dorsal interossei of adult
modern humans. Chimpanzees have undergone a secondary
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R. Diogo et al. / Journal of Human Evolution 63 (2012) 64e78
reversion to the plesiomorphic state, probably because their flexores breves profundi do not fuse with the intermetacarpales during
ontogeny to form the dorsal interossei (Table 1; Fig. 6). As explained
above, chimpanzees also display a secondary reversion of a synapomorphy of the Hominidae in that adult chimpanzees have two
contrahentes digitorum in addition to the the adductor pollicis, one
going to digit 4 and the other to digit 5 (in other adult hominids
there is usually none). Because the studies of Cihák (1972) suggest
that in at least modern humans the contrahentes are lost (i.e.,
‘reabsorbed’) during ontogeny, the presence of metacarpales and of
contrahentes in chimpanzees is very likely due to a prolonged or
delayed development of the hand musculature of these apes, i.e., in
this particular case extant chimpanzees are seemingly more
neotenic than modern humans (Diogo and Wood, in press). This is
in line with other recent studies that have pointed out that
although in the literature it is often stated that modern humans are
in general more neotenic than other primates, the empirical data
collected in the last decades reveal that both paedomorphic and
peramorphic processes have been involved in the mosaic evolution
of humans and of other hominoids (see, e.g., Bufill et al., 2011; and
references therein).
The main controversy concerning the evolution and taxonomic
distribution of the so-called ‘deep head of the flexor pollicis brevis’
and of the volar interosseous of Henle mainly concerns the identity
of one of the flexores breves profundi (i.e., number 2, which plesiomorphically in mammals goes to the ulnar side of digit 1).
Although the so-called ‘volar interosseous of Henle’ is usually not
shown in modern human anatomical atlases, it is present in the
majority of modern humans. For example, Abramowitz (1955),
Lewis (1989), Susman et al. (1999), Henkel-Kopleck and Schmidt
(2000) and Morrison and Hill (2011) report the presence of volar
interosseous of Henle in 100%, 92%, 86%, 69%, and 91%, respectively,
of the individuals examined. This structure was also found in the 18
modern human individuals examined in this study (GWUANA HS16, HU D43 and HU D45; Fig. 4).
As the alternative name ‘interosseous volaris primus’ indicates,
some authors consider that this structure, (e.g., Figs. 4and 5; see
below) corresponds to a vestigial flexor brevis profundus 2 (i.e., it is
a fourth, and most radial, palmar interosseus). However, our
comparative and phylogenetic analyses strongly suggest that the
‘interosseous volaris primus’ corresponds instead to a structure
that is derived from a thin, deep additional slip of the adductor
pollicis (Diogo and Wood, 2011) that we suggest should instead be
named the adductor pollicis accessorius (see below and Table 1). In
fact, the ‘interosseous volaris primus’ often blends with the
adductor pollicis distally (see Diogo and Wood, 2011, 2012) and, at
least in modern humans, it is innervated by the branches of the
deep branch of the ulnar nerve that innervate the adductor pollicis
(and not by the branches of this deep branch that innervate the
dorsal and ventral interossei: Fig. 4; Bello-Hellegouarch et al.,
submitted). Moreover, contrary to the statements of some authors
(e.g., Susman, 1994), our analyses revealed that the so-called ‘deep
head of the flexor pollicis brevis’ of modern human anatomy is
present in the vast majority of primates and that it corresponds to
the flexor brevis profundus 2 of other mammals (Table 1; Diogo and
Wood, 2011, 2012). For example, the structure designated as the
flexor brevis profundus 2 in rats is the structure that is designated
as ‘deep head of the flexor pollicis brevis’ of modern humans. Such
a structure is also found in the vast majority of non-human
primates, except for the New World monkeys in which this structure is either missing or, more likely, has fused with the flexor
brevis profundus 1 component of the ‘superficial head of the flexor
pollicis brevis’ of these monkeys. As Diogo and Wood (2011) argue,
most authors have found a flexor brevis profundus 2 in the nonhuman and non-platyrrhine primates, but many have erroneously
designated this structure either a component of the adductor pollicis or they have referred to it as the ‘interosseous volaris primus of
Henle’. Linscheid et al. (1991) have designated the adductor pollicis
accessorius sensu the present paper as the ‘accessory adductor
muscle’ or the ‘adductor pollicis accessory’, but their study is
somewhat confusing because despite using this name they clearly
consider that this muscle corresponds to the flexor brevis profundus 2, and not to part of the adductor pollicis, of other mammals
(see, e.g., their Fig. 8). According to the authors, the adductor pollicis accessorius sensu the present paper is present in all eight
modern human hands dissected by them, inserting onto the ulnar
wing tendon of the thumb; the origin is from metacarpal 1 in four
hands, from metacarpals 1 and 2 in two hands, from metacarpal 2
in one hand, and from the trapezium in one hand. Contrary to the
hypothesis defended in the present paper, they thus consider that
the ‘deep head of the flexor pollicis brevis’ of modern human
anatomy corresponds to part of the oblique head of the adductor
pollicis, and not to the flexor brevis profundus 2, of other mammals.
Moreover, they use the name ‘adductor pollicis, accessory oblique
head’ to designate an extra head of the adductor pollicis that is
present in six of the eight modern human hands dissected by them
and that originates from metacarpal 2.
In summary, our comparative and phylogenetic analyses indicate
that the flexor brevis profundus 2 has been present and has basically
kept the same anatomical configuration from the LCA of eutherian
mammals to H. sapiens, where it forms the so-called ‘deep head of
the flexor pollicis brevis’. The names ‘deep head of the flexor pollicis
brevis’ and ‘superficial head of the flexor pollicis brevis’ are thus
inappropriate and in our opinion should be abandoned, because the
former corresponds directly to the flexor brevis profundus 2 of other
mammals while the latter derives from the flexor brevis profundus 1
(the opponens pollicis being also derived from the flexor brevis
profundis 1: see above and Table 1). We propose that the ‘deep head
of the flexor pollicis brevis’ and ’superficial head of the flexor pollicis
brevis’ are therefore designated as flexor brevis profundus 2 and as
flexor pollicis brevis, respectively (see, e.g., Fig. 4; Table 1). As we
have argued above, the ‘volar interosseous of Henle’ of modern
humans does not correspond to the flexor brevis profundus 2 of
other mammals (i.e., it is not a true palmar interosseus), but instead
it is very likely derived from the adductor pollicis (Fig. 9; Table 1:
adductor pollicis accessorius; see below).
Extensor pollicis brevis
In modern humans, the extensor pollicis brevis, which is
innervated by the posterior interosseous nerve, usually runs from
the dorsal surface of the radius and the adjacent interosseous
membrane to the base of the proximal phalanx of digit 1. Within the
200 adult modern human upper limbs examined by Kaneff (1959,
1968, 1969, 1979, 1980a, b), the extensor pollicis brevis is missing in
just over 1% of cases and in just over 5% of cases this muscle is
reduced to a tendon connected to the tendon of the abductor pollicis longus or to ligaments adjacent to the insertion of this tendon.
In most of the cases he examined, Kaneff reported that the fleshy
belly of the extensor pollicis brevis blends with the belly of the
abductor pollicis longus. According to the ontogenetic studies of
Lewis (1910), the abductor pollicis longus and extensor pollicis
brevis usually only become separate entities late in modern human
development. In our comparative sample, the only other group
apart from modern humans with a distinct extensor pollicis brevis
is the hylobatids. A separate extensor pollicis brevis was found in
the hylobatids dissected by Bischoff (1870), Kohlbrügge (18901892), Duckworth (1904) and Michilsens et al. (2009) and by us
(e.g., Fig. 7). The exception is Deniker (1885), who did not find
a distinct extensor pollicis brevis in the gibbon foetus dissected by
R. Diogo et al. / Journal of Human Evolution 63 (2012) 64e78
A
DP
B
DP
PP
DP
PP
MI
OH
C
AB
D
DP
PP
PP
MI
OH
75
MI
MI
OH
PPI
OH
PPI
Figure 9. Simplified scheme showing our hypothesis about the evolution of the adductor pollicis accessorius (or ‘interosseous volaris primus of Henle’ of modern human anatomy):
A) First stage of evolution, with a mainly undivided oblique head of the adductor pollicis (OH); B) Second, hypothetical stage of evolution, with the oblique head plus an additional
bundle (AB) that has an origin separated from the main body of this head but still a common insertion together with that main body; C) Third, hypothetical stage of evolution, in
which the insertion of the additional bundle is also somewhat separated from the main body of the adductor pollicis, forming an almost completely differentiated PPI; D) Fourth,
hypothetical stage of evolution, showing a PPI that is even more lateral (radial) and thus even more separated from the main body of the oblique head of the adductor pollicis,
resembling a PPI configuration that is commonly found in modern humans (DP, distal phalanx of digit 1; MI, metacarpal I; PP, proximal phalanx of digit 1).
him. Contrary to the condition in modern humans, in hylobatids the
extensor pollicis brevis usually does not extend to the proximal
phalanx of the thumb, inserting instead onto the base of metacarpal
I and/or the adjacent sesamoid or carpal bones. In gorillas (e.g.,
Hepburn, 1892; Straus, 1941a, b; Raven, 1950; Preuschoft, 1965;
Sarmiento, 1994), a tendon of the abductor pollicis longus often
inserts onto the proximal phalanx of the thumb and the term
‘extensor pollicis brevis’ has been used to describe this (N.B., in
other great apes, including those dissected by us, the abductor
pollicis longus usually inserts onto metacarpal I and/or onto carpal
bones: see Diogo and Wood, 2011). However, as Huxley (1864),
Macalister (1873), Bischoff (1880), Deniker (1885), Tuttle (1970),
Kaneff (1979, 1980a, b), and Aziz and Dunlap (1986) have stressed,
in gorillas the tendon going to the proximal phalanx of the thumb is
the result of a bifurcation of the tendon of the abductor pollicis, the
other branch of this tendon usually going to the metacarpal I
(Fig. 8). Our dissections corroborate this. Thus, contrary to the
condition in modern humans and hylobatids, in gorillas and in
other primates there is no separate extensor pollicis brevis muscle
(i.e., a distinct belly separated from abductor pollicis longus). It
should moreover be noted that in the literature reviews carried out
by Straus (1941a, b) and Sarmiento (1994), for gorillas they found
that in just over half of the cases the abductor pollicis longus only
extends as far as the proximal phalanx of the thumb.
In summary, modern humans are peculiar because they have
a distinct extensor pollicis brevis that attaches to the proximal
phalanx of the thumb, hylobatids are peculiar because they have
a distinct extensor pollicis brevis that usually attaches to the base of
metacarpal I and/or to adjacent bones, and gorillas are peculiar
because in about half of the cases one of the two tendons of the
abductor pollicis longus attaches to the proximal phalanx of the
thumb. According to our dissections and review of the literature, in
chimpanzees, orangutans and in non-hominoid primates the
abductor pollicis longus usually has two tendons, but with the
exception of one of the 20 chimpanzees reviewed by Keith (1899),
these do not extend to the proximal phalanx of the thumb.
Conclusions
Our comparative and phylogenetic analyses indicate that the
forearm muscles in primates usually number between 18 and 19
(Table 1). Two of the 19 muscles predicted to be plesiomorphically
present in primates may be missing in some groups (e.g., the epitrochleoanconeus is usually absent in hominoids except Pan and the
anconeus is usually absent in Hylobates). Modern humans, because
they usually lack the epitrochleoanconeus but have two muscles
going to the phalanges of the thumb (flexor pollicis longus to the
distal and extensor pollicis brevis to the proximal), have more forearm muscles (i.e., 20) than any other primate studied by us (Table 1).
Hylobatids also have a flexor pollicis longus and an extensor pollicis
brevis, but as stated above they normally lack an anconeus, so they
have 19 forearm muscles (Table 1). With respect to the hand muscles,
phylogenetically plesiomorphic primates such as strepsirrhines and
Tarsius usually have more than 30 muscles, but modern humans
usually have only 21 muscles (Table 1). The hand muscles that
modern humans have lost relative to phylogenetically plesiomorphic
primates (i.e., contrahentes, intermetacarpales and interossei accessorii) attach to digits 2e5 (Table 1). The hand muscles that are
conserved as separate structures in modern humans are those that
insert onto the thumb. Modern humans usually also have an additional pollical structure that may also be present in gorillas and
chimpanzees, which is often designated as ‘musculus interosseous
volaris primus of Henle’ but should be designated as musculus
adductor pollicis accessorius (Table 1).
Contrary to what is sometimes suggested in the literature, none
of the muscles and muscle bundles in the modern human forearm
and hand are unique to modern humans. Nonetheless, it is probably
not a coincidence that the three derived structures found in
modern humans and in only one or two other primate genera (i.e.,
adductor pollicis accessorius is also found in some Pan and Gorilla;
flexor pollicis longus and extensor pollicis brevis also found in
Hylobates) all involve the thumb. In fact, this is consistent with the
hypothesis that movements of the thumb played an important role
in human evolution. Marzke et al. (1998) suggested that the flexor
pollicis longus and extensor pollicis brevis may have co-evolved to
enable the members of the subtribe Hominina to maintain the
metacarpophalangeal joint in extension while flexing the distal
phalanx of the thumb as occurs in stone tool making and particularly usage. However, the presence of the flexor tendon attachment
site on distal phalanges of all known fossil taxa of the subtribe
Hominina suggests that some of this musculature was present early
in human evolution and indeed it may be the primitive condition
for the Pan-Homo LCA.
The functional significance of the adductor pollicis accessorius is
more obscure, because this structure usually connects the ulnar side
of the base of metacarpal I to the wing tendon of the extensor
apparatus of digit 1. It is not very substantial and it is difficult to see
(e.g., Morrison and Hill, 2011) how it could confer significant
biomechanical advantage across the joints of the thumb. Detailed
comparative morphological and functional analyses, ideally
including electromyographic studies, should be carried out in
modern humans and also in gorillas and chimpanzees in order to
76
R. Diogo et al. / Journal of Human Evolution 63 (2012) 64e78
better understand the functional and evolutionary significance of this
enigmatic structure. In addition, further studies of more specimens of
other primate taxa are needed to check if this structure may be
present in at least some specimens of non-hominin taxa as well.
The adoption and consistent use of the names proposed in this
paper is not a mere nomenclatural detail: it is a return to an old, and
Darwinian, tradition in which it is important to understand the
phylogeny and homology of each and every anatomical structure. It
is also a way to stress that modern humans usually have 11 muscles
(abductor pollicis longus, extensor pollicis brevis, extensor pollicis
longus, flexor pollicis longus, abductor pollicis brevis, flexor pollicis
brevis, opponens pollicis, adductor pollicis, dorsal interosseus 1,
adductor pollicis accessorius, and flexor brevis profundis) attached
to metacarpal I and the pollical phalanges, and not nine as it often
stated in atlases and textbooks. We hope that this paper will attract
the attention of the authors of human anatomy atlases and textbooks and will thus result in the inclusion, in these atlases and
textbooks, of information about the musculus adductor pollicis
accessorius and the musculus flexor brevis profundus 2.
Acknowledgements
We thank R. Walsh and F. Slaby (Department of Anatomy,
George Washington University), R. Bernstein and S. McFarlin
(Department of Anthropology, George Washington University),
N. Rybczynski (Canadian Museum of Nature), H. Mays (Cincinnati
Museum of Natural History), A. Aziz (Department of Anatomy,
Howard University), F. Pastor (Department of Anatomy, University
of Valladolid), A. Gorow, H. Fitch-Snyder and B. Rideout (San Diego
Zoo) and J. Fritz and J. Murphy (Primate Foundation of Arizona) for
kindly providing the non-primate and primate mammalian specimens dissected during this project. RD was supported by a George
Washington University (GW) Presidential Merit Fellowship and by
a Howard University start-up package, BW by the GW University
Professorship in Human Origins, the GW Provost and the GW
Selective Excellence Program, and BGR by the National Science
Foundation (BCS-0725122).
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