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Directional asymmetry in the forelimb of Macaca mulatta.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 77:1-6 (1988)
Directional Asymmetry in the Forelimb of Macaca mufatta
DEAN FALK, LINNEA PYNE, R. CRISS HELMKAMP,AND C. JEAN
DEROUSSEAU
Department of Anthropology, State University of New York, Albany, New
York 12222 (D.F.); Department of Sociology and Anthropology, Purdue
Uniuersity, West Lafayette, Indiana 47907 (R.C.H.); Department of
Psychology, Bowdoin College, Brunswick, Maine 0401 1 (L.P.);
Department of Anthropology, New York Uniuersity, New York, New York
10003 (C.J.D.)
Cerebral asymmetry, Evolution, Handedness,
KEY WORDS
Rhesus monkey, Skeletal asymmetry
ABSTRACT
Asymmetry was investigated in the forelimbs of 150 rhesus
monkey (Macaca mulatta) skeletons using measurements of right and left humerii, radii, ulnae, second metacarpals, and femora. Seven of the ten forelimb
dimensions were larger on the right than on the left side. Paired t-tests revealed
that the mean of the right side was significantly larger than that for the left
for two measurements of the ulna and two of the humerus. No measurement
was sigmfkantly larger on the left than on the right side. These results indicate
a small but significant asymmetry in the forelimb bones of rhesus monkeys and,
as is the case for humans, the direction of asymmetry favors the right side. Our
findings are consistent with an interpretation of hypertrophy of certain muscles
and opens the question of whether rhesus monkeys preferentially use their right
forelimbs for manipulative tasks that require manual dexterity, as is the case
for humans. These forelimb skeletal asymmetries are discussed in light of the
recent literature on cortical asymmetry and handedness in nonhuman primates.
The purpose of this article is to report
asymmetry in the forelimb of rhesus monkeys (Mucaca mulatta) and to compare the
patterns of asymmetry to those of humans.
Our findings are interpreted within an evolutionary framework that focuses on the evolution of right-handedness in hominids.
Forelimb asymmetry is well documented
in the skeleton of Homo sapiens. Among 116
right-handed white adolescents, biepicondylar breadth of the humerus was significantly
larger on the right side, whereas 19 nonright-handed individuals showed no significant asymmetry (Schell et al., 1985). Schell
et al. also examined upper arm and calf circumferences and concluded that their results were “consistent with an explanation
in terms of preferred use of one side of the
body and consequent muscle hypertrophy . . .”
In a study of tennis players versus nontennis players, Buskirk et al. (1956) suggest
that small bilateral differences in bone dimensions and muscle hypertrophy favoring
the dominant arm may be enhanced by
increased unilateral activity. While 11 nontennis players showed an asymmetry in ul-
(9 1988 ALAN R. LISS, INC
nar length favoring the dominant-hand arm,
ten tennis players exhibited not only longer
ulnae but also longer radii in the dominanthand arm. A similar study of bone growth
in young males (Watson, 1973) lends support to the suggestion that sports involving
unilateral activity result in increased asymmetry in the patterns of growth and formation of bones.
Other studies suggest that features on the
right side will be larger than those on the
left regardless of hand use. Garn et al. (1976)
found that among 208 right-handed and 19
left-handed individuals, total cross-sectional
area and cortical area of the second metacarpal bone were larger on the right side in
most people, regardless of hand preference.
Plato et a1 (1980) also showed that total mid-
Received September 21,1987; revision accepted March 9,1988.
Address reprint requests to Dr. Dean Falk, Department of
Anthropology, Social Science 263, State University of New York,
Albany, New York 12222.
2
D. FALK ET AL.
7. Distal breath of ulna, measured from the
styloid process to the head
8. Length of the olecranon process of the
ulna, measured along the axis of the bone,
from the proximal face of the semilunar
notch to the proximal tip of the olecranon
9. Maximum length of ulna, measured
using an osteometric board
10. Maximum length of the second metaMATERIALS AND METHODS
carpal
Measurements were taken (by L.P.) from 11. Biepicondylar breadth of the distal felimb bones of 150 monkeys (M. rnulatta) from
mur
the Cay0 Santiago Skeletal Collection at the
University of Puerto Rico. All monkeys were
Comparisons of the 11 measurements by
known to have reached sexual maturity, and side are based on sample sizes ranging from
the sample included 64 females, 80 males, 148 to 150 pairs. The paired t-test was emand six of unknown sex (because of incom- ployed since the right and left measurement
plete specimens and/or records). Eleven pairs are not independent, and since size
measurements were taken independently on variation among the skeletal cases is conright and left sides with a sliding caliper siderable. Differences were considered sig(unless otherwise stated). Intraobserver er- nificant if the two-tailed probability was less
ror was measured by comparing repeated than or equal t o .05. All descriptive and inmeasurements of all 11 variables in 15 skele- ferential statistics were calculated using the
tons and determining the technical error of Statistical Package for the Social Sciences
measurement (Johnston et al., 1974). The (Nie et al., 1975) on the CDC 6500 computer
variation between sides was found to be sig- at Purdue University.
nificantly greater than the observer error for
RESULTS
each of the 11 traits, indicating that measurement error does not significantly conSummary statistics and t-test results are
tribute t o the observed differences between presented in Tables 1 and 2. The differences
sides. Root mean square errors were com- between right and left means for the 11
puted between initial and repeated meas- measurements range from .OOO to .489 mm.
urements for the 11 variables, independently The mean of the right side is shown to be
for right and left sides. They range from .01 larger than that for the left in eight of the
to .13 mm on the left side, and .02 to .13 mm 11 measures. Two means, for distal width
on the right side. Measurements 2 , 3 , 5 , and and length of radius, are smaller on the right
8 below were developed for this study; the side than on the left. The right and left samremaining seven measurements were taken ple means are equal for biepicondylar breadth
from the literature (Bass, 1971; Buskirk et of the humerus.
al., 1956; Garnet al., 1976; Plato et al., 1980;
Of the measures that show asymmetry,
Schell et al., 1985):
four show statistically significant differences. All four are forelimb measures and
are larger on the right side than on the left.
Two are measurements of the ulna, overall
1. Biepicondylar breadth of humerus
2. Length of the lateral supracondylar ridge length (right-left = .387 mm, t = 2.69), and
of humerus, measured from the proxi- length of the olecranon process (right-left =
mal end of the capitulum to the end of .205 mm, t = 5.62), and two are measurements of the humerus, length of the suprathe ridge
3. Maximum diameter of humerus across condylar ridge (right-left = .489 mm, t =
the distal portion of the lateral lip of the 3.10), and diameter of the humerus at the
lateral lip of the intertubercular groove (rightintertubercular groove
4. Distal breadth of radius, measured from left = .078 mm, t = 2.33). These four significantly asymmetrical dimensions reprethe ulnar notch to the styloid process
5. Width of the shaft of the radius at the sent 44%of the forelimb measures examined
radial tuberosity, measured a t the point in this study, and it is noteworthy that three
other forelimb measures also show a tendof maximum protrusion
6. Maximum length of radius, measured ency to be larger on the right than on the
left side.
using an osteometric board
shafl width, length, cross-sectional area, and
cortical area of the second metacarpal bone
were larger in the right hands of both righthanded and left-handed individuals, but only
the asymmetries in the right-handed individuals were significant. It should be noted,
however, that left-handed individuals are
under-represented in these studies compared t o right-handed subjects.
(149
Diameter at
intertubercular groove
Biepicondylar breadth
Femur
Hand
Length, second
metacarpal
(148)
LeR
Right
Right
LeR
28.100
28.089
36.860
36.855
12.069
11.864
Right
LeR
Length, olecranon
process
(150)
7.149
7.113
Right
Left
Distal breadth
Left
151.963
151.576
Right
Left
9.542
9.511
9.368
9.383
Right
Left
137.713
137.777
13.133
13.055
40.700
40.211
28.526
28.526
Right
Left
Right
LeR
Left
Right
Left
Right
x
Right
(148)
(148)
Maximum diameter
radial tuberosity
Ulna
Length
(149)
Distal breadth
(148)
(149)
Length, lateral
supracondylar ridge
Radius
Length
(148)
N
Biepicondylar breadth
Measurement
Humerus
TABLE 1. Means, standard deviations, and ranges (millimeters)
2.583
2.560
4.215
4.257
2.238
2.184
1.131
1.168
18.525
18.299
1.276
1.318
1.647
1.639
16.930
16.957
2.040
2.113
4.454
4.515
2.974
3.054
SD
Maximum
20.70- 33.50
20.40- 34.15
24.75- 45.00
24.50- 44.85
5.80- 16.30
5.80- 15.80
4.90- 12.65
4.60- 12.40
97.50-192.35
96.50-192.00
6.40- 12.90
6.30- 13.35
5.65- 14.30
5.85- 13.50
87.00-175.50
87.00-172.50
8.10- 18.40
7.10- 18.80
27.60- 54.00
27.90- 49.90
20.40- 34.30
20.05- 35.70
Minimum
4
D. FALK ET AL.
TABLE 2. Mean differences (right-left), standard deviations, and paired t-test scores
No. of pairs
Measurement
Humerus
Biepicondylar breadth
Length, lateral
supracondylar ridge
Diameter at
intertubercular groove
Radius
Length
Distal breadth
Maximum diameter,
radial tuberosity
Ulna
Length
Distal breadth
Length, olecranon
process
Hand
Length, second
metacarpal
Femur
Biepicondylar breadth
R,,
-
X,,n(m)
SD
t-score
148
149
0.000
0.489
0.497
1.925
0.00
3.10**
149
0.078
0.408
2.33*
148
149
148
- 0.064
- 0.015
0.031
1.308
0.374
0.306
148
150
150
0.387
0.036
0.205
1.756
0.308
0.446
2.69**
1.42
5.62***
148
0.004
0.419
0.12
148
0.011
0.414
0.31
~
~
0.60
0.49
1.20
*P < .05.
**P 4 .01.
***P< ,001
Although a full treatment of sex differences in directional asymmetry is beyond the
scope of the present report, paired t-tests
were done separately by sex for the 11 measures. For the four measures shown in Table
2 that yielded significant asymmetries favoring the right side when averaged across
sex, significant asymmetries occurred in females for all but ulna length. For males on
the other hand, significant asymmetries occurred only for ulna length and length of the
olecranon process. One measure that did not
show significant asymmetry in the combined
sample, distal breadth of ulna, was significantly longer on the right side in the female
sample.
DISCUSSION
Our results indicate that a small but significant asymmetry characterizes the forelimbs of rhesus monkeys. As is the case for
humans, the direction of asymmetry reported here for Macaca favors the right side.
Dhall and Singh (1977) report greater mean
weight of the humerus, radius, and ulna on
the right side for rhesus monkeys, and the
ulna appears to be significantly longer on
the right side in both humans (Buskirk et
al., 1956) and rhesus monkeys. Although our
study did not find significant asymmetry in
biepicondylar breadth of the humerus, as has
been found for humans (Schell et al., 1985),
we do report significant asymmetry favoring
the right side either in the length of the supracondylar ridge or in the diameter of the
humerus at the lateral lip of the intertubercular groove in rhesus. We failed to find significant asymmetry in the length of the second
metacarpal, as reported for humans (Plato
et al., 19801, although right side measures
of cortical area of the second metacarpal have
been found to be significantly greater than
left side measures for Macaca (C.J. DeRousseau, unpublished data). It is also interesting to note that, as for humans (Schell
et al., 1985; Laubach and McConville, 1967;
Malina and Buschang, 1984), no significant
asymmetry was found in biepicondylar
breadth of the femur.
The four measures that were found to be
significantly larger in the right upper extremity of rhesus monkeys are consistent with
an interpretation of hypertrophy of certain
muscles (Schell et al., 1985) that abduct and
flex the arm, flex the forearm, and extend
the forearm and wrist. The maximum diameter of the humerus a t the lateral lip of
the intertubercular groove was found to be
significantly wider on the right side than on
the left in this study. This site represents
the combined insertions of the pectoralis major (a flexor of the arm) and the deltoideus
muscle (an abductor) in rhesus monkeys
(Hartman and Straus, 1933). The lateral su-
DIRECTIONAL ASYMMETRY IN MACACA
pracondylar ridge of the humerus and the
olecranon process of the ulna were also found
to be significantly longer on the right than
on the left side. A lengthened supracondylar
ridge may indicate a longer origin for the
brachioradialis muscle, which is an extremely powerful flexor of the forearm in
rhesus (Hartman and Straus, 1933). The extensor carpi radialis longus also originates
from the supracondylar ridge and inserts on
the dorsal surface of the second metacarpal
(Hartman and Straus, 1933). This muscle
acts to extend the wrist. The lengthened olecranon process of the right side receives the
insertion of the common tendon of the triceps muscle, which is an important extensor
of the forearm in rhesus monkeys.
All of these asymmetries indicate that lever arms of movement in the forelimb would
be slightly longer on the right than on the
left side. In sum, the asymmetries of forelimb described above open the question of
whether rhesus monkeys preferentially use
their right arms for tasks that involve abduction and flexion of the arm, flexion of the
forearm, and extension of the forearm and
wrist? Or, put another way, are rhesus monkeys in some sense right-handed?
At first glance, it would seem that the answer to this question appears to be no. Handedness in nonhuman primates has been
widely studied (see MacNeilage et al., 1987,
for review), and the general consensus is that
monkeys are not handed in the human sense
(Deuel and Dunlop, 1980; Lehman, 1978;
Kruper et al., 1966; and Warren, 1953).
Whereas approximately 91% of humans are
right-handed (see Falk, 1987, for review),
many studies of nonhuman primates report
a “U-shaped distribution with an approximately equal number of left and right handers, and a variable percentage of animals
without preference”(MacNeilageet al., 1987).
However, MacNeilage et al. (1987)suggest
that nonhuman primates do display hand
preference patterns, although they differ from
the right-handedness that is typical of humans. Their survey of the literature led the
authors to conclude that Old World monkeys
are characterized by coexistence of a right
hand preference for some types of actions
and a left hand preference for others. Specifically, left hand preferences were for
reaching (food)while right hand preferences
were for practiced performance and “manipulation acts analogous to that observed in
humans.” The authors note a tendency for
left hand preference for food reaching in pri-
5
mates to be higher when a stabilization
movement (by the right hand) is also required and they point out that a division of
labor between a dominant and a supportive
hand also characterizes certain tasks requiring human bimanual coordination.
It would appear from the work of MacNeilage et al. (1987) that rhesus monkeys
are right-handed for manipulative acts that
require high manual dexterity (e.g., two successive single finger manipulations), as is
the case for most humans. However, the reason rhesus monkeys do not appear to be righthanded in the human sense is because they
are left-handed for other (reaching) acts. Our
finding of skeletal asymmetries that favor
the right side in the forelimb of rhesus monkeys and that are similar t o (but not identical with) those seen in human forelimbs
lends support to the conclusions of MacNeilage et al. (1987).
The findings of other workers suggest that
asymmetry in the forelimb of rhesus monkeys reflects not only functional asymmetry
for certain kinds of motor activities but also
cortical lateralization that may have been a
precursor (in a common ancestor) to the human condition. Split-brain rhesus monkeys
have been shown to be right hemisphere
dominant for differentiating photographs of
monkeys’ faces (Hamilton and Vermiere,
1985). Other studies (Petersen et al., 1978;
Heffner and Heffner, 1984) have demonstrated that the left hemisphere of monkeys
in the genus Macaca is dominant for processing species-specific vocalizations. As is
the case for chimpanzees and humans, the
length of the left Sylvian fissure was found
to be significantly longer than its right counterpart in endocranial casts from rhesus
monkey skulls (Falk et al., 1986). In sum,
monkeys of the genus Macaca appear to exhibit left hemisphere dominance for fine motor skills carried out with the right hand, as
well as functions related to complex vocal
communications, and right hemisphere dominance for certain visual processes. Our finding of skeletal asymmetry in the forelimb of
rhesus monkeys is in keeping with the fact
that brains of Macaca appear to be lateralized along lines similar to the human condition.
ACKNOWLEDGMENTS
We thank the University of Puerto Rico
for free access to the Cay0 Santiago Primate
Skeletal Collection. This research is supported by Leakey Foundation grant 1157
6
D. FALK ET AL
(L.P.),National Science Foundation grants
BNS-8406541 and BNS-8796195 (D.F.),and
Public Health Service award 1 R 0 1 NS24904
(D.F.).
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