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. 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