Age- and sex-associated variations in the directional asymmetry of rhesus macaque forelimb bones.

Several investigators have questioned the significance of handedness as an explanation of directional forelimb asymmetries, yet little has been done to isolate other explanatory factors. In this investigation, we analyze 61 female and 76 male rhesus macaque skeletons for evidence of age- and/or sex-associated variations in ten forelimb bone measurements. All significant directional asymmetries are found to favor the right side. Although some of these asymmetries are found to favor the right side. Although some of these asymmetries are compatible with the interpretation of muscle hypertrophy associated with preferential use of the right forelimb, the overall pattern suggests that age- and sex-related ontogenetic factors deserve equal consideration. Significant sex differences in asymmetry means are present within and across age groups (juveniles, subadults, and adults), and numerous changes in asymmetry with age are also found. A pattern of decreasing asymmetry with age was found in males, with 40% of the ten measures being asymmetrical in juveniles, 30% in subadults, and 20% in adults. Among females, this pattern is reversed. No significant asymmetries were found for juvenile or subadult females, whereas 40% of the measures were asymmetrical in adult females. We conclude that greater consideration of age- and sex-related factors is necessary when drawing samples for the purpose of investigating asymmetries, and an awareness of trait-specific age and sex patterns of variation is necessary when citing forelimb asymmetries in demographically nonrepresentative populations as evidence of handedness or other behavioral asymmetries.

Cortical asymmetries in frontal lobes of rhesus monkeys (Macaca mulatta).

Cortical sulci were digitized and their lengths determined with 3-dimensional computer technology on 335 endocranial casts from rhesus monkeys with known maternal genealogies, ages at death, and sex. Non-metric data were also collected from 403 endocasts. Frontal lobes were directionally asymmetrical with lengths of the left central, right rectus (principal), and right lateral orbital sulci significantly longer. The positions of the medial and lateral ends of the central sulcus were significantly different in the two hemispheres, and there was significant protrusion of the frontal lobe (petalia) on the right side. Together, these data indicate elongation of the right orbital and dorsolateral frontal lobe. The asymmetries reported here probably involve short-term memory for visual information. This raises interesting questions about the extent to which macaques are right hemisphere dominant for processing visual information as compared to humans.

Heritability and association of cortical petalias in rhesus macaques (Macaca mulatta).

Frontal and occipital petalias, the anterior or posterior protrusions of a cerebral lobe on one side or the other, are among the most striking anatomical asymmetries in human brains. Our previous studies of rhesus macaques revealed a relatively high frequency of right frontal petalias, whereas occipital petalias were seen less often and were equally common on right and left sides. In the present study, we test the hypothesis that variation in frontal and occipital lobular morphology is, in part, genetically based, and that frontal and occipital petalias are associated with one another. With a sample of 403 rhesus macaque endocasts, we found that right frontal petalias were more commonly associated with left occipital petalias than would be expected by chance. The concurrence of right frontal and left occipital petalias is the most common variant in human brains. We also found significant but moderate heritability for frontal petalias, while the heritability estimate for occipital petalias was relatively low and not statistically significant. This result suggests a genetic basis for variation in the degree of anatomical cerebral lateralization.

Heritability of brain size and surface features in rhesus macaques (Macaca mulatta).

The extent of heritability for overall brain size and regional cortical surface features such as sulcus lengths is important for demonstrating a genetic component to the observed phenotypic differences among individuals and for evaluating the potential for evolutionary change in response to selection. Although the genetics of brain size has been extensively considered, the detailed morphology of the cortical surface has not previously been subjected to genetic analysis. We estimated the heritability of brain size and cortical sulcus lengths using 438 endocranial casts taken from skeletons of rhesus macaques (Macaca mulatta) from the Cayo Santiago population. Estimates were obtained both by mother-offspring regression and symmetric-differences-squared (SDS) methods. Brain size, measured as cranial capacity, was highly and significantly heritable in this population, confirming results of previous studies with laboratory mice. Overall, cortical sulcus lengths were also heritable, with 35% of the sulci significantly heritable at the 5% level in the mother-offspring analysis. The average mother-offspring heritability estimate, 0.31, was the same as the average heritability obtained previously from a series of 56 cranial metric characters. The SDS analyses generally corresponded to the findings based on mother-offspring regressions, although the significance test appeared more conservative. Both gross and detailed morphology of the brain are heritable.

Endocranial suture closure in rhesus macaques (Macaca mulatta).

Endocasts from skulls of 330 rhesus monkeys (Macaca mulatta) of known age are scored for closure of nine bilateral and three unilateral sutures or segments of sutures. A variety of tests reveals a strong relationship between age and stages of suture closure, although increasingly broad confidence intervals prevent sutures from being very useful for precisely aging older macaques. The order in which endosutures begin to close, as well as that in which closure is finally achieved, is determined for macaques, and these sequences compared to those for endosutures of humans (Todd and Lyon, 1924). The basilar suture is the earliest to close, while the masto-occipital and rostral and caudal squamosal sutures achieve closure quite late in both species. On the other hand, humans and macaques differ in their schedules for the sphenofrontal suture and in the initiation of closure for the rostral portion of the squamosal suture. Two sutures close significantly sooner on the right than on the left side (the rostral squamosal and masto-occipital) and asymmetry favoring closure of the right lateral lambdoid suture also approaches significance at the 0.05 level. No sutures close significantly sooner on the left side. It is suggested that macaque sutures may close from the inside out, that endosutures are more sensitive than ectosutures for detecting sequences in which cranial sutures begin to close, and that directional asymmetries in suture closure of macaques may be related to minor asymmetries in brain/skull shape (petalias).

Directional asymmetry in the forelimb of Macaca mulatta.

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 significantly 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.