Quantitative genetics of skeletal nonmetric traits in the rhesus macaques on Cayo Santiago. I. Single trait heritabilities

The use of skeletal nonmetric traits in studies of biological relationships often involves the assumption that variation in these traits is genetic. Studies of nonmetric traits in human groups and in inbred strains of mice and rabbits have indicated a genetic component to nonmetric trait variation. Skeletons of animals with known matrilineage membership were obtained from the Cayo Santiago skeletal collection in order to obtain a direct estimate of the heritabilities of several nonmetric traits in the free-ranging population of rhesus macaques on Cayo Santiago. Falconer's (1965) method was used to calculate heritability. Heritability estimates range from zero to one, and half of them are greater than 0.5. This indicates that there is a considerable amount of genetic variation for these traits among the Cayo macaques. There is a significant tendency for traits scoring the number of foramina to have lower heritabilities than those scoring hyperstotic or hypostotic traits.     

Quantitative genetics of skeletal nonmetric traits in the rhesus macaques of Cayo Santiago. III. Relative heritability of skeletal nonmetric and metric traits

This study addresses the long-standing controversy in skeletal biology concerning the relative utility of skeletal metric and nonmetric traits for studies of biological relationship. This controversy centers on the relative heritability of these two trait sets. This paper presents heritabilities for a series of skeletal metric and nonmetric traits measured with the same sample of mother-offspring pairs from the Cayo Santiago skeletal collection of rhesus macaques. Skeletal nonmetric traits display significantly greater heritability estimates than metric traits. This difference is due primarily to the high heritability estimates of hyperostotic nonmetric traits. Foraminal traits are not significantly more heritable than skeletal metric traits. The generality of this pattern of heritability values, in which hyperostotic nonmetric traits are more highly heritable than foraminal nonmetric and metric traits, depends on future empirical study of the correlation of heritability values in populations and theoretical work.     

Genetic correlations between sides and heritability of asymmetry for nonmetric traits in rhesus macaques on Cayo Santiago

The use of nonmetric traits for estimation of biological distance is a long-standing practice in biological anthropology. Nonmetric traits can be scored using either the individual or the side of the individual as the unit of measure. If sides of the individual are genetically correlated the use of sides would produce redundant genetic information. For this reason, Korey (Am. J. Phys. Anthropol. 53:19-23, 1980) argues for the use of individuals as the unit of measure for nonmetric traits. Ossenberg (Am. J. Phys, Anthropol. 54:471-479, 1981), however, argues that bilateral occurrence of nonmetric traits indicates greater genetic liability for the trait and that therefore the sides are the more biologically correct unit of measure. Genetic correlations for 13 cranial nonmetric traits are estimated for a sample of rhesus macaque skeletons from Cayo Santiago. In addition, heritability of asymmetry is estimated for these 13 traits as a test of Ossenberg's contention that asymmetry is genetically influenced. Significant genetic correlations between sides support Korey's contention that nonmetric traits should be scored by individual. Only two asymmetry heritabilities were significantly different from zero, providing no significant support for Ossenberg's contention that asymmetry is genetically determined. Our results support the theory that asymmetry represents a measure of the ability of an organism to buffer stresses. Therefore, a measure of the heritability of asymmetry is a measure of the heritability of the ability to buffer stresses. This ability does not appear to be heritable in this sample.     

The relationship between cranial metric and nonmetric traits in the rhesus macaques from Cayo Santiago

This study addresses the relationship between cranial metric variables and nonmetric traits using the skeletal sample of rhesus macaques from Cayo Santiago. Discriminant function analysis is used to study the metric differences between macaque crania grouped according to the presence or absence of nine nonmetric traits. The computation of total structure coefficients from the discriminant function analyses provides information regarding how closely each metric variable is related to the discriminant functions derived. Total structure coefficients have not been used previously in the study of the relationship between metric and nonmetric traits. The results of the analysis are interpreted using an explicit approach to cranial morphogenesis-functional cranial analysis. It is concluded that the relationship between cranial metric and nonmetric traits is explicable in terms of a common developmental pathway shared by the two types of traits. Identification of the specific etiology of nonmetric traits depends on future anatomical studies or organisms throughout the period of nonmetric trait development.     

Social group fission and the origin of intergroup genetic differentiation among the rhesus monkeys of Cayo Santiago.

The serum transferrin locus is used to investigate the roles of the lineal effect of fission, male migration effect of fission, and genetic drift in causing intergroup genetic differentiation among the rhesus macaques of Cayo Santiago. These three mechanisms prove sufficient to explain the degrees of differentiation between the newly formed social groups A, K, and L as of July 1, 1971. The lineal effect of fission provides a baseline of intergroup differentiation which is altered by forces leading to intragroup genetic change, the male migration effect and genetic drift. The importance of population dynamics for the distribution of alleles among subgroups of a population is recognized.     

Demographic components of gene frequency change in free-ranging macaques on Cayo Santiago

Gene frequency profiles from January 1973 to January 1977 for three polymorphic loci were examined in Cayo Santiago rhesus social groups. The effects of demographic components (i.e., births, deaths, immigrations, emigrations, and group fission and fusion) on total change in gene frequencies are assessed. Allelic frequencies at the carbonic anhydrase II, 6-phosphogluconate dehydrogenase, and transferrin loci were analyzed in four social groups. In the two groups that underwent fission and fusion during the study period, the timing of these processes was related to the largest short-term changes in gene frequences. However, immigration and emigration had the greatest effect on total change in gene frequency in all groups during the study period. The relative importance of births and deaths in producing gene frequency change varied among the social groups. These results suggest that the relative importance of the demographic components of gene frequency change in primate populations is determined by behavioral patterns and ecological conditions specific to the population considered.     

Osteoarthritis of the hand in nonhuman primates: A clinical,radiographic, and skeletal survey of Cayo Santiago rhesus macaques

Abstract: We describe the relative prevalence and pattern of distribution of osteoarthritis (OA) in the hands of elderly (>15 years) rhesus macaques using clinical, radiographic, and skeletal examinations. In the clinical study the prevalence of nodes was 72% and 16% in the distal inter-phalangeal joints (DIPJ) and proximal inter-phalangeal joints (PIPJ), respectively, 31% of all monkeys had polyarticular nodes. Radiographic OA was present in 55%, 9.1%, and 0% of the DIPJs, PIPJs, and thumb bases, respectively. Skeletal OA as defined by joint surface eburnation for the DIPJ, PIPJ, and thumb base were 16%, 8%, and 2%, respectively. A similar pattern of hand OA with humans is described except for the thumb base OA. This may be due to the relatively rudimentary manipulative role of the macaque thumb. The finding of polyarticular nodal OA raises the possibility of a common pathogenensis for IPJ OA amongst primates.     

The hemogram,serum biochemistry,and electrolyte profile of the free-ranging Cayo Santiago rhesus macaques (Macaca mulatta)

Sixty-four male and 33 female free-ranging rhesus monkeys (Macaca mulatta) from one of six social groups on the island of Cayo Santiago, Puerto Rico, were surveyed to establish normal values for the hemogram and serum biochemical and electrolytes for the colony. Mean values (± 1 SD) are reported by sex for each of three age groups (2–3, 4–9 and ≥ 10 years). All adult females (≥ 4 years) were pregnant. There were significant differences for a number of variables compared to the range reported in the existing literature, and among the age and sex groups in the sampled population.     

Quantitative genetics of cranial nonmetric traits in randombred mice: heritability and etiology

Cheverud and Buikstra (1981) demonstrated a tendency for nonmetric traits representing the number of foramina to have lower heritabilities than those representing hyperstotic or hypostotic traits in a sample of rhesus macaques. Based on this observation, Cheverud and Buikstra hypothesize that differences in the heritability of the two sets of traits may be due to differences in trait etiology. This study addresses the proposed relationship between trait heritability and etiology. Heritability values are calculated for 35 cranial nonmetric traits in a sample of 320 randombred mice using analysis of variance. The results are minimally consistent with the etiological hypothesis, but only 4 of the 35 traits showed statistically significant heritability values. These results are discussed with reference to the assumption that nonmetric traits have a strong genetic component. It is concluded that the developmental pathways that genetic variation traverses before being expressed in the form of nonmetric traits must be understood before variation in nonmetric traits can be used to its fullest potential.     

Differential distribution of antibodies to different viruses in young animals in the free-ranging rhesus macaques of Cayo Santiago

BACKGROUND: The breeding colony of free-ranging rhesus macaques was established in 1938 in Cayo Santiago (CS) with animals collected in northern India. The seroprevalence to cercopithecine herpesvirus type 1 (B virus) and simian retroviruses has been studied previously. RESULTS: This is the first report on the seropositivity to different viruses using samples collected shortly after removing animals (n = 245) from CS. All samples were negative for measles, simian immunodeficiency virus and simian type D retroviruses. The overall prevalence of antibodies was around 50% for simian T-lymphotropic virus I (STLV-I). For B virus, the prevalence was 38%. CONCLUSIONS: Data obtained showed marked differences in the antibody distribution to B virus and STLV-I within the free-ranging colony of rhesus macaques. Implication of these data for the Specific Pathogen Free program at the Caribbean Primate Research Center are also discussed.     

Effect of tetanus toxoid inoculation on mortality in the Cayo Santiago macaque population

Tetanus was a major cause of mortality in the free-ranging population of rhesus monkeys (Macaca mulatta) on Cayo Santiago. From 1977 to 1984 the mean (±1 SD) annual total mortality rate (excluding neonatal deaths within 48 h postpartum, abortions, and stillbirths) was 6.39% ± .94%, and the mean annual tetanus mortality rate was 1.33% ± .45%. Tetanus deaths accounted for 19.5% of the total mortality in the colony. In 1985, all monkeys on the island, except infants and six adult monkeys, were given primary inoculations of tetanus toxoid. The following year, boosters were administered, and yearlings received primary inoculations. One fatal case of tetanus and one recovery from mild disease occurred in uninoculated adult monkeys in 1985, but no additional cases have been observed since. For 1985–1986 the mean annual total mortality rate was 3.69% ± .05%, and the mean annual tetanus mortality rate was .08% ± .08%. Thus, during the 2 years after inoculation against tetanus, the mean annual total mortality rate and the mean annual tetanus mortality rate declined by 42.2% and 94.0%, respectively, when compared to the 8-year period (1977–1984) prior to inoculation. These differences were significant [(χ² = 12.48; P < .005), (χ² = 16.94; P < .005)]. The elimination of tetanus infections through mass inoculation of the Cayo Santiago colony is expected to have a profound impact on the demography of the population by increasing the rate of population growth, by decreasing the differential rates of increase of the component social groups, and by changing the age distribution of the population.     

Relationships between non-metric skeletal traits and cranial size and shape.

A long-standing controversy exists about the comparative utility of metric and non-metric traits as biological indicators in population studies. We hypothesize that the underlying scale which determines the presence or absence of a cranial non-metric trait is an expression of general and/or local size variation in the cranium. Therefore metric and non-metric traits will share a common developmental determination. The hypothesis implies that the underlying scale of a non-metric trait will be correlated with measures of cranial size and shape. Forty-eight cranial metric and twenty-five cranial non-metric traits were scored on the left side of adult male crania from four North American Indian populations. New threshold traits were generated for each non-metric trait by dichotomizing discriminant scores produced by discriminant function analysis. The discriminant analysis was performed using metric traits to discriminate between groups formed by non-metric trait presence or absence. Every non-metric trait tested was significantly correlated with its threshold trait in at least one population. The correlations were of moderate to high levels depending on the trait and population sample studied. This implies that metric and non-metric traits share a moderate to high degree of developmental determination. The cause of these correlations may lie in the common effects that growth and development of the soft tissue and functional spaces of the cranium exert on both metric and non-metric traits.     

Social relationships between adult male and female rhesus macaques: II. non-sexual affiliative behaviour

The social relationships of adult male rhesus macaques (Macaca mulatta) in Group I of the Cayo Santiago colony were studied over a period of 14 months. Relationships were found in which adult males and sexually mature females were persistently close to one another in nonsexual contexts, both within and across seasons. Males of long tenure and high dominance rank tended to have more female partners, and more persistent relationships, than more recent immigrants of lower rank. Correlations with length of tenure were stronger than those with dominance rank. Closely-related females tended to have persistent relationships with the same male. In most cases the female was primarily responsible for maintaining proximity in non-sexual contexts. Dyads which were persistently within 5 m of each other in the birth season were more likely to form a consortship in the subsequent mating season than those which had a brief relationship. A similar tendency was apparent in the 1 m data but it was not statistically significant. There was no association between persistent proximity during the birth season and the occurrence of long, or multiple consortships, nor with the maintenance of proximity or direction of grooming between consort partners. The pattern of consortships was not closely related to the formation of persistent relationships in the subsequent birth season. Females occasionally received protection from their male partners and, in some cases, spent more time in the feeding corral with them than did other females. Affiliative relationships can be very enduring and may have long-term benefits that were not apparent during the study period.     

Sociometrics of Macaca mulatta: II. Decoupling centrality and dominance in rhesus monkey social networks

The concept of the linear dominance hierarchy and a much less precise notion of a central/peripheral ordering of individuals have been prominent among the ideas about social organization of monkey groups. Although the latter has seldom been quantified, the ranks of individuals in the two orders are usually assumed to be correlated. This paper reports on a longitudinal study of a free-ranging group of rhesus monkeys. The individual histories of progression of dominance rank and an independently determined measure of centrality in the social grooming network are compared among a set of males. Centrality is not a static correlate of dominance rank as implied by the findings of short-term studies. Rather, centrality is a more sensitive indicator of status than is dominance rank, to which it is related in a dynamic fashion. Small changes in dominance rank may be followed by large changes in centrality. An increase in centrality may facilitate rise in dominance rank. These findings suggest a complex psychology of status, rather than a simple causative relation between the two variables.     

Ontogeny and diachronic changes in sexual dimorphism in the craniofacial skeleton of rhesus macaques from Cayo Santiago, Puerto Rico

Insight into the ontogeny of sexual dimorphism is important to our understanding of life history, ecology, and evolution in primates. This study applied a three-dimensional method, Euclidean Distance Matrix Analysis, to investigate sexual dimorphism and its diachronic changes in rhesus macaque (Macaca mulatta) skulls. Twenty-one landmarks in four functional areas of the craniofacial skeleton were digitized from macaques of known age and sex from the Cayo Santiago collections. Then, a series of mean form matrices, form difference matrices, and growth matrices were computed to demonstrate growth curves, rates and duration of growth, and sexual dimorphism within the neurocranium, basicranium, palate, and face. The inclusion of fully adult animals revealed a full profile of sexual dimorphism. Additionally, we demonstrate for the first time diachronic change in adult sexual dimorphism caused by extended growth in adult females. A quicker growth rate in males from ages 2 to 8 was offset by a longer duration of growth in adult females that resulted in diminished dimorphism between the ages of 8 and 15. Four functional areas showed different sex-specific growth patterns, and the rate and duration of growth in the anterior facial skeleton contributed most to the changing profiles of sexual dimorphism. The late maturation in size of the female facial skeleton corresponds to later and less complete fusion of facial sutures. The prolongation of growth in females is hypothesized to be an evolutionary response to high levels of intrasexual competition, as is found in other primate species such as common chimpanzees with similar colony structure and reproductive behavior. Further investigation is required to determine (1) if this phenomenon observed in craniofacial skeletons is linked to sexual dimorphism in body size, and (2) whether this diachronic change in sexual dimorphism is species specific. The changing profile of sexual dimorphism in adult rhesus macaques suggests caution in studying sexual dimorphism in fossil primate and human forms.     

Bone mineral density, osteopenia, and osteoporosis in the rhesus macaques of Cayo Santiago

This cross-sectional study investigates metabolic bone disease and the relationship between age and bone mineral density (BMD) in males and females of a large, well-documented skeletal population of free-ranging rhesus monkeys (Macaca mulatta), from the Caribbean Primate Research Center Museum collection from Cayo Santiago, Puerto Rico. The sample consists of 254 individuals aged 1.0-20+ years. The data consist of measurements of bone mineral content and bone mineral density, obtained from dual-energy X-ray absorptiometry (DEXA), of the last lumbar vertebra from each monkey. The pattern of BMD differs between male and female rhesus macaques. Females exhibit an initial increase in BMD with age, with peak bone density occurring around age 9.5 years, and remaining constant until 17.2 years, after which there is a steady decline in BMD. Males acquire bone mass at a faster rate, and attain a higher peak BMD at an earlier age than do females, at around 7 years of age, and BMD remains relatively constant between ages 7-18.5 years. After age 7 there is no apparent effect of age on BMD in the males of this sample; males older than 18.5 years were excluded due to the presence of vertebral osteophytosis, which interferes with DEXA. The combined frequency of osteopenia and osteoporosis in this population is 12.4%. BMD values of monkeys with vertebral wedge fractures are generally higher than those of virtually all of the nonfractured osteopenic/osteoporotic individuals, thus supporting the view that BMD as measured by DEXA is a useful but imperfect predictor of fracture risk, and that low BMD may not always precede fractures in vertebral bones. Other factors such as bone quality (i.e., trabecular connectivity) should also be considered. The skeletal integrity of a vertebra may be compromised by the loss of key trabeculae, resulting in structural failure, but the spine may still show a BMD value within normal limits, or within the range of osteopenia.     

A four-year study of the association between male dominance rank, residency status, and reproductive activity in rhesus macaques (Macaca mulatta)

Considerable controversy exists on the nature of the relationship between male dominance rank and reproductive activity. The nature of this relationship has important implications for understanding the manner in which males compete for access to limited resources. Behavioral data on mating patterns were collected over a four-year period from one social group of rhesus macaques on Cayo Santiago. Correlations between dominance rank and reproductive activity were not stable over a four-year period, but changed yearly. Positive, significant correlations were present in the first two years of the study while non-significant correlations were found in the second two years. The variation found in the correlations between rank and mating activity could be accounted for by changes in the mating frequencies of different classes of males. The long-term resident males had declines in ejaculation frequencies over the duration of the study. Males who immigrated into the group had yearly increases in reproductive behavior over three consecutive years. Maturing natal males also increased their levels of reproductive activity from year-to-year. Combining these mating patterns over time resulted in shifting the proportions of matings away from the long-term residents and in favor of the new males. High-ranking males had an advantage in reproductive activity over the first two years of the study, as measured by both the total number of ejaculations and the mean number of ejaculation per male. New males, comprised of recent immigrants and maturing natal males, had a greater level of reproductive activity over the last two years. These results suggest that the effect of rank on reproductive activity is variable and that males utilize alternative tactics to attain access to limited resources. Simple one-factor models explaining the relationship between rank and reproductive activity must be replaced with models explaining how alternate strategies affect male competition and reproductive success in primates.     

Reproductive performance, population dynamics and anthropometrics of the free-ranging Cayo Santiago rhesus macaques

This report summarizes demographic data collected on the Cayo Santiago colony of rhesus monkeys from 1976-1983 and compares the results with those from 1959-1964 [8,9]. For males and nonpregnant/nonlactating, pregnant, and lactating females mean (+/- 1 SD), body weights, crown-rump lengths, and ponderal indices are tabulated for each age on a large (n = 586) single sampling of this free-ranging population of macaques.     

Age- and gender-related changes in body size, adiposity, and endocrine and metabolic parameters in free-ranging rhesus macaques.

Normative age- and gender-related changes in body composition, serum lipids, testosterone, and insulin-like growth factor (IGF-1) were examined in the Cayo Santiago free-ranging rhesus macaques. In both adult males and females, body weights, crown-rump lengths, and circumference of the limbs were lowest in the oldest group (20+ years of age) as compared with other adult age classes. Body fat, as reflected in subcutaneous fatfold thickness and waist/thigh ratios, were higher in adult females than adult males. This gender dimorphism was first detectable among the 6-9 year old age group. Greatest body fat among females was observed in the 10-14 age group, whereas in males the highest values were observed in the 15-19 age group. Differences in body composition were also observed with respect to reproductive status. Although there were no gender differences in overall cholesterol levels, there were age-related differences between males and females, and only in males were cholesterol values positively related to adiposity. There were no age- or gender-related differences in triglyceride values, but levels were significantly higher in pregnant females in comparison with other reproductive states. Levels of testosterone were not significantly related to any morphometric parameter and values did not decrease significantly with age. Levels of IGF-1 exhibited a significant age-related decrease among adult males, and females had higher levels independent of age. The similarities between the present findings and human studies suggest that further studies in the free-ranging rhesus macaques would provide a bridge between studies of laboratory-housed primates and studies of human beings with respect to the etiology of obesity and life-history changes in body composition and endocrine and metabolic parameters.     

Ontogeny of locomotion in rhesus macaques (Macaca mulatta): II. Postural and locomotor behavior and habitat use in a free-ranging colony

This study quantifies changes in postural and locomotor behavior as well as habitat use across the life span of free-ranging rhesus macaques (Macaca mulatta) in the Cayo Santiago colony in Puerto Rico. It focuses on developmentally related changes from birth to adulthood, and complements an earlier study by Turnquist and Wells ([1994] J Hum Evol 26:487-499) on the early postnatal ontogeny of the musculoskeletal system of the same colony. A total of 6,551 locomotor and postural events was analyzed. Selection and use of substrate correlated well with age. The more sedentary adult and dependent infant select safe, wide, horizontal arboreal settings in contrast to the older Infant IIs and Juveniles, who are learning locomotor and postural skills through independent chase and play. Infant macaques, when independent, often employ a low center of gravity and widely abducted limbs in order to broaden their contact with the base of support. This study shows that the previously reported ontogenetic changes in morphology are closely paralleled by changes in postural and locomotor behavior, and these in turn are correlated to changes in habitat use, particularly during the formative years.