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.     

Quantitative genetics of skeletal nonmetric traits in the rhesus macaques on Cayo Santiago. II. Phenotypic,genetic, and environmental correlations between traits

The general lack of phenotypic correlation among skeletal nonmetric traits has been interpreted as indicating a lack of genetic correlation among these traits. Nonmetric traits scored on animals in the skeletal collection of rhesus macaques from Cayo Santiago are used to calculate phenotypic, genetic, and environmental correlations between traits. The results show that even when phenotypic correlations are low, there may be large, significant genetic correlations among these traits. The genetic correlation pattern suggests that genes which affect nonmetric trait variation act primarily at a local level in the cranium, even though there are genes with pleiotropic effects on skeletal nonmetric traits throughout the cranium. Environmental and phenotypic correlations do not show this neighborhood pattern of correlation.     

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.     

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.     

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.     

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.     

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.     

The incidence of bilateral nonmetric skeletal traits: A reanalysis of sampling procedures

For reporting the incidence of bilateral skeletal traits, the choice between sampling statistics depends upon more than their relative efficiencies. Of overreaching importance are the fundamentally different assumptions about the genetic significance of bilateral asymmetry represented by the two principal sampling approaches. Sampling by side is consistent with the premise that trait expression on each side reflects an additive component of genetic variation. Implicit in sampling by individual, by contrast, is the proposition that asymmetries of expression result chiefly from developmental noise. The pattern of age-regression indicated for many of these traits, suggesting a transient developmental role for unilateral expression, supports both this latter view and the thesis of stress asymmetry. Given this pattern, furthermore, incorporating unadjusted trait frequencies into divergence statistics would seem injudicious.     

Secondary sex ratio variation in the Cayo Santiago macaque population

Secondary sex ratios (SSR) were calculated from 1,385 offspring delivered by 372 females in the Cayo Santiago population of free-ranging rhesus monkeys (Macaca mulatta) from 1976 through 1984. The SSR for the entire colony ranged from 0.86 to 1.46 males per female (combined total: 1.08), but no significant difference was observed (P > .05). SSR values were compared among the troops for each year. The SSR differed significantly among the six social groups (P < .05) only in 1978. The annual SSR of each troop was compared over 9 years. Significant variation was found only in group O. The annual SSR was significantly skewed (P < .05, males > females) for three troops in 3 separate years. The SSR did not vary according to troop rank. No significant difference was found among the 17 matrilines of the population, but comparison of matrilines within each social group revealed a significant difference in the SSR (P < .02) for the three matrilines in group I. This was due to the significantly skewed SSR (P = .0080, females > males) of the DM genealogy in that troop. SSR values were not related to matrilineal rank. Individual dominance rank did not bias the SSR. Complete reproductive histories for 266 females showed no evidence of significantly skewed SSR values. Age-related effects on the SSR were examined by using cross-sectional and cohort-based analyses. The SSR did not vary significantly (P > .05) with maternal age, but it was significantly skewed (P < .05) toward males at the ages of 5 and 9 years. Parity had no significant effect (P > .05) on SSR values. Wide variation occurred in the SSR of the Cayo Santiago population. Rank-related adjustment of the SSR at the level of the troop, matriline, or individual, as reported in short-term studies of other primate social groups, may reflect normal annual variation in the SSR evident only from longitudinal observations of large multigroup primate populations.     

Palatine torus in the Greenlandic Norse.

Physical anthropologists have long been intrigued by the distinctive oral tori expressed by the medieval Norse populations of Iceland and Greenland. To assess the temporal and spatial variation of one form of oral tori, palatine torus, observations were made on all available Greenlandic Norse skeletons, as well as on samples of medieval Icelanders and Norwegians. In terms of temporal variation, 12th to 14th century (medieval) Greenlanders from the Eastern and Western settlements exhibited higher frequencies and more pronounced expressions of palatine torus compared with early 11th century Greenlanders. The early Greenlandic sample closely approximated the medieval Icelandic and Norwegian samples for total torus frequency, although the Norwegians exhibited the trait to a less pronounced degree. As degree of expression is the most distinctive aspect of torus variation among the Norse, some combination of environmental factors, including increased masticatory stress and chronic undernutrition, probably accounts for most of the difference between settlement period and medieval Greenlanders. Although palatine torus may be hereditary in part, environmental factors play a significant role in the expression of this trait.     

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.     

Intestinal Parasites of the Free-Ranging Cayo Santiago Rhesus Monkeys (Macaca mulatto)

Free-ranging rhesus macaques on the island of Cayo Santiago, Puerto Rico, were surveyed for intestinal parasites for the first time in over 40 years. Results were compared with the only previous study [10], and the relationships between the prevalence of Strongyloides and dominance rank, body weight, age, and matriline examined in the sampled population.     

Seroprevalence of B virus (Herpesvirus simiae) antibodies in a naturally formed group of rhesus macaques

Eighty-two percent of a group of rhesus monkeys removed from Cayo Santiago were seropositive for B virus (Herpesvirus simiae) antibodies. Similar results were obtained from the Cayo Santiago macaque population two decades ago and from feral Indian rhesus monkeys. Thus it is likely that B virus has been enzootic in the Cayo Santiago population since 1938, when the colony was established with stock imported from India.     

Absence of Naturally Acquired Tetanus Antitoxin in the Free-Ranging Cayo Santiago Rhesus Monkeys (Macaca mulatta)

Tetanus is enzootic in the free-ranging rhesus monkey colony on Cayo Santiago. The disease accounts for 25% of all mortalities in the population. The high prevalence of tetanus provided a unique opportunity to study the potential roles of geophagia, wounding, and clinical tetanus infections on the development of naturally acquired tetanus antitoxin in rhesus macaques. Eighty-six unvaccinated monkeys, including six that recovered from tetanus, were serosurveyed using a mouse toxin neutralization test. None of the animals had detectable antitoxin titers (<0.001 AU/ml), suggesting that natural immunity to tetanus is either rare or nonexistent in the Cayo Santiago colony.     

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.