Avoidance of close consanguineous inbreeding in captive groups of rhesus macaques

In three captive groups of rhesus macaques (Macaca mulatto) the intensity of inbreeding avoidance was directly correlated with the closeness of kinship. The incidence of inbreeding between matrilineal relatives was lower than expected were mating to occur randomly with regard to matrilineal affiliation. The avoidance of mating between sons and their mothers and between matrilineal sibs contributed about squally to this outcome. The incidence of mating between more remote matrilineal relatives was lower than, but could not be shown to differ significantly from, that expected at the 0.05 level of probability. Familiarity fostered by interactions among matriline members probably provides a focus for avoidance of matrilineal inbreeding, and might influence male dispersal. Results of this study are consistent with reports of female rhesus macaques' avoidance of sexual activity with matrilineal male relatives as predicted by parental investment theory The observed incidence of inbreeding between patrilineal relatives was not different from that expected, but significantly fewer of the patrilineally inbred matings involved father/daughter matings than expected were mating random. Recognition of phenotypic similarities might provide a focus for avoidance of inbreeding between fathers and their daughters, but is loss reliable than strategies for avoiding matrilineal inbreeding. Adaptations for avoiding matrilineal inbreeding that are more effective than those for avoiding patrilineal inbreeding might have evolved because the risk of patrilineal inbreeding, and hence the resulting loss in fitness, is marginal compared to that for matrilineal inbreeding in free-ranging groups. © 1995 Wiley-Liss, Inc.     

Influence of regional crossbreeding between rhesus macaques on the rate of weight gain of their offspring

To evaluate potential heterosis resulting from breeding between rhesus macaques of Chinese and Indian origin in a captive social group, the rates of weight gain of Indian (nonhybrid) rhesus monkeys were compared with those of their hybrid (half Chinese/half Indian) peers. The coefficients for the linear regression of age on weight were estimated for each animal for each exact age between 1 and 4, when that regression is strictly linear, at which he/she lived in the group. The average rates of weight gain of hybrids and nonhybrids were compared using the t statistic. Both male and female hybrids exhibited statistically significantly higher rates of weight gain than their nonhybrid peers before, but not after, age 4. No evidence could be found that either hybrid status or rate of weight gain increases fitness, at least under captive conditions. © 1994 Wiley-Liss, Inc.     

Wounding patterns in three species of captive macaques

The incidence of wounding in captive groups of rhesus (Macaca mulatta), pigtail (M. nemestrina), and stumptail (M. arctoides) macaques was studied for 21 months. Groups were monitored daily for evidence of wounding. Wounded animals were captured, treated by veterinary staff, and returned following recovery. Records were kept on the age, sex, and species of the recipient, along with the type and location of wound. In each species of macaque, adult males incurred the highest frequency of wounds and multiple wounds of any age-sex class. This contrasted with previously reported behavioral data indicating low frequencies of aggression received by adult males, especially contact aggression and bites. These discrepancies indicate wounding frequencies do not necessarily correspond with behavioral measures of aggression. Inhibition of aggression directed toward infants and the selective avoidance of bites directed to vital body regions were presented as possible mechanisms that modify intragroup aggression. Increased wounding in the birth season under captive conditions suggests that the pattern of increased wounding reported during the breeding season under freeranging conditions may reflect xenophobic responses to immigrating males, rather than direct male-male competition for estrous females.     

Primigravidity,body weight,and costs of rearing first offspring in rhesus macaques

Body size is associated with menarche and ovarian function, but the relationship to first conception is rarely examined. We conducted a longitudinal investigation of rhesus macaques, Macaca mulatta, to determine the effect of differences in body weight on both the age at first conception and survivorship of first progeny. Young females who became pregnant weighed significantly more than peers who remained barren, with weight changes for females who successfully raised offspring no different than those for females who did not produce offspring. Infant mortality among primiparae was not significantly greater than that among multiparae, although nearly twice as high. First-born males tended to have lower survivorship than first-born female offspring. We suggest that reproductive costs encountered by primiparous females are more likely to be modulated by immature neuroendocrine function than by inexperience, small body size, or infant suckling patterns. We conclude that body size influences probability of first conception, socioendocrine factors mediate the likelihood of infant survival, and primiparous production of male progeny seems to exert a greater reproductive cost than does production of female progeny. Am. J. Primatol. 46:135–144, 1998. © 1998 Wiley-Liss, Inc.     

Determining genetic background in captive stocks of cynomolgus macaques (Macaca fascicularis)

Background As in other model organisms, genetic background in the non‐human primates Macaca mulatta and Macaca fascicularis is an experimental variable that affects the response of other study variables. Genetic background in model organisms is manipulated by breeding schemes but is generally pre‐determined by the source population used to found captive stocks. In M. fascicularis three such sources have been distinguished, however, these are not routinely taken into consideration when designing research. Methods We exemplify a mitochondrial DNA (mtDNA)‐based strategy to trace the maternal geographic origins of M. fascicularis animals of unspecified origins. Results Macaca fascicularis of unspecified origins kept at primate research centers carry mtDNA haplotypes representing all three major genetic subdivisions. Conclusions We suggest that the genetic background of study animals could be better specified in the future using an mtDNA‐based approach, which would enable informed selection of study animals and help reduce variation within and among studies.     

Identification of rhesus macaques with spontaneous endometriosis

Abstract: Rhesus macaques (Macaca mulatta) with endometriosis were identified using reproductive histories, serum levels CA-125, pelvic ultrasonography, laparoscopy, and histopathology. All animals were evaluated from a large breeding colony and had a history of infertility and/or spontaneous abortions. Laparoscopy and ultrasonography were performed on 40 macaques: 27 macaques from the breeding colony with elevated CA-125 levels, ten macaques from the breeding colony with normal or low serum CA-125 levels, and three macaques from another facility with previously diagnosed spontaneous endometriosis. Clinical endometriosis was diagnosed by laparoscopy in 16/37 (43%) macaques from the breeding colony and was confirmed by histologic examination in all animals biopsied. The disease was classified as minimal (40%), mild (25%), moderate (10%), or severe (25%). The most common sites of endometriosis were the serosal surface of the uterus (75%) and the posterior cul-de-sac (75%). In this study, CA-125 levels were useful in identifying animals from the breeding colony with endometriosis. The rhesus macaque provides a valuable animal model to study endometriosis and potentially to assess efficacy of therapeutic agents for this disease condition.     

Inbreeding in three captive groups of rhesus monkeys

Using electrophoretic and serological genetic markers each of 17 potentially inbred matings in three groups of rhesus monkeys could be classified as either inbred or noninbred matings. Although nine of these 17 matings involved either father-daughter or paternal half-sib matings, only 7.4 were expected by chance alone. At least two, and possibly as many as three, of the nine cases of inbreeding involved father-daughter matings. Thus, no evidence of avoidance of inbreeding was observed in the closed captive groups of rhesus monkeys studied. Colony management policies must be developed to minimize the opportunity for or the deleterious effects of both father-daughter and half-sib matings. Furthermore, kin selection theory should consider why kin recognition, if it occurs, does not lead to avoidance of inbreeding.     

Absence of deleterious effects of inbreeding in rhesus macaques

The limited availability of rhesus macaques through importation and the need for large numbers of them for use in biomedical research in this country have led to large- scale efforts to breed them domestically in captive groups. Since gene flow into the groups is usually restricted, consanguineous inbreeding can lead to inbreeding depression, which is characterized by increases in mortality, declines in fertility, and reductions in traits associated with physiological efficiency. For this reason, it is desirable to determine the level of inbreeding at which inbreeding depression occurs in rhesus macaques. I compared fertility, mortality, and the rate of weight gain in inbred and noninbred rhesus monkeys in three captive groups. There is no evidence of inbreeding depression in rhesus macaques whose inbreeding coefficients are ≤ 0.125, a level at which inbreeding depression is known to occur in some species.     

Tracking of dye-labeled lymphocytes in rhesus macaques

Abstract: Lymphocytes were isolated from rhesus monkeys and marked with a fluorescent lipophilic dye to monitor their distribution in vivo. Dye-labeled cells were either monitored by blood draws over a three-month period, or identified within peripheral organs upon autopsy. Lymphocyte labeling conditions were optimized. Dye-labeled lymphocytes could be detected in the circulation for at least 100 days by flow cytometry and fluorescence microscopy. Activated lymphocytes were removed from the circulation more rapidly than lymphocytes that had not been activated.     

High-resolution chromosomes of rhesus macaques (Macaca mulatta)

Late-prophase high-resolution chromosomes were successfully cultured for 22 of 27 Macaca mulatta samples. Twelve of the successful cultures were adequate for karyotyping high-resolution spreads. High-resolution chromosome technique provides an important contribution to primate genetics because it can be used to identify chromosomal anomalies undetected in metaphase spreads and may be useful for paternity exclusion analysis.     

A benign method for maintaining ovulatory estrogen levels in cycling rhesus macaques

The goal of this study was to develop a relatively noninvasive technique for generating ovulatory estrogen levels in cycling females over extended periods of time. Eleven intact cycling rhesus macaques were given weekly injections of estradiol cypionate in an effort to obtain weekly levels which approximated ovulatory levels. A dose of 500 μg generated weekly estrogen values averaging 370 ± 18 pg/ml. This method is a satisfactory alternative to more traditional techniques. It involves no surgical procedures, it is relatively nonintrusive, it does not terminate a female's reproductive career, and it is not as time-consuming as daily injections. Female cycle state can be altered with a minimum of manipulation for studies involving the behavior of estrous females.     

Genetic variation in transferrin alleles of rhesus macaques, Macaca mulatta

The rhesus macaque displays an extensive polymorphism at the transferrin locus. A principal components analysis describes the variance and covariance of alleles at the transferrin locus in eight widely dispersed sample populations. Using an eigenvectorial representation of the covariance matrix and systematically approximated geographical locations the distribution of populations and transferrin alleles is compared. Alleles with high variance prove to be the determining factor in the placement of populations in a "genetic map" and provide a means for interpreting the low congruence of genetics and geography found.     

Pair-housing rather than single-housing for laboratory rhesus macaques

A total of 378 adult and juvenile rhesus macaques of both sexes were transferred from single- to isosexual pair-housing arrangements. The incidence of serious injury resulting from partner incompatibility was 0.8% during the first year after pair formation. It was concluded that pair-housing offers a safe option to address the animals' social needs in compliance with federal rules and professional standards.     

Paternity exclusion in six captive groups of rhesus monkeys (Macaca mulatta)

Five genetic markers were employed to attempt to identify the fathers of 135 Macaca mulatta offspring living in large outdoor field cages. Family studies of two of these markers to confirm mode of inheritance of phenotypes had not heretofore been reported. Of the 284 exclusions required to identify the fathers of all 135 monkeys, 198 (or 70 percent) were possible using only these five genetic polymorphisms. For 58 (or 43 percent) of these 135 offspring the father was identified. These data were applied to estimate the association between dominance rank of fathers and reproductive success. Fertility of first- and second-ranking fathers was judged to be about twice as high as that of third- and fourth-ranking fathers.     

Consequences of group fission for the patterns of relatedness among rhesus macaques

When mammalian social groups exceed their optimal size, they often tend to split. In view of the potential evolutionary benefits, it should be more advantageous for animals to stay with kin, rather than nonkin, during such fission events. In the present study, the spontaneous fission of two social groups, R and S, of rhesus macaques living on Cayo Santiago, Puerto Rico, provided the opportunity to compare the kinship structure of the corresponding parent and daughter groups, using information on both maternal and paternal relatedness. In both instances, maternal half-siblings and pairs of animals from the same family were significantly more prevalent in the fission products than in the parent group. During the split of group R, significantly more paternal half-siblings stayed in the remnants of the parent group than joined the seceding group. Our findings are compatible with previous behavioural studies demonstrating that female primates bias their social behaviour more to maternal than to paternal kin, but that both types of half-siblings prefer each other more than unrelated animals. It remains to be clarified by future research, however, whether the observed co-segregation of paternal half-sibs in our study reflects active choice or is a by-product of the group-specific kin structures, prior to fission.     

Antibody responses to two encephalomyocarditis virus vaccines in rhesus macaques (Macaca mulatta)

Abstract: Two groups of rhesus macaques (Macaca mulatta) housed in rodent-controlled outdoor corrals were inoculated with two different encephalomyocarditis virus (EMCV) vaccines. One group (n = 45) received a vaccine made from an inactivated field isolate of virus cultured during an outbreak at a zoo in Florida. This vaccine produced fourfold increases in the titers of 28 animals (62%); the increases persisted for at least 18 months (last test) after a single injection of the vaccine. The other group (n = 51) received a vaccine made from an inactivated porcine field strain of the virus. This vaccine did not produce titers in any of the vaccinees.     

Aspects of fight interference in free-ranging and compound-dwelling rhesus macaques (Macaca mulatta)

Patterns of fight interference (agonistic aiding) were compared among three groups of rhesus monkeys (Macaca mulatta) living in two settings: (1) two groups at Cayo Santiago (Caribbean Primate Center); and (2) one group at the Yerkes Regional Primate Research Center (YRPRC). A total of 1,227 interference episodes were recorded in 1,650 hours of observation. The only significant intergroup difference was the increased tendency of males at YRPRC to aid aggressors rather than victims. Among other findings, females aided relatives, interfered against target animals dominant to themselves, aided juveniles, and aided victims more consistently and frequently than did males. Importantly, female interference became more male-like in pattern when aid was given to nonrelatives. Neither the dominant males nor males in general displayed a unique or consistent tendency to interfere in fights in a manner which could be interpreted as controlling aggression. The males' interference patterns also did not suggest they were forming coalitions to either attain or defend status rankings. It is concluded that, overall, observations of compound-dwelling and free-ranging rhesus monkeys reveal similar relationships. Further, while female rhesus monkeys interfered in fights in a manner consistent with the control of aggression and protection of kin, the motives of male interferers remain unknown; however, their behavior is consistent with the hypothesis that they were reducing intermale tensions while, at the same time, minimizing physical risk.     

Glucose disappearance rate in rhesus monkeys: Some technical considerations

The intravenous glucose tolerance test (IVGTT) has been widely used as a tool to assist in the diagnosis of diabetes mellitus. Glucose disappearance rate (K_G) is calculated as an indicator of relative glucose tolerance; however, a standardized dose, consistent sampling times, and a consistent formula for the calculation of K_G have not yet been established for rhesus monkeys. Interpretation of results reported by different laboratories has, therefore, been rendered difficult. In the present study, 48 IVGTTs obtained from 33 male rhesus monkeys ranging widely in glucose tolerance have been analyzed. Various formulas for calculating K_G values have been tested in all experiments including a range of different pairs of time points, as well as the t_1/2. Regression analysis revealed that the log_e transformation of the plasma glucose levels obtained after an intravenous glucose load were best fitted with a straight line during the period between five and 20 minutes (R² = 0.97 ± 0.005). The use of time points prior to the five-minute value tended to produce spuriously larger K_G values, while sampling points that were later than 30 min occasionally produced an invalid K_G because in some monkeys the plasma glucose levels had already returned to basal levels. The advantages of using the five- and 20-minute glucose levels in calculating the K_G include (1) the optimal reflection of tissue uptake of glucose; (2) the relatively short sampling time required to obtain an accurate, consistent, and meaningful value for K_G; and (3) the relative ease in the calculation of K_G.     

The formal hierarchy of rhesus macaques: An investigation of the bared-teeth display

Teeth-baring in a large captive rhesus monkey group (Macaca mulatta) was observed over a 30-month period. Its directional consistency among adults was significantly higher than that of aggression. The unidirectionality was so extreme that the facial display must be seen as a formal status indicator; ie, a signal of which the direction is independent of short-term contextual variation. As such, it seems adapted for communication about the state of the relationship. Formal dominance relationships among adults could be arranged in a hierarchy which approached perfect linearity. Focal observations demonstrated that teeth-baring was associated with withdrawal. It was uncommon among foraging monkeys, perhaps because dominant animals paid less attention to their subordinates in this context. The speed of rank acquisition by young females, in terms of received teeth-baring, was highest among peers and lowest against the group's old matriarchs. The age at which dominance over unrelated adult females was achieved correlated negatively with the amount of affiliative contact with these females. This translates into a positive correlation between bonding and rank establishment, indicating that dominance processes may be indistinguishable from social integration.     

Hormonal effects of early rearing conditions in the infant rhesus monkey

Mother-reared and nursery-reared rhesus monkeys were evaluated during the first month of life to assess the effects of early rearing on endocrine status in infancy. Plasma cortisol and growth hormone (GH) levels were measured in two conditions: (1) basal and (2) 30 min following removal from either the mother or the nursery. Nursery-reared infants had lower basal GH levels and higher cortisol levels than did mother-reared infants. Both GH and cortisol levels rose significantly following separation and reached similar levels in the mother-reared and nursery-reared infants. Mother-reared animals exhibited higher GH levels in response to a pharmacological GH-stimulation test. Thus nursery rearing of primate infants significantly affected the baseline secretion of two important endocrine systems, but did not appear to alter markedly the acute endocrine response to a psychological stressor.