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.     

Growth and developmental outcomes of three high-risk infant rhesus macaques (Macaca mulatta)

Infants classified as "high risk" are born with a greater chance of developing medical complications at birth, and may have cognitive and other developmental complications later in life. Very few reports exist regarding the survival and outcome of such infants in primate colonies. Here we present early growth and developmental data on three high-risk infant rhesus macaques (one female and two males) that were born either with intrauterine growth restriction (IUGR; born below the 1st birth weight percentile for gestational age) or extremely prematurely (at gestational days 128 and 140; mean full-term gestation=164 days). We compared the outcome of these infants with that of healthy controls born at term and found no gross developmental delays in these infants with respect to growth, neonatal reflex and motor skill development, early cognitive development, or social behavior. Neurological and cognitive assessments were compared in terms of both postnatal and gestational age. The survival of these infants was dependent on a 24-hr staffed nursery and a fluid protocol that catered to each high-risk infant's individual needs. When such measures are implemented, infants such as these have a good chance of survival and can serve as excellent models for high-risk human babies and their subsequent development.     

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.     

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.     

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.     

Leptin, adiposity, and testosterone in captive male macaques

Leptin is considered to act as a signal relating somatic energetic status to the reproductive system. However, the nature of that signal and its relationship with male reproductive function across nonhuman primate species are unclear. We suggest that species-specific differences in leptin physiology may be related to the degree of environmental variation and variation in the importance of energy stores for male reproduction. In order to test the role of seasonality in species differences among nonhuman primates, we compared leptin, testosterone, and body composition in male rhesus (n = 69) and pig-tailed (n = 43) macaques. Despite having larger abdominal fat deposits, the rhesus macaques did not exhibit significantly higher leptin levels (rhesus, 2.21 +/- 0.43 ng/ml; pig-tailed, 2.12 +/- 0.39 ng/ml). Both species showed increases in leptin across adolescent, subadult, and adult age-groups (P = 0.036 for rhesus; P = 0.0003 for pig-tailed by ANCOVA). Testosterone was not significantly associated with leptin in either the rhesus (r = 0.039; P = 0.754) or pig-tailed (r = 0.2862; P = 0.066) samples. Comparison of leptin levels across the two species using univariate modeling procedures showed no significant age-group by abdominal fat interaction. These findings suggest little difference in leptin production between these two closely related species, despite the difference in breeding seasonality.     

Treatment of nonspecific diarrhea with metronidazole in rhesus macaques

Nonspecific diarrhea was successfully treated with metronidazole in 76% (13/17) of cases in adult rhesus macaques (Macaca mulatta). Effective treatment was achieved by oral administration of metronidazole daily at a low dose of 250 mg for at least eight days or at high daily doses of 500-1,500 mg for one to four days. Minimal effective total dose was 1500 mg. Apart from occasional vomiting, no side effects were observed.     

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.     

Colon cancer in aged captive rhesus monkeys (Macaca mulatta)

The age-related incidence of malignant neoplasia was surveyed from a total of 301 necropsy cases of rhesus monkeys ranging in age from 13–37 years performed in the Pathology Service Unit of the Wisconsin Regional Primate Research Center during the past 15 years. All our aged monkeys lived in indoor cages and were fed with monkey chow and supplemental fruits during the past decades. In this survey, we found a total of 51 malignant neoplasms, and among them 25 cases were colon cancer. The incidence of colon cancer increased with advancing age: 3.2% at 13–19 years, 9.2% at 20–25 years, 13.5% at 26–29 years, and 20.7% at 30–37 years. Most cancers were located in the cecum and transverse regions with a unicentric origin. Two multicentric cases were associated with chronic hypertrophic colitis. Precancerous polypous lesions were not found in all cases. Histologically, all cases were mucinous adenocarcinoma and had local invasion to the muscular wall. Metastasis to the mesenteric lymph nodes was found in only two cases. As in humans, colon cancer is a common outcome of aging in nonhuman primates. Am. J. Primatol. 44:19–27, 1998. © 1998 Wiley-Liss, Inc.     

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.     

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.     

Phylogenetic analysis of chinese rhesus macaques (Macaca mulatta) based on mitochondrial control region sequences

Between one and six subspecies of Chinese rhesus macaques (Macaca mulatta) have been proposed based on morphological differences and/or their geographic distribution. In this study, a 489 base pair fragment of the mitochondrial control region was amplified from 230 DNA samples collected from rhesus macaques in the Sichuan province in Western China. The fragment was then sequenced and aligned with 208 sequences from wild rhesus macaques, sampled throughout the species' geographic range in China downloaded from GenBank. Phylogenetic analysis of the 182 unique sequences identified among these samples divided Chinese rhesus macaques into two western haplogroups (haplogroups A and B) and three older eastern haplogroups (haplogroups C, D, and E), whose differentiation probably occurred during the penultimate glacial event. During the warming after the penultimate glacial event, haplogroups A, B, and E rapidly expanded and a relatively young subhaplogroup of haplogroup E, E', limited to Southern China but shared with Vietnamese rhesus macaques, was reintroduced from Indochina during the last glacial event. One haplotype most closely related to subhaplogroup E' probably represents the isolation of Hainan Island, to where it is restricted, from the mainland by the formation of the Qiongzhou Strait approximately 8,500 years ago. The distribution of haplogroups both informs the phylogeographic history of dispersal of Chinese rhesus macaques and has implications for their suitability as animal models in biomedical research.     

Milk composition varies in relation to the presence and abundance of Balantidium coli in the mother in captive rhesus macaques (Macaca mulatta)

Primate infants require extensive maternal investment, and lactation is the most expensive aspect of this investment. However, the relationship between maternal condition and milk composition has been largely uninvestigated in primates. To better understand this relationship, I collected mid-lactation milk samples from 46 captive multiparous rhesus macaques (Macaca mulatta) at the Caribbean Primate Research Center, Sabana Seca Field Station, Puerto Rico. The maternal variables assessed were age, weight, weight for crown-rump length (CRL), and presence of parasites. Additionally the analysis included infant age, weight, and sex. Protein concentration in milk showed little interindividual variation, whereas fat had a high variance. Mothers without the lower intestinal parasite Balantidium coli had a significantly higher fat concentration in milk than mothers with B. coli, but other parasite species (Trichuris trichiura and Strongyloides fulleborni) were not associated with milk fat concentration. Females with younger infants had a higher fat concentration in their milk than mothers with older infants; however, the association between B. coli and milk fat remained significant after controlling for infant age. These results, obtained from a well fed captive population, indicate that even small differences among mothers are associated with milk composition.