Genetic characterization of rhesus macaques (Macaca mulatta) in Nepal

Indian-origin rhesus macaques (Macaca mulatta) have long served as an animal model for the study of human disease and behavior. Given the current shortage of Indian-origin rhesus, many researchers have turned to rhesus macaques from China as a substitute. However, a number of studies have identified marked genetic differences between the Chinese and Indian animals. We investigated the genetic characteristics of a third rhesus population, the rhesus macaques of Nepal. Twenty-one rhesus macaques at the Swoyambhu Temple in Kathmandu, Nepal, were compared with more than 300 Indian- and Chinese-origin rhesus macaques. The sequence analyses of two mitochondrial DNA (mtDNA) loci, from the HVS I and 12 S rRNA regions, showed that the Nepali animals were more similar to Indian-origin than to Chinese-origin animals. The distribution of alleles at 24 short tandem repeat (STR) loci distributed across 17 chromosomes also showed greater similarity between the Nepali and Indian-origin animals. Finally, an analysis of seven major histocompatibility complex (MHC) alleles showed that the Nepali animals expressed Class I alleles that are common to Indian-origin animals, including Mamu-A*01. All of these analyses also revealed a low level of genetic diversity within this Nepali rhesus sample. We conclude that the rhesus macaques of Nepal more closely resemble rhesus macaques of Indian origin than those of Chinese origin. As such, the Nepali rhesus may offer an additional resource option for researchers who wish to maintain research protocols with animals that possess key genetic features characteristic of Indian-origin rhesus macaques.     

Oxytocin and pair compatibility in adult male rhesus macaques (Macaca mulatta)

Pair housing is considered one of the best ways of promoting psychological wellbeing for caged macaques. However, incompatible partnerships can result in stress or aggression. Though previous studies have analyzed the role of variables such as age, weight, gender, and temperament on pair compatibility, few have examined the relationship between physiological parameters and pair compatibility. Oxytocin is known to promote prosocial nonsexual behavior in various primate species and may serve as an indicator of pair compatibility. In this study, we examined the association between peripheral oxytocin levels and prosocial behaviors in isosexual pairs of male rhesus macaques. We hypothesized that animals that demonstrated high levels of prosocial behaviors would have higher oxytocin levels than those showing low levels of the behavior. In addition, to elucidate the relationship between oxytocin and compatibility, we compared peripheral oxytocin between the highly affiliative animals and single‐housed males identified as having multiple unsuccessful pair attempts with multiple partners. We collected plasma oxytocin on 40 pairs of monkeys that had lived together for at least 1 month and 20 single‐housed animals. Further, we simultaneously collected behavioral data on the pairs, recording prosocial interactions (e.g., groom, play). Oxytocin varied among individuals, but was highly correlated between members of a pair (r = 0.58, p < .001). Additionally, prosocial behavior was positively correlated with plasma oxytocin (r = 0.38, p < .02). However, contrary to our expectations, oxytocin did not differ between single and highly affiliative pair‐housed animals (F_(1,38) = 0.71, p = .40). Our results suggest that oxytocin may be associated with the quality of isosexual pairs of male macaques. More work is needed to determine the nature of this relationship.     

Expression and metabolic activity of flavin‐containing monooxygenase 1 in cynomolgus macaque kidney

Flavin‐containing monooxygenase 1 (FMO1) largely remains to be characterized in cynomolgus macaque kidney. Immunoblotting showed expression of cynomolgus FMO1 in kidneys where activities of FMO1 (benzydamine N‐oxygenation) were detected. No sex differences were observed in their contents or activities. These results suggest the functional role of cynomolgus FMO1 in kidney.     

Genetic variants of serum butyrylcholinesterase in Chilean Mapuche Indians

We estimated the frequencies of serum butyrylcholinesterase (BChE) alleles in three tribes of Mapuche Indians from southern Chile, using enzymatic methods, and we estimated the frequency of allele BCHE*K in one tribe using primer reduced restriction analysis (PCR-PIRA). The three tribes have different degrees of European admixture, which is reflected in the observed frequencies of the atypical allele BCHE*A: 1.11% in Huilliches, 0.89% in Cuncos, and 0% in Pehuenches. This result is evidence in favor of the hypothesis that BCHE*A is absent in native Amerindians. The frequencies of BCHE*F were higher than in most reported studies (3.89%, 5.78%, and 4.41%, respectively). These results are probably due to an overestimation of the frequency of allele BCHE*F, since none of the 20 BCHE UF individuals (by the enzymatic test) individuals analyzed showed either of the two DNA base substitutions associated with this allele. Although enzymatic methods rarely detect the presence of allele BCHE*K, PCR-PIRA found the allele in an appreciable frequency (5.76%), although lower than that found in other ethnic groups. Since observed frequencies of unusual alleles correspond to estimated percentages of European admixture, it is likely that none of these unusual alleles were present in Mapuche Indians before the arrival of Europeans.     

A panel of 20 highly variable microsatellite polymorphisms in rhesus macaques (Macaca mulatta) selected for pedigree or population genetic analysis

This paper reports 20 new microsatellite loci that are highly polymorphic in rhesus macaques (Macaca mulatta). We screened known human microsatellite loci to identify markers that are polymorphic in rhesus macaques, and then selected specific loci that show substantial levels of heterozygosity and robust, reliable amplification. The 20 loci reported here were chosen to include one highly informative microsatellite from each rhesus monkey autosomal chromosome. Fourteen of the 20 polymorphisms are tetranucleotide repeats, and all can be analyzed using standard PCR and electrophoresis procedures. These new rhesus markers have an average of 15.5 alleles per locus and average heterozygosity of 0.83. This panel of DNA polymorphisms will be useful for a variety of different genetic analyses, including pedigree testing, paternity analysis, and population genetic studies. Many of these loci are also likely to be informative in other closely related Old World monkey species.     

Impact of internal and external factors on prosocial choices in rhesus macaques

While traditional economic models assume that agents are self-interested, humans and most non-human primates are social species. Therefore, many of decisions they make require the integration of information about other social agents. This study asks to what extent information about social status and the social context in which decisions are taken impact on reward-guided decisions in rhesus macaques. We tested 12 monkeys of varying dominance status in several experimental versions of a two-choice task in which reward could be delivered to self only, only another monkey, both the self and another monkey, or neither. Results showed dominant animals were more prone to make prosocial choices than subordinates, but only when the decision was between a reward for self only and a reward for both self and other. If the choice was between a reward for self only and a reward for other only, no animal expressed altruistic behaviour. Finally, prosocial choices were true social decisions as they were strikingly reduced when the social partner was replaced by a non-social object. These results showed that as in humans, rhesus macaques'' social decisions are adaptive and modulated by social status and the cost associated with being prosocial.This article is part of the theme issue ‘Existence and prevalence of economic behaviours among non-human primates’.     

Habituation and desensitization as methods for reducing fearful behavior in singly housed rhesus macaques

Operant conditioning using positive reinforcement techniques has been used extensively in the management of nonhuman primates in both zoological and laboratory settings. This research project was intended to test the usefulness of counter-conditioning techniques in reducing the fear-responses of singly housed male rhesus macaques living in the laboratory environment. A total of 18 male rhesus macaques (Macaca mulatta) were selected for this project and randomly assigned to one of three groups: a desensitization training group, a husbandry training group, or a control group. Behavioral data were collected before and after a 6 weeks training and/or habituation period during which the first two groups received a total of 125 min of positive reinforcement training (and also were assumed to undergo habituation to the environment) and the control group experienced only simple habituation to the environment. Based on a Wilcoxon Matched-Pairs Sign Test, we found that a significant proportion of animals exposed to desensitization training showed a reduction in the rate at which they engaged in cringing toward humans (exact significance=0.016, one-tailed, N-ties=6), cringing in general (exact significance=0.016, one-tailed, N-ties=6), and in stress-related behaviors (exact significance=0.016, one-tailed, N-ties=6). This was not the case for animals exposed to basic husbandry training or animals in the control group. A significant proportion of desensitization-exposed animals also showed a reduction in the duration of time spent cringing toward humans (exact significance=0.016, one-tailed, N-ties=6), but not in cringing behaviors in general or in stress-related behaviors. There were not a significant proportion of animals in either the husbandry training group or the control group that showed a decrease in duration of these behaviors. Results of this study could enhance both laboratory animal welfare and laboratory animal research, and could be a first step in developing techniques for reducing fearful behavior in rhesus monkeys in the laboratory environment.     

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.     

Normative nerve conductions in the tail of rhesus macaques (Macaca mulatta)

BACKGROUND: The aim of this study was to test the feasibility of using the tail of Macaca mulatta for neurophysiological testing of the peripheral nervous system. METHODS: Motor and sensory nerve conduction studies (NCS) of the tail were obtained by surface stimulation and recording. The technique utilized was novel. Unlike other NCS obtained from other peripheral nerves, this technique did not require any special neurophysiological expertise. RESULTS: The latency of the motor and sensory response was 2.5 +/- 0.71 and 1.1 +/- 0.27 ms respectively. The amplitude of the motor and sensory response was 8.1 +/- 5.1 mV and 14.6 +/- 9.4 microV respectively. Similar to human beings, there was a statistically significant relationship between age and motor amplitude, motor latency and sensory latency. CONCLUSIONS: Based on our results, a relatively simple, reproducible neurophysiological monitoring technique of the peripheral nervous system is possible.     

Computed tomography or necropsy diagnosis of multiple bullae and the treatment of pneumothorax in rhesus macaques (Macaca mulatta)

Pulmonary bullae and pneumothorax have various etiologies in veterinary medicine. We diagnosed multiple pulmonary bullae combined with or without pneumothorax by computed tomography (CT) or necropsy in seven rhesus macaques (Macaca mulatta) imported from China. Two of seven rhesus macaques accompanied by pneumothorax were cured by fixation of ruptured lung through left or right 3rd intercostal thoracotomy. Pneumonyssus simicola, one of the etiologies of pulmonary bullae, was not detected from tracheobronchiolar lavage. To the best of our knowledge, this is the first case report on the CT‐aided diagnosis of pulmonary bullae and the successful treatment of combined pneumothorax by thoracotomy in non‐human primates (NHPs).     

Changes in selected serum biochemical and EKG values with age in cynomolgus macaques

Normal serum values for alkaline phosphatase were significantly higher in juvenile male cynomolgus monkeys compared to adults. Conversely, blood urea nitrogen (BUN) was significantly lower in juveniles than adults. A comparison of selected EKG parameters from each group revealed no significant differences; however, there was a trend towards mean left axis deviation in adult animals.     

Restoration of sexual performance in old rhesus macaques paired with a preferred female partner

Experiments were undertaken to determine whether the decline in the ejaculation frequency of old male rhesus macaques is due to a decrease in physical capacity. In the first experiment, the capacity of old males to ejaculate in a series of biweekly tests was investigated. Six old (18–23 years) and six young (8– 12 years) male rhesus macaques were given 10-min tests of sexual behavior with nine different females chosen at random. The old males were also given 10-min tests with a preferred female, 1339. When the old males were tested with nine different females, their sexual performance (e.g., frequency of ejaculation) was significantly less than that of the young males, but their performance was comparable to that of young males in nine tests with female 1339. In a second experiment, the capacity of old males to show repeated ejaculations over a 3-hr period was tested. The same old and young males were given a 3-hr test with female 1339. The sexual performances (number of ejaculatory series completed and behavior displayed within each ejaculatory series) of the old males did not differ significantly from those of the young. Also, no significant differences in behavior were observed between young and old males during the first 10 min of the 3-hr tests. Our data show that the decline in the sexual performance of old rhesus males is not due to a decreased capacity to perform sexually or to physical debilitation.