Phylogeographic analysis of pigtail macaque populations (Macaca nemestrina) inferred from mitochondrial DNA

Mitochondrial DNA variation was surveyed in nine populations of the pigtail macaque (Macaca nemestrina), covering all three recognized subspecies in Southeast Asia. To do this, a 2,300 base pair fragment spanning the mitochondrial NAD 3 and NAD 4 genes and flanking tRNA subunits leucine and glycine was targeted for amplification and digested with a battery of 16 restriction endonucleases. Out of a total of 107 individuals, 32 unique haplotypes could be distinguished. Parsimony and neighbor-joining analyses grouped the haplotypes into five strongly supported assemblages representing China/Thailand, Malaysia, Sumatra, Borneo, and Siberut. These results indicate that the mainland and island mtDNA haplotypes are strictly and uniquely limited to the geographic ranges of the recognized morphological subspecies. Cladistic and neighbor-joining analyses indicate that inferred phylogenies of mtDNA haplotypes are congruent with subspecies designations. Furthermore, in support of morphological studies, results indicate that the Mentawai macaque is most likely not a distinct species but a subspecies of M. nemestrina. Am J Phys Anthropol 104:35–45, 1997. © 1997 Wiley-Liss, Inc.     

Correlation of perineal detumescence and ovulation in the pigtail macaque (Macaca nemestrina).

A study was made of the relationship between ovulation and perineal detumescence in the pigtail macaque (Macaca nemestrina). Daily laparoscopic examation of both ovaries was made beginning on the 9th day of the menstrual cycle. The appearance of the ovaries was recorded and photographs were taken of the perineum and ovaries. This procedure was repeated daily until the 5th day after ovulation or until the 20th day of the menstrual cycle for presumed anovulatory cycles. The time at which ovulation occurred was correlated with first signs of detumescence, both events occurring within a 24-hour period.     

Infant abuse associated with psychosocial stress in a group-living pigtail macaque ( Macaca nemestrina) Mother

This study reports a case of infant abuse by a pigtail macaque mother living in a captive social group. Patterns of abusive behavior appeared three weeks after the birth of the infant and were in strict temporal as sociation with the repeated kidnapping and severe harassment of the infant by the alpha-female in the group. Before and after the period of social stress, the mother exhibited proper caregiving behavior towards her infant. The analysis of the abusive mother's style of interaction with her infant relative to three control mothers indicated that she was an extremely permissive mother. It is argued that the mother's failure to adapt her mothering style to better protect her infant during the period of repeated kidnappings and the resulting lack of control over the situation may be the mechanism by which stress precipitated infant abuse. © 1994 Wiley-Liss, Inc.     

Group formation of female pigtail macaques (Macaca nemestrina)

Human epidemiological studies have suggested that social variables can modulate the effects of stress on the immune system, and this concept has been gaining increasing attention with positive results emerging from empirical studies using nonhuman primates over the last two decades. Results from a previous study in rhesus monkeys suggested that receiving grooming positively affected recovery of T-helper and T-suppressor cells following the initial stress associated with group formation, and this co-varied with high dominance rank. Thus, the present study was undertaken in order to determine: (1) if the stress effect of formation could be replicated in another species and (2) if social behaviors or dominance rank, given that formation is a stressor, might independently correlate with physiological recovery from the stressor. Eight adult female pigtail macaques were moved from individual cages and simultaneously introduced into an outdoor enclosure along with an adult male, while eight weight-matched controls remained in individual caging. Behavioral data were collected during the introduction and over 4 weeks thereafter. Blood samples were collected prior to and at intervals for 4 weeks following formation. Compared to control subjects, the test subjects showed an increase in basal cortisol secretion (+28.9%) and a significant decrease in T-helper cells (-33.6%), T-suppressor cells (-30.8%), and B cells (-22.5%), while there was a significant increase in white blood cells (+29.5%) 24 hr following formation. When dominance rank and seven behavioral categories were analyzed, only the frequency of receiving grooming significantly predicted change, with animals who received a greater frequency of grooms showing a lesser negative percent change from baseline in the absolute number of T-helper cells 1 week following formation. The establishment of a dominance hierarchy, apparent within 1 week, was accomplished with no serious fighting and a complete absence of wounding or trauma, suggesting that psychosocial stress was responsible for the physiological changes observed. © 1996 Wiley-Liss, Inc.     

Factors influencing aggressive behavior and risk of trauma in the pigtail macaque (Macaca nemestrina).

Several experiments and surveys were conducted in a large colony of pigtail macaques (Macaca nemestrina) to determine some of the influences of spatial and social factors on aggressive behavior and risk of trauma. Female subjects exhibited more aggression when they had access to two-room suites than when they had access to single rooms. The frequency of aggressive interactions among females was positively related to the number of females per group. The presence of one or more males in groups inhibited aggressive interaction among females. Less aggression occurred among females in groups containing infants than in groups containing no infants. Provision of cover by introduction of concrete cylinders into rooms reduced aggression among members of stable groups. Subjects in newly-formed groups composed of unfamiliar animals sustained fewer injuries than did those in groups formed by merger of groups or subgroups of familiar animals.     

Dyadic and triadic reconciliation in pigtail macaques (Macaca nemestrina)

The tendency in primates for former antagonists to approach and affiliate following aggression has been termed reconciliation because the response is thought to resolve social conflicts produced by aggression. In primate societies, however, an aggressive interaction between two individuals often spreads to include other group members, especially the kin of the combatants. If post conflict affiliation resolves aggressive conflicts in a group, then affiliative increases might occur between combatants and the kin of their opponents following aggression as well as between former opponents. This hypothesis was tested in a captive group of 39 pigtail macaques (Macaca nemestrina) by comparing affiliative response frequencies of combatants during the 5 minute period following aggression to affiliative response frequencies during 5 minute baseline periods not preceded by aggressive activity. Following aggression, affiliation rates increased between combatants and their opponents, aggressors and the kin of their opponents, and aggressors and their own kin. Additional analyses showed that aggression among kin was reconciled more often than aggression among nonkin. Recipients of aggression reconciled with their attackers more often than aggressors reconciled with their victims. Animals with similar dominance ranks reconciled proportionately more often than those with large rank disparities and aggressive infractions of a calculated dominance hierarchy were reconciled more often than attacks consistent with the hierarchy. Results suggest that both dyadic and triadic reconciliations occur in M. nemestrina and that compared to other primate species M. nemestrina exhibit a moderate-to-high conciliatory tendency.     

A field study of the pigtail monkey (Macaca nemestrina)

A field study of the pigtail monkey (Macaca nemestrina) was conducted in Malaysia. An initial six month survey revealed a badly disturbed, diminishing population. Intensive observation required prolonged extensive habituation efforts including a modified form of provisionization and the use of a trained captive pigtail monkey. The pigtail monkey was found to be an arboreal deep forest animal which, nonetheless, came to the ground more often than any other monkey in the forests of Malaya. Responses observed in the natural habitat could not be differentiated from those seen in captive groups; but response frequencies differed. Social patterns observed were similar to those seen in other macaques but differed notably from those seen in sympatric leaf monkeys. Travel patterns, feeding, agonistic responses, sexual behavior, play and other responses are described and discussed.     

Diurnal variation of common behaviors of pigtail monkeys (Macaca nemestrina)

Diurnal variation of eight common behaviors was studied in a social group of pigtail macaques (Macaca nemestrina). In agreement with previous work, all behaviors showed marked variation throughout the day, and differences between day and night levels were significant for most behaviors. Several significant inter-behavior correlations were found which suggested that common factors were major determinants of groups of behaviors. Significant correlations between separate diurnal cycles of sleep, grooming, and general activity demonstrated that these behaviors were among the most consistent with respect to diurnal cycles. The results point to the usefulness of diurnal studies in planning primate research designs, e.g., in controlling for variables associated with diurnal cycles.     

Catalogue of sounds of the Pigtailed macaque (Macaca nemestrina)

A catalogue of sounds from a laboratory population of Pigtailed macaques has been developed from spectograms. Sounds are divided into four general classes: clear, harsh and high-pitched calls, and miscellaneous sounds. It appears that all parameters of the vocal signal are independently manipulatable. A plot of selected spectral characteristics demonstrated the uniqueness of individual signals. In some instances, different sounds are developed by rearrangement of specific fragments, or by acoustical activities performed on similar sounds. This latter phenomenon, which will be termed mosaicism , parallels aspects of language design. Lastly, comparison of spectrograms for Pigtailed macaques with those published for Rhesus macaques ( Macaca mulatta ) reveals similarities in structure.     

Mhc-DRB genes of the pigtail macaque (Macaca nemestrina): implications for the evolution of human DRB genes.

The DRB family of human class II major histocompatibility complex (Mhc) loci is unusual in that individuals differ in the number and combination of genes (haplotypes) they carry. Indications are that both the allelic and haplotype polymorphisms of the DRB loci predate speciation. Searching for the evolutionary origins of these polymorphisms, we have sequenced five DRB clones isolated from a cDNA library of a pigtail macaque (Macaca nemestrina) B lymphocyte line. The clones represent five different genes which we designate Mane-DRB*01-Mane-DRB*05. The genes appears to be approximately equidistant from each other, so that allelic relationships between them cannot be established on the basis of the sequence data alone. If positions coding for the peptide-binding region of the class II beta chains are eliminated from sequence comparisons, the Mane-DRB genes appear to be most closely related to the human (HLA) DRB1 genes of the DRw52 group. We interpret this finding to indicate that the ancestral gene of the DRw52 group of human DRB1 alleles separated from the rest of the HLA-DRB1 alleles before the separation of the Old World monkeys (Cercopithecoidea) from the apes (Hominoidea) in the early Oligocene. After this separation, the ancestral DRB1 gene of the DRw52 group duplicated in the Old World monkey lineage to give rise to genes at three loci at least, while in the ape lineage this gene may have remained single and diverged into a number of alleles instead. These findings suggest that some of the polymorphism currently present at the DRB1 locus is greater than 35 Myr old.     

Social density and aggression in captive groups of pigtail monkeys (Macaca nemestrina)

A survey of aggressive behavior in 72 groups of pigtail monkeys (Macaca nemestrina) housed under identical spatial conditions revealed that frequency of contact aggression (grab, push, hit, bite) was directly related to social density. This result conforms with expectations of effects of crowding, but contrasts with previous work on responses to manipulation of spatial density. A similar paradoxical contrast between the effects of social density and spatial density has been documented in humans, and consequently development of a nonhuman primate model for study of crowding stress may be warranted. The choice of social density for captive nonhuman primate groups should be made with great care to avoid densities that result in destructive aggression.     

Heterochrony and sexual dimorphism in the pigtailed macaque (Macaca nemestrina)

Somatic growth is not a simple linear process with a constant rate of growth. The most successful attempts to quantify growth as a function of age or size have employed nonlinear techniques. Sexual dimorphism of primate growth, weight vs. age, was examined using nonlinear models with Sirianni and Swindler's ([1985] Growth and Development of the Pigtailed Macaque, Boca Raton, FL: CRC Press) growth data on the pigtailed macaque (Macaca nemestrina). The best fit of several exponential growth models was the Gompertz curve: Different multiple phase models were also fit, where each phase represents a distinct exponential component. The two-phase models proved to be the best (R² = .0.84 for females, 0.91 for males), suggesting that there are two growth spurts, one in infancy and one at puberty. The timing of the beginning and end of the first spurt is the same in males and females, but the rate, and value of the asymptote for this phase, is greater in males. The timing of the second spurt is earlier, and the rate of growth for this spurt is smaller in females than males. The sexual dimorphism in these species is not a simple rate change, but a complex interaction of timing and rate over the entire period of growth. It would be impossible to separate these entities with a linear, polynomial, or single-phase model of the data. While these data and results complement much of the existing work on adult dimorphism, they also emphasize the vital role that ontogenetic data have in elucidating the underlying evolutionary mechanisms that generate sexual dimorphism. © 1994 Wiley-Liss, Inc.     

Allogrooming in two species of macaque (Macaca nemestrina andMacaca radiata)

This paper analyzes allogrooming (social grooming) data collected from two large, fully integrated and long established social groups of macaques (one of pigtail macaques and one of bonnet macaques). The data demonstrates a species and sex difference for total allogrooming given with females of both species giving more grooming than the males and with pigtails as a species giving more grooming than bonnets. Also, pigtail females gave more allogrooming to clan members than to nonclan members, but this was not true for pigtail males, bonnet males, and bonnet females. Allogrooming given and allogrooming received by age class for both species showed development of a sexual dichotomy at three to four years. The analysis characterized some of the social structures extant in two closely related species of macaque, particularly the somewhat different use of allogrooming in pigtail females as opposed to the other three categories of animals. Social implications with relation to macaque societies are discussed.     

Detection of systemic amyloidosis in the pig-tailed macaque (Macaca nemestrina)

Secondary amyloidosis is a progressive systemic disease for which there is no reliable diagnostic assay, preventive measure, or treatment. In an attempt to elucidate an antemortem diagnosis, 30 female pig-tailed macaques (Macaca nemestrina) at the Washington National Primate Research Center were surveyed for amyloidosis. Amyloid was demonstrated histologically in 47% (14 of 30) of the animals. The distribution and severity of amyloid deposition was variable. Affected animals had a mean age (+/-1 standard deviation) of 13.2 +/- 4.9 y, which was significantly greater than the mean age of unaffected animals (9.3 +/- 4.1) y. Twelve tests were evaluated for detection of amyloidosis; the diagnostic value of each was determined through comparison of histologically positive and histologically negative animals. Diagnostic tests evaluated were endoscopic examination and biopsy of the stomach and colon, abdominal ultrasonography, hepatic radiology, serum amyloid A (SAA), endothelin 1, alpha-fetal protein, aspartate aminotransferase (AST), alanine aminotransferase, gamma-glutamyltransferase (GGT), alkaline phosphatase, cholesterol, blood urea nitrogen, total bilirubin, C-reactive proteins, and erythrocyte sedimentation rate. Amyloidotic animals demonstrated a distinctive serologic profile: elevated SAA, GGT, and AST in combination with decreased total protein and albumin. Radiology demonstrated hepatomegaly in animals with hepatic amyloid deposition. In the absence of known infection or trauma, an amyloidotic serologic profile and radiologic hepatomegaly are consistent with systemic amyloidosis in M. nemestrina.     

A periodic dosing model of fetal alcohol syndrome in the pig-tailed macaque (Macaca nemestrina)

A nonhuman primate on a periodic ethanol dosing schedule should provide a model of fetal alcohol syndrome (FAS) most relevant to the majority of pregnant women who are “social drinkers” and can exercise reasonable control over their ethanol intake. In this pilot study, four pregnant pig-tailed macaques (Macaca nemestrina) received ethanol once a week from 40 days' gestation. Doses were 2.5 gm/kg for three moderate-dose animals (MDAs) and 4.1 gm/kg for one high-dose animal (HDA). Peak blood ethanol levels reached a mean of 240–256 mg/dl for the MDAs and averaged 379 mg/dl for the HDA. Peak acetaldehyde did not vary with dose. One MDA aborted after the first dose. The other three pregnancies were compared with eight to ten control pregnancies, and the infants' development over the first six months was compared with that of the control offspring. Nutritional status of the pregnant females was normal. The fetal heart rate response to maternal restraint was absent in the HDA. Gestational duration and simian Apgar scores were normal. All three infants were abnormally large, and two were also abnormally heavy, with body weight appropriate to skeletal size. Skeletal maturation, judged by ossification and tooth eruption, was not accelerated. The high-dose infant (HDI) was scaphocephalic, with an underdeveloped cranial base and midface, and its brain was small and dysplastic; its reflex, motor, and cognitive development were retarded. One moderate-dose infant (MDI) had some brain abnormalities; it was hyperkinetic and showed developmental retardation on several behavioral measures. The other MDI was normal. We conclude that the periodic model offers an effective means of investigating FAS in M. nemestrina. Furthermore, when nutrition is maintained, intermittent intake of ethanol by the pregnant primate does not necessarily reatard fetal growth.     

Pregnancy outcomes after weekly oral administration of ethanol during gestation in the pig-tailed macaque (Macaca nemestrina)

Ethanol was orally administered once per week to gravid pig-tailed macaques (Macaca nemestrina) in doses of 0.3, 0.6, 1.2, 1.8, 2.5, 3.3, or 4.1 g/kg. A control group received a sucrose solution, isocaloric and isovolemic to the highest ethanol dose. Pregnancy was followed after 116 possible conceptions in 54 females. Peak plasma ethanol concentrations (PPECs) ranged from 24 +/- 6 mg/dl at the 0.3 g/kg dose to 549 +/- 71 mg/dl at the 4.1 g/kg dose. An increased rate of spontaneous abortion was related to ethanol exposure at and above 1.8 g/kg (mean PPEC = 205 mg/dl). Pregnancy failure in the first 30 days of gestation increased at doses above 2.5 g/kg. The effect on pregnancy outcome of weekly exposure to ethanol in this nonhuman primate is comparable to available data on humans. The methodology of this study represents an effective model for studying ethanol teratogenesis in a nonhuman primate.     

A comparison of two timed-mating strategies for breeding pigtail monkeys. (Macaca nemestrina)

Pigtail monkeys (Macaca nemestrina) were time-mated using female perineal “sex skin” tumescence cyclicity as an indicator of ovulation time. The goal of these matings was production of infants of known gestational age for an investigation using a nonhuman primate model to study causes, correlates, and consequences of premature birth. Two breeding strategies were employed. The first involved allowing breeders constant access to one another for 72 hours at the time ovulation was predicted to occur from previous data on cyclicity of perineal tumescence. The second method limited exposure to two hours daily until perineal detumescence occurred. The second strategy has been considerably more effective than the first.     

Sex differences in the acquisition of communicative competence by pigtail macaques (Macaca nemestrina)

Previous study of captive pigtail monkeys (Macaca nemestrina) revealed that victims of an attack by a group member employed one of four acoustically different recruitment calls (Gouzoules&Gouzoules: Animal Behaviour 37:383–401, 1989). The calls appear to provide allies with information pertinent to decisions about fight intervention. Each call was associated with an agonistic context distinguished by the relative rank of the opponent and the severity of the attack. Monkeys younger than 3 years of age were significantly less likely to use a contextually appropriate call than were older animals and their calls tended to be acoustically less like the prototype for a given context. Analyses reported on here revealed that, among juveniles, females were more proficient than males in both the proper contextual use and the production of these calls. These findings suggest parallels with human sex differences in the development of communicative competence. The evolutionary origins for these sex differences in macaque vocal development may be based in the different life history patterns males and females exhibit.     

Sex hormones correlated with sex skin swelling and rectal temperature during the menstrual cycle of the pigtail macaque (Macaca nemestrina).

Daily measurement of serum luteinizing hormone, estradiol-17beta, and progesterone were made during the menstrual cycle in nine pigtail macaques (Macaca nemestrina). All data were normalized to the day of the luteinizing hormone peak. Serum estradiol-17beta increased from approximately 100 pg/ml during the early follicular phase to 442 +/- 156 pg/ml during the maximum midcycle concomitant with the luteinizing hormone peak, and a small increase in serum estradiol-17beta was observed during the luteal phase coincident with the progesterone peak. Serum progesterone values increased slightly at the time of the luteinizing hormone peak and increased from 0.2-0.3 ng/ml during the midfollicular phase to peak levels of 8.3 +/- 1.75 ng/ml 9 days after the luteinizing hormone surge. Serum luteinizing hormone remained low and relatively constant throughout the early and midcycle, then sharply increased approximately four-fold to peak values of 6.25 +/- 0.9 ng/ml. Sex skin swelling increased slowly during the follicular phase and declined slowly throughout the early luteal phase. Rectal temperature did not change significantly throughout the menstrual cycle. The similarity of plasma sex hormone changes during the menstrual cycle between women and the pigtail macaque suggested that this nonhuman primate should be a useful animal model for studying human reproduction.