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.     

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.     

Supernumerary epiphyses in the macaque (Macaca nemestrina).

The frequency, age distribution and development of supernumerary epiphyses in the hand and foot were radiographically documented in 98 macaque fetuses and infants. Extra epiphyses were observed only on distal metacarpal 1 and metatarsal 1, and were present in 15% of a cross-sectional sample and 20% of a longitudinal sample. They appeared coincidentally with the ossification of other secondary epiphyses of the hand and foot. Development of extra epiphyses in this species seems to be a normal phenomenon.     

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.     

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.     

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.     

Ossification in the hand and foot of the pigtail macaque (Macaca nemestrina). II. Order of appearance of centers and variability in sequence

The order of appearance of the carpals, tarsals and secondary epiphyseal centers in the hand-wrist and foot-ankle regions of the fetal and infant pigtail macaque (Macaca nemestrina) was reconstructed using a cross-sectional sample of 127 animals and a longitudinal one of 14 animals. Comparison of the most common sequence in the monkey with that described in the human studies showed major interspecific differences in the order of appearance of several groups of centers, particularly those involving the thumb and great toe. The monkey displays a degree of sequence variability equivalent to that documented by the human longitudinal data, with certain centers markedly variable in timing and/or order of appearance. The evidence from related animals suggests a strong genetic component underlying some of the variable sequences observed, as has been reported in the human studies. The demonstrated variability in both timing and sequence precludes the use of specific centers in the determination of gestational age in fetuses of unknown conception date.     

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.     

Sex differences in use of a species-typical facial gesture by pigtail monkeys (Macaca nemestrina)

A species-typical gesture, the “jaw thrust”, was sequentially analyzed in a group of adultM. nemestrina. The major finding was a sex difference in apparent function with male jaw thrust sequences most likely to result in sexual behavior and female sequences most likely to terminate in agonistic behavior. Sex differences in the initiation and reception of jaw thrusts were also observed; they were most commonly initiated by males and directed toward females. Marked stereotypy of the behavioral sequences including jaw thrusts was observed: only a small proportion of the species’ behavioral repertoire was exhibited in temporal association with the gesture. Despite the striking nature of the gesture and the frequency with which it was exhibited, a majority of the signals had no overt social effect.     

The skin of primates. XXXVII. The skin of the pig-tail macaque (Macaca nemestrina)

The skin of the pig-tail macaque is basically similar to that of the rhesus monkey and the stump-tail macaque. The epidermis is thin and contains occasional basal melanocytes. The dermis, rich in elastic fibers, is practically free of pigment-containing cells. The upper dermis is highly vascular in the perianal region and sex skin. Cholinesterase-reactive nerve endings are plentiful beneath the friction surfaces of the pes and manus, mucous membranes, and junction of the hairy gluteus and glabrous ischial callosity. Hederiform-like endings are present in the eyelid, pinna, and frontal scalp. Apocrine and eccrine sweat glands occur throughout the hairy skin in a 2–3: 1 ratio. Both types are invested by nerves reactive for acetyl- and butyrylcholinesterase.     

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.     

Teratogenic effects of retinoic acid in pigtail monkeys (Macaca nemestrina). I. General features.

Daily oral administration of 10 mg/kg retinoic acid to pregnant Macaca nemestrina monkeys on days 20 to 44 resulted in a high frequency of craniofacial and musculoskeletal malformations. Craniofacial defects including cleft palate and anomalies of the prinna were common as were ectrodactyly, kyphosis, and muscular-joint contractures. Transposition of the great vessels of the heart occurred in one animal and polycystic kidney and associated urogenital anomalies in another. Shorter treatment periods with similar or higher dosages were not teratogenic and were less fetocidal. Although only relatively long treatment courses were teratogenic, the defects that resulted were morphologically similar to those induced with retinoic acid or other vitamin A compounds in other animal orders.     

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.     

Progesterone treatment suppresses estrogen receptor in the sex skin of Macaca nemestrina

We measured tightly bound nuclear estrogen receptors (ER) in sex skin biopsies obtained from pig-tailed macaques (Macaca nemestrina) which were previously ovariectomized and treated with an estradiol-progesterone regimen. Incubation of fresh tissue slices with a saturating concentration of [3H]estradiol (E2) was done to determine the capacity of nuclear acceptor sites to bind activated ER with high affinity. The radiolabeled ER was extracted from nuclei with 0.5 M KCl, complexed with an anti-ER monoclonal antibody, and quantitated by analysis on sucrose gradients. Even though serum E2 levels were unchanged, 7 and 14 days of sequential progesterone (P) treatment decreased ER amounts below those found after 7, 14 and 21-23 days of E2 treatment. ER regulation in sex skin of this species is similar to that found in macaque reproductive tract; P suppresses ER levels even in the presence of continuous E2. The tissue responses of sex skin to the hormone treatments correlated well with the measured fluctuations of tightly bound nuclear ER, which suggests the functional significance of this ER component.     

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.     

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.     

The pigtail macaque (Macaca nemestrina) model of COVID-19 reproduces diverse clinical outcomes and reveals new and complex signatures of disease

The novel coronavirus SARS-CoV-2, the causative agent of COVID-19 disease, has killed over five million people worldwide as of December 2021 with infections rising again due to the emergence of highly transmissible variants. Animal models that faithfully recapitulate human disease are critical for assessing SARS-CoV-2 viral and immune dynamics, for understanding mechanisms of disease, and for testing vaccines and therapeutics. Pigtail macaques (PTM, Macaca nemestrina) demonstrate a rapid and severe disease course when infected with simian immunodeficiency virus (SIV), including the development of severe cardiovascular symptoms that are pertinent to COVID-19 manifestations in humans. We thus proposed this species may likewise exhibit severe COVID-19 disease upon infection with SARS-CoV-2. Here, we extensively studied a cohort of SARS-CoV-2-infected PTM euthanized either 6- or 21-days after respiratory viral challenge. We show that PTM demonstrate largely mild-to-moderate COVID-19 disease. Pulmonary infiltrates were dominated by T cells, including CD4+ T cells that upregulate CD8 and express cytotoxic molecules, as well as virus-targeting T cells that were predominantly CD4+. We also noted increases in inflammatory and coagulation markers in blood, pulmonary pathologic lesions, and the development of neutralizing antibodies. Together, our data demonstrate that SARS-CoV-2 infection of PTM recapitulates important features of COVID-19 and reveals new immune and viral dynamics and thus may serve as a useful animal model for studying pathogenesis and testing vaccines and therapeutics.