Evidence for a lentiviral etiology in an epizootic of immune deficiency and lymphoma in stump-tailed macaques (Macaca arctoides).

A retrospective study determined that an epizootic of immune suppression and lymphoma in stump-tailed macaques (Macaca arctoides) that began in 1976 was associated with a horizontally spread lentivirus infection. This conclusion was based on serology, epidemiology, pathology, and virus isolation. The lesions found in the stump-tailed macaques were more compatible with lesions seen in SIV-infected rhesus than those seen in rhesus macaques infected with type D retroviruses. A lentivirus, isolated from a rhesus inoculated with lymph node homogenate from a stump-tailed macaque, was designed SIVstm and was pathogenic for rhesus macaques. The isolate was antigenically related to other SIVs as well as to HIV-1 and HIV-2. Two surviving stump-tailed macaques sent to another colony carried SIVstm latently for at least 7 years and disseminated it throughout that colony.     

四足型灵长类踝关节的生物力学研究

对猕猴属５种踝关节和跟骨生物力学和多变量分析的结构表明,踝关节的运动主要与距骨关节面的形态有关。楔形指数和跟骨指数是区别种间差异的重要指标。结合生态学观察的结果推测,短尾猴和藏酋猴的运动方式最为接近,表现出适应地栖四足型运动的特征,而豚尾猴和熊猴有关对的树栖运动方式,猕猴的运动介于两者之间,既有一定的地栖性运动,也有较大的树栖性运动。     

Weights and heights of stump-tailed macaques (Macaca arctoides) living in colony groups.

Weights and heights of adults, week-old infants, and animals of intermediate ages were obtained from colony groups of stump-tailed macaques and are compared with similar measurements of rhesus, Japanese macaques, and other stump-tailed monkeys.     

X-ray induced translocations in premeiotic germ cells of monkeys

The induction of reciprocal translocations by various X-ray exposures was studied in spermatogonial stem cells of rhesus monkeys (Macaca mulatta) and stump-tailed macaques (Macaca arctoides) by means of spermatocyte analysis many cell generations after irradiation. The yields of translocations recovered from irradiated stump-tailed macaques were lower than those observed in rhesus monkeys and represent in fact the lowest induction rates per Gy ever recorded for experimental mammals. In the rhesus monkey a humped dose-effect relationship was found with (a) a homogeneous response with (pseudo-)linear kinetics below 1 Gy, (b) much more variability at higher doses, and (c) no induction at all at doses of 4 Gy and above. It is suggested that the post-irradiation proliferation differentiation pattern of surviving rhesus monkey spermatogonial stem cells i mainly responsible for these characteristics of the dose-response curve.     

Amino acids in the plasma of fasting Japanese monkeys (Macaca fuscata fuscata andM. f. yakui)

The plasma levels of 26 amino acids and related compounds were determined in five male and five female adult members of each of the two subspecies of Japanese monkeys,Macaca fuscata fuscata andM. f. yakui. Activities of L-asparaginase and histaminase in plasma were also measured.Numerous differences in amino acid levels between the sexes in the subspeciesfuscata were noted, with the female consistently exhibiting lower values. Few differences were observed between the sexes of the subspeciesyakui or between the two subspecies of Japanese monkeys. These monkeys were similar to other previously studied nonhuman primates in exhibiting measurable levels of 3-methylhistidine in plasma. There were numerous quantitative differences among Japanese monkeys and stump-tailed macaques, rhesus monkeys, chimpanzees, and man, with the Japanese monkeys usually exhibiting higher plasma levels.L-asparaginase activity was not detectable in these Japanese monkeys. Histaminase activity was similar to that previously measured in pig-tailed macaques and chimpanzees, lower than that in rhesus monkeys and stump-tailed macaques, and higher than that in man.     

Blood groups of macaques:a comparative study.

Distribution of the human-type and of the simian-type blood groups in rhesus, crab-eating, bonnet, pig-tailed and stump-tailed macaques revealed significant similarities and differences among these species. Human-type A--B-O blood groups cut across taxonomic lines and seem less value for taxonomic purposes than the simian-type blood groups detected by cross-reacting isoimmune rhesus monkey sera.     

Molecular phylogeny of macaques: implications of nucleotide sequences from an 896-base pair region of mitochondrial DNA

We determined the nucleotide sequences of an 896-base pair region of mitochondrial DNA (mtDNA) from 20 primates representing 13 species of macaques, a baboon, and a patas. We compared these sequences and the homologous sequences from four macaques and a human against each other and deduced the phylogenetic relationships of macaques. The results from the phylogenetic analyses revealed five groups among the macaques: (1) Barbary macaque, (2) two species of Sulawesi macaques, (3) Japanese, rhesus, Taiwanese, crab-eating, and stump-tailed macaques, (4) toque, pig-tailed, and lion-tailed macaques, and (5) Assamese and bonnet macaques. The phylogenetic position of Tibetan macaque remains ambiguous as to whether it belongs to the fourth or fifth group. Phylogenetic trees revealed that Barbary macaque diverged first from the other Asian macaques. Subsequently, the four groups of Asian macaques diverged from one another in a relatively short period of time. Within each group, most of the species diverged in a relatively short period of time following the divergence of the groups. Assuming that the Asian macaques diverged from the outgroup Barbary macaque three million years ago (MYA), the divergence times among groups of Asian macaques were estimated at 2.1-2.5 MYA and within groups at 1.4- 2.2 MYA. The intraspecific nucleotide diversity observed among three rhesus macaques was so large that they did not form a monophyletic cluster in the phylogenetic trees. Instead, one of them formed a cluster with Japanese and Taiwanese macaques, whereas the other two formed a separate cluster. This implies that either polymorphisms of mtDNA sequences that existed before the divergence of these three species (ca. 700,000 years ago) have been retained in rhesus macaques or introgression has occurred among the three species.      

Comparative anatomy and histology of the cervix uteri in non-human primates

The uterine cervix of rhesus macaque, crab-eating macaque, stump-tailed macaque, pig-tailed macaque, marmoset, baboon, patas, and squirrel monkeys was studied macroscopically and microscopically. Distribution of spermatozoa and leukocytes in the lumen and within the crypts and clefts was studied in rhesus and marmoset uterine cervix. The cervical canal of baboon, patas, marmoset, and stump-tailed monkeys is straight or slightly bent. The presence of variably developed ventral and dorsal colliculi in rhesus, crab-eating, and pig-tailed macaques causes the dorsoventral sinuosity of the cervical canal. The cervix of all investigated specimens is fundamentally fibrous tissue and the amount of muscle fibers increases toward the uterine corpus. The cervical mucosa of baboon, marmoset, and patas monkeys contains a large amount of clefts and tubular tunnels of variable structure, length, width, direction, and degree of branching. The cervical mucosa of macaques contains a large number of crypts of complex structure, length, width and degree of branching. The cervical crypts in macaques are usually longer in the ectocervix; whereas, in the midcervix, mucosa contains small crypts, clefts and long tunnels. Squamo-columnar junction is located near the external os in baboon, patas, marmoset, rhesus, crab-eating, and pig-tailed monkeys. In squirrel monkey, squamous epithelium is continuous through the external os, covers the vestibule and external surface of the cervical colliculi. In stump-tailed macaque, squamo columnar junction is located in the vagina, 1–3 cm from the external os of the cervix. The vaginal wall between the squamo-columnar junction and the external os of the cervix is covered with heavily branched mucosa lined with columnar epithelium. Ciliated cells of cervical epithelium occur in 9 to 19%. A large number of spermatozoa and a relatively low number of leucocytes have been found within crypts and clefts of cervical mucosa. The results are discussed in relation to the function of the cervix in different stages of the cycle, during pregnancy and parturition.This investigation was supported in part by Ford Foundation Grant No. 710-0287.     

四种猕猴属动物精母细胞联会复合体的比较研究

本工作采用去污剂微铺展——硝酸银染色技术研究熊猴、平顶猴、藏酋猴、恒河猴及其亚种毛耳猴的精母细胞联会复合体（SC）核型、SC的结构及其在减数分裂中的行为。结果表明这几种动物的SC核型以及SC的发育过程基本一致。SC的形成开始于偶线期,成熟于粗线期,解体于双线期。在减数分裂前期,性染色体轴呈强嗜银性,配对明显落后于常染色体。根据减数分裂前期性染色体的形态和行为,性染色体的配对可分为五种类型。此外,本文还对XY染色体的同源性和侧轴加粗等现象进行了讨论。     

Blood groups of pig-tailed macaques (Macaca nemestrina).

The human-type A-B-O blood groups of 57 pig-tailed macaques (Macaca nemestrina) were determined and the calculated gene frequencies, O = 0.8908, A = 0.0825 and B = 0.0267, gave excellent fit with the hypothesis of inheritance by triple allelic genes. In tests for simian-type blood groups with rhesus, baboon and crab-eating macaque immune antisera, it was shown that the red cells of pig-tailed macaques are polymorphic for several simian-type specificities defined by those cross-reacting sera. Pig-tailed macaques share with other macaque species the complex Drh-graded blood group system, which seems to occupy a special role among red cell antigens of macaques. Normal sera of three female macaques contained spontaneous isoagglutinins which selectively agglutinated the red cells of some pig-tailed as well as stump-tailed macaques.     

Copulatory behavior in relation to anatomical characteristics of three macaques

Anatomy of copulatory organs and patterns of copulatory behavior were studied in three species of Macaca. The copulatory behavior of the rhesus monkey (M. mulatta) and crab-eating macaque (M. fascicularis) were similar. Mounting time was longer in stump-tailed macaque (M. arctoides) (48 seconds) than in the rhesus monkey or crab-eating macaque (8.5 seconds). Species differences were correlated with anatomical differences in the female and male reproductive organs. In the stump-tailed macaque the male has a relatively long penis, and the female has an elaborate vestibular colliculus in the vestibule. Both rhesus and crab-eating macaques have a short penis, and the female has no vestibular colliculus. Under scanning electron microscope, cone-like projections (3–4 mm) were observed on the surface of the glans and corpus penis of M. arctoides. In M. fascicularis shorter projections (0.05–0.1 mm) were observed on the glans penis but not the corpus penis.     

Nonhuman Primates in the Namdapha National Park, Arunachal Pradesh, India

Namdapha National Park and Tiger Reserve in the Changlang District of Arunachal Pradesh in northeastern India are rich in biodiversity. The dense evergreen forest of the park with high canopy coverage supports a variety of fauna including primates. In February, 2002, we surveyed the primates in Namdapha National Park to assess their status. We directly sighted, 5 species of diurnal primates, and secondary information shows the presence of stump-tailed macaques and slow lories. We encountered 10 groups of hoolock gibbons (33 individuals), 9 troops of capped langurs (61 individuals), 15 groups of Assam macaques (209 individuals), 6 groups of rhesus macaques (74 individuals) and one unidentified group of macaques (15 individuals). Hunting, rather than habitat destruction, is the chief potential threat for primates in the park.     

Morphometric analysis ofMacaca arctoides andM. thibetana in relation to other macaque species

As a first step in reviewing the classification of the two stump-tailed macaque species,Macaca arctoides andM. thibetana, as compared with other species of the genusMacaca, 72 linear dental and cranial variables of 11 macaque species were examined by morphometric analyses. The results indicate that the two stump-tailed species are the largest of the macaques and although rather similar overall, they exhibit significant differences in the pattern of variation in most of the five skull regions as shown by Principal Components and Canonical Variate Analyses. Euclidean Distances based on Canonical Variate scores indicate that the females ofM. arctoides andM. thibetana are more widely separated than eight other pairs of macaque species, and that the separations of the respective males are greater than those of three other pairs of species. These findings are consistent withFooden's classification of the stump-tailed macaques as two separate species (Fooden, 1976;Fooden et al., 1985). The present results suggest, as other researchers have proposed on the basis of external features, biochemistry and genetics, that the two stump-tailed macaque species andM. assamensis are closely related. The results also tentatively imply associations withM. fuscata andM. sylvanus but these require further study. The findings have implications for the assessment of the various Chinese Pleistocene macaque fossils.     

TRIM5 Suppresses Cross-Species Transmission of a Primate Immunodeficiency Virus and Selects for Emergence of Resistant Variants in the New Species

Simian immunodeficiency viruses of sooty mangabeys (SIVsm) are the source of multiple, successful cross-species transmissions, having given rise to HIV-2 in humans, SIVmac in rhesus macaques, and SIVstm in stump-tailed macaques. Cellular assays and phylogenetic comparisons indirectly support a role for TRIM5α, the product of the TRIM5 gene, in suppressing interspecies transmission and emergence of retroviruses in nature. Here, we investigate the in vivo role of TRIM5 directly, focusing on transmission of primate immunodeficiency viruses between outbred primate hosts. Specifically, we retrospectively analyzed experimental cross-species transmission of SIVsm in two cohorts of rhesus macaques and found a significant effect of TRIM5 genotype on viral replication levels. The effect was especially pronounced in a cohort of animals infected with SIVsmE543-3, where TRIM5 genotype correlated with approximately 100-fold to 1,000-fold differences in viral replication levels. Surprisingly, transmission occurred even in individuals bearing restrictive TRIM5 genotypes, resulting in attenuation of replication rather than an outright block to infection. In cell-culture assays, the same TRIM5 alleles associated with viral suppression in vivo blocked infectivity of two SIVsm strains, but not the macaque-adapted strain SIVmac239. Adaptations appeared in the viral capsid in animals with restrictive TRIM5 genotypes, and similar adaptations coincide with emergence of SIVmac in captive macaques in the 1970s. Thus, host TRIM5 can suppress viral replication in vivo, exerting selective pressure during the initial stages of cross-species transmission.     

中国猕猴生态学研究进展

中国的灵长类学研究始于19世纪中期之后,而兴盛于20世纪80年代至今。猕猴（Macaca mulatta）是世界及中国分布最为广泛的一种非人灵长类动物,在中国境内分布于17个省（市、区）,已被列为国家二级重点保护野生动物。迄今为止,学者们已对猕猴进行了包括地理分布、种群动态、食性、社会生态、保护生态等多方面的研究。本文拟对国内有关猕猴生态学方面的研究工作进行回顾与综述,以期通过对以往工作的汇总,梳理关于猕猴的研究线索与动态,并对今后的研究有所启示。     

Effect of photoperiod on characteristics of semen obtained by electroejaculation in stump-tailed macaques (Macaca arctoides)

Some environmental variables determining seasonal reproduction in mammals are temperature, humidity, food availability, and photoperiod. Among these, photoperiod is considered the main regulator of primates’ seasonal reproduction, thus the latitudinal distribution of primate populations is a key factor determining the appearance of seasonal reproduction. The present work presents supporting discrete seasonality in male stump-tailed macaques (Macaca arctoides). We investigated whether semen quality and testosterone covaried with Mexico City’s photoperiod and relative humidity by analyzing variations in the portions that form the ejaculate: the seminal liquid, the seminal coagulum, and the copulatory plug. Five male adult stump-tailed macaques were electroejaculated once a month, obtaining three semen samples per male, from August 2011 to July 2012 (except for December 2011) (n = 165). Our results showed that stump-tailed macaque sperm counts were significantly different between the portions of the ejaculate. The seminal coagulum contained the significantly largest number of spermatozoids, followed by the copulatory plug and the seminal fluid. Photoperiod and relative humidity had major influence on the sperm count in the seminal coagulum and the testosterone concentrations. Testosterone reached its highest values around the time when days and nights lasted the same hours, decreasing when days either grew longer or became shorter. Concerning relative humidity, sperm counts in the seminal coagulum were highly variable on dry days, but decreased as the relative humidity increased. We conclude that stump-tailed macaques have a discrete seasonality, occurring in spring and fall when macaques’ reproductive condition and readiness for postcopulatory intrasexual competition increase.     

Social communication among captive stump-tailed macaques (Macaca arctoides)

I compared the frequency of occurrence, contextual usage, and meaning of some of the most prominent gestural signals in stump-tailed macaques. I recorded the occurrence of 15 visual and tactile behavior patterns in a multimale multifemale captive group of stump-tailed macaques with the behavior sampling method in 100 hr of observation and analyzed the data via factor analysis and analyis of variance. The hindquarter presentation was the most frequent gesture. It was displayed by subordinates to appease dominants even in the absence of impending risk of aggression. Bared-teeth, lip-smack, teeth-chatter, and present-arm are submissive signals as well, but they differ from the presentation and from one another in their contextual usage. Nonthrusting mount, hip-touch, hip-clasp, and genital manipulation are directed down the hierarchy and appear to reflect dominance, reassurance, protection, or bonding. Mock-bite is a ritualized aggressive behavior pattern, often used to resolve uncertain dominance relationships. Ventroventral embrace occurs as a female bonding pattern. Overall, most gestural signals in stump-tailed macaques relate to dominance and submission and, to a lesser extent, social bonding.     

Pathogenicity of simian-human immunodeficiency virus SHIV-89.6P and SIVmac is attenuated in cynomolgus macaques and associated with early T-lymphocyte responses

Because most studies of AIDS pathogenesis in nonhuman primates have been performed in Indian-origin rhesus macaques (Macaca mulatta), little is known about lentiviral pathogenicity and control of virus replication following infection of alternative macaque species. Here, we report the consequences of simian-human immunodeficiency virus SHIV-89.6P and SIVmac251 infection in cynomolgus (Macaca fascicularis) and rhesus macaques of Chinese origin. Compared to the pathogenicity of the same viruses in Indian rhesus macaques, both cynomolgus and Chinese rhesus macaques showed lower levels of plasma virus. By 9 to 10 months after infection, both viruses became undetectable in plasma more frequently in cynomolgus than in either Chinese or Indian rhesus macaques. Furthermore, after SHIV-89.6P infection, CD4+ T-cell numbers declined less and survival was longer in cynomolgus and Chinese rhesus macaques than in Indian rhesus macaques. This attenuated pathogenicity was associated with gamma interferon ELISPOT responses to Gag and Env that were generated earlier and of higher frequency in cynomolgus than in Indian rhesus macaques. Cynomolgus macaques also developed higher titer neutralizing antibodies against SHIV-89.6 at 10 and 20 weeks postinoculation than Indian rhesus macaques. These studies demonstrate that the pathogenicity of nonhuman primate lentiviruses varies markedly based on the species or geographic origin of the macaques infected and suggest that the cellular immune responses may contribute to the control of pathogenicity in cynomolgus macaques. While cynomolgus and Chinese rhesus macaques provide alternative animal models of lentiviral infection, the lower levels of viremia in cynomolgus macaques limit the usefulness of infection of this species for vaccine trials that utilize viral load as an experimental endpoint.     

短尾猴下颌骨的性二型

对30个成年短尾猴下颌骨的8个有关变量作了性二型研究。单因子分析说明,8个变量均达到了显著差异水平。判别分析得到的第一判别式为:D=-11.013+1.151下颌骨髁长+0.269下颌骨髁宽。当D=-1.271±0.182时,标本为雌性;当D=0.973±0.290时为雄性。雄性下颌骨髁比雌性更长和更宽,且变化较为稳定,可作为种内性别间的鉴别特征。雄性比雌性具有较大咀嚼阻力臂(下颌长),但其他阻力臂则比雌性相对较短。与一些灵长类相同变量的比较说明,短尾猴下颌骨结构与猕猴较为接近,与长尾叶猴则相差甚远。这可反映它们食性和行为方面的亲疏关系。