Testis size,epididymis weight,and sperm competition in rhesus macaques

The intensity of sperm competition is often measured using the gonadosomatic index (testes/body weight). But sperm competition could be mediated more by size of the epididymis than by size of the testicles, and little information is available on the relationship between testicular and epididymal size. We found that both organs were positively correlated in size among male rhesus macaques. Body weight accounted for over 70% of the variance in testicle size and volumetric estimates of testicle size accurately reflected testicle weight. We conclude that methods for ascertaining testicle size are accurate, but the covariation in size between testicles and epididymis will hamper understanding of the physiological mechanisms involved in sperm competition in primates. © 1993 Wiley-Liss, Inc.     

Effects of reproductive condition and dominance rank on cortisol responsiveness to stress in free‐ranging female rhesus macaques

The hypothalamic–pituitary–adrenal (HPA) axis modulates individuals' physiological responses to social stress, which is an inevitable aspect of the daily lives of group‐living animals. Previous nonhuman primate studies have reported that sex, age, rank, and reproductive condition influence cortisol levels under stressful conditions. In this study we investigated cortisol responses to stress among 70 multiparous, free‐ranging female rhesus macaques (Macaca mulatta) on the island of Cayo Santiago, PR. Plasma cortisol samples were collected in two consecutive years under similar conditions. Twenty‐two females were sampled both years, and most of those females were lactating in only one of the years. Individual differences in cortisol levels were stable across years, even though reproductive condition changed for most individuals. No relationship was found between age or social rank and cortisol levels. Of the females that changed reproductive conditions, cortisol levels were higher when they were lactating than when they were cycling, and the amount of change in cortisol from cycling to lactating was greatest for low‐ranking individuals. Heightened reactivity to stress during lactation may be the result of concerns about infant safety, and such concerns may be higher among low‐ranking mothers than among higher ranking mothers. Psychosocial stress and hyperactivation of the HPA axis during lactation can suppress immune function and increase vulnerability to infectious diseases, thus explaining why adult females in the free‐ranging rhesus macaque population on Cayo Santiago have a higher probability of mortality during the birth season than during the mating season. Am. J. Primatol. 72:559–565, 2010. © 2009 Wiley‐Liss, Inc.     

Decrease in sexual initiative and responsiveness in female rhesus macaques (Macaca mulatta) during pregnancy

Although the sexual behavior of female rhesus macaques (Macaca mulatta) has been reported to decrease during pregnancy, systematic studies have been largely confined to reports of male behavior. Therefore, we designed a study to examine changes in female sexual behavior during pregnancy. Six cycling multiparous female rhesus macaques were paired during the periovulatory period of the menstrual cycle and during the first and second halves of pregnancy with six sexually experienced males of the same species. Each female was paired with the same male in all tests. The means of the behavioral measures scored on days 11–13 of the menstrual cycle, 35–56 of pregnancy, and 147–168 of pregnancy were compared. Females showed a significant decrease in the present contact ratio and the rate of threat-aways during pregnancy. Males showed lower rates of threatening-away, contacting, mounting, intromitting, and ejaculating when females were pregnant. The extent to which the decrease in male sexual behavior can be accounted for by an increase in female rejection is uncertain, but it is probably as significant as any loss of attractiveness that might accompany pregnancy.     

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.     

Multiple sirehood in free-ranging twin rhesus macaques (Macaca mulatta)

Rhesus macaque females regularly copulate with a number of partners, and produce a single offspring per reproductive cycle in over 99% of cases. We used genotyping of 10 STR markers to determine paternity in the Cayo Santiago population of rhesus macaques. About 1,500 monkeys have been analyzed to date, with their marker genotypes entered into a computerized database. These data enable us to report the first documented case in any cercopithecine nonhuman primate species of the production of twin offspring sired by different males.     

A non-invasive technique for the control of intestinal parasites in rhesus macaques (Macaca mulatta).

Control of intestinal parasites is a major concern in maintaining the health and well-being of captive primates. This study established that percutaneous application of ivermectin was as effective as subcutaneous administration for the control of nematodes in captive rhesus macaques. The method is less intrusive than the standard subcutaneous or oral delivery routes and did not adversely affect the health of any of the study subjects.     

The human-ABO blood groups of free-ranging long-tailed macaques (Macaca fascicularis) and parapatric rhesus macaques (M. mulatta) in Thailand

BACKGROUND: Long-tailed and rhesus macaques are widely used in biomedical research; therefore, the known blood group is important. METHODS: The human-type ABO blood group was determined in wild or semi-wild long-tailed and rhesus macaques in Thailand. A total of 729 long-tailed and 160 rhesus macaques from 20 localities were temporarily caught. RESULTS: The frequency profiles of blood groups, calculated by averaging the frequency of each troop in long-tailed and rhesus macaques, were AB > O > B > A at 29.6%, 27.4%, 27.2%, and 15.8%, and B > AB > A > O at 39.6%, 33.4%, 18.2%, and 8.8%, respectively. Irrespective of locality, the frequencies were AB > O > B > A of 29.6%, 28.0%, 24.4%, and 18.0%, and AB > B > A > O of 37.5%, 28.7%, 26.9%, and 6.9%, respectively, for all long-tailed and rhesus macaques. The frequency profile of blood groups in Thai rhesus macaques was somewhat similar to that in the parapatric long-tailed macaques; however, it was different from other rhesus populations where only group B was detected. CONCLUSIONS: Our data support the hypothesis that Indochinese rhesus macaques are hybrids between rhesus and long-tailed macaques in the past.     

基于高通量测序的不同年龄恒河猴肠道菌群结构差异分析

目的观察不同年龄恒河猴肠道菌群结构和丰度的变化。方法 50只恒河猴,分为成年(5～10岁)、老年(10岁以上)2组,其中成年组33只,老年组17只。采集动物的新鲜直肠粪便,提取DNA后使用Illumina高通量测序平台对样本中细菌16S rDNA-V3区进行测序,定量分析肠道菌群的结构和丰度。结果老年组和成年组获得的优化序列数差异无显著性(P> 0.05)。α-多样性分析,老年组恒河猴肠道菌群的Chao1指数(P=0.0174)、Simpson指数(P=0.0258)、ACE指数(P=0.0121)与成年组比较降低,Shannon指数与成年组比较升高(P=0.0132)。老年组与成年组相比,在门水平,拟杆菌门(Bacteroidetes)相对丰度升高(P=0.0013),厚壁菌门(Firmicutes)、螺旋体门(Spirochaetes)、疣微菌门(Verrucomicrobia)、粘胶球形菌门(Lentisphaerae)相对丰度降低(P=0.0283,P=0.0002,P=0.0482,P=0.0242)。在科水平,Prevotellaceae相对丰度升高(P=0.0001),Ruminococcaceae、Clostridiales、Spirochaetaceae、Christensenellaceae相对丰度降低(P=0.0039,P=0.0080,P=0.0002,P=0.0021)。在属水平,老年组unidentified_Prevotellaceae相对丰度升高(P=0.0001),乳杆菌属(Lactobacillus)、八迭球菌(Sarcina)、unidentified_Spirochaetaceae相对丰度降低(P=0.0114,P=0.0227,P=0.0028)。β-多样性分析,老年组肠道菌群与成年组分布在不同区域,差异有显著性(P=0.003)。LEfSe分析,在成年组,链球菌属(Streptococcus)、布赫纳氏菌属(buchnera)、乳杆菌属(lactobacillus)是具有统计学意义的生物标记物。结论恒河猴肠道菌群的结构随年龄增长而改变。丰度降低,多样性增高。     

Consequences of group fission for the patterns of relatedness among rhesus macaques

When mammalian social groups exceed their optimal size, they often tend to split. In view of the potential evolutionary benefits, it should be more advantageous for animals to stay with kin, rather than nonkin, during such fission events. In the present study, the spontaneous fission of two social groups, R and S, of rhesus macaques living on Cayo Santiago, Puerto Rico, provided the opportunity to compare the kinship structure of the corresponding parent and daughter groups, using information on both maternal and paternal relatedness. In both instances, maternal half-siblings and pairs of animals from the same family were significantly more prevalent in the fission products than in the parent group. During the split of group R, significantly more paternal half-siblings stayed in the remnants of the parent group than joined the seceding group. Our findings are compatible with previous behavioural studies demonstrating that female primates bias their social behaviour more to maternal than to paternal kin, but that both types of half-siblings prefer each other more than unrelated animals. It remains to be clarified by future research, however, whether the observed co-segregation of paternal half-sibs in our study reflects active choice or is a by-product of the group-specific kin structures, prior to fission.     

Aspects of fight interference in free-ranging and compound-dwelling rhesus macaques (Macaca mulatta)

Patterns of fight interference (agonistic aiding) were compared among three groups of rhesus monkeys (Macaca mulatta) living in two settings: (1) two groups at Cayo Santiago (Caribbean Primate Center); and (2) one group at the Yerkes Regional Primate Research Center (YRPRC). A total of 1,227 interference episodes were recorded in 1,650 hours of observation. The only significant intergroup difference was the increased tendency of males at YRPRC to aid aggressors rather than victims. Among other findings, females aided relatives, interfered against target animals dominant to themselves, aided juveniles, and aided victims more consistently and frequently than did males. Importantly, female interference became more male-like in pattern when aid was given to nonrelatives. Neither the dominant males nor males in general displayed a unique or consistent tendency to interfere in fights in a manner which could be interpreted as controlling aggression. The males' interference patterns also did not suggest they were forming coalitions to either attain or defend status rankings. It is concluded that, overall, observations of compound-dwelling and free-ranging rhesus monkeys reveal similar relationships. Further, while female rhesus monkeys interfered in fights in a manner consistent with the control of aggression and protection of kin, the motives of male interferers remain unknown; however, their behavior is consistent with the hypothesis that they were reducing intermale tensions while, at the same time, minimizing physical risk.     

Costs and benefits of maternal aggression in lactating female rhesus macaques

Data from over 400 hr of observation of mother-infant rhesus macaques indicate that during the first 12 weeks of lactation infants are at risk from other group members and that mothers use aggression as well as restraining to protect them. Maternal aggression was negatively correlated with infant restraining. High-ranking mothers reacted aggressively to individuals handling their infants more than did middle- and low-ranking mothers. Conversely, middle- and low-ranking mothers restrained their infants more than did high-ranking mothers. Maternal aggression did not vary with infant age. Maternal aggression was directed toward a higher proportion of higher-ranking adult females and their immature offspring and was more likely to be followed by counter-aggression than nonmaternal aggression, i.e. aggression not related to interactions involving the infant. Middle-and low-ranking mothers suffered higher costs in terms of retaliation than high-ranking mothers. It is argued that the occurrence and distribution of maternal aggression among species and individuals should depend on the risk posed to infants by conspecifics as well as on the characteristics of the social structure (e.g. degree of asymmetry of agonistic contests) and of the mother (e.g. her dominance rank) which may affect the probability of retaliation.     

Estradiol increases somatomedin-C concentrations in adolescent rhesus macaques (Macaca mulatta)

Estradiol (E2) may enhance somatomedin-C (Sm-C) secretion during puberty in female rhesus monkeys. The present study evaluated the importance of age and acute changes in E2 on Sm-C secretion. Intact (INT) females at their first ovulation (age 3.5 yr; n = 6) had higher levels of Sm-C across the ovulatory cycle than did intact adults (ADT) (n = 5). Levels of Sm-C were similar for both groups during the follicular and luteal phases despite higher follicular phase levels of E2. Young, ovariectomized, E2-treated (E2OVX) females (age 3.5 yr; n = 5; E2 = 50 pg/ml) had higher basal levels of Sm-C than did either age-matched ovariectomized (OVX) females (n = 3), ovariectomized adults (OXA), or E2-treated ovariectomized adults (E2A) (E2 = 100 pg/ml). When ovariectomized groups were given E2 to induce ovulatory increases, no changes in serum Sm-C occurred. Comparisons among age-mates revealed that basal levels of Sm-C were similar between INT and E2OVX, yet these levels were higher than those for OVX. Sm-C levels were similar among all adult groups. Serum growth hormone (GH) was highest in E2OVX, next highest in INT and OVX, and lowest in all adults. Higher Sm-C levels in young animals are, thus, related to these age differences in GH concentrations and are further enhanced by basal levels of E2 and not by acute changes in this steroid. Low Sm-C secretion in adults is associated with low GH levels. Thus, the facilitory effect of basal E2 on Sm-C release is observed during conditions when basal GH levels are elevated, a situation normally limited to adolescence.     

Paternity assessment in rhesus macaques (Macaca mulatta): Multilocus DNA fingerprinting and PCR marker typing

Establishing kinship relations in primates using modern molecular genetic techniques has enhanced the ability to scrutinize a number of fundamental biological issues. We screened 51 human short tandem repeats (STRs) for cross-species PCR amplification in rhesus macaques (Macaca mulatta) and identified 11 polymorphic loci with heterozygosity rates of at least 0.6. These markers were used for paternity testing in three social groups (M, R, and S) of rhesus macaques from Cayo Santiago, Puerto Rico. Several consecutive birth cohorts were analyzed in which approximately 200 males were tested for paternity against more than 100 mother/infant pairs. Despite a combined exclusion rate of more than 99.9% in all three groups, some cases could not be solved unequivocally with the STR markers and additional testing of the MHC-associated DQB1 polymorphism. A final decision became possible through multilocus DNA fingerprinting with one or more of the oligonucleotide probes (GATA)₄, (CA)₈, and (CAC)₅. Paternity assessment by multilocus DNA analysis with probe (CAC)₅ alone was found to have limitations in rhesus macaques as regards the number of potential sires which might be involved in a given case. Multilocus DNA fingerprinting requires large amounts of DNA, and the ensuing autoradiographic patterns present difficulties in comparisons across gels and even within the same gel across remote lanes. Computer-assisted image analysis was incapable of eliminating this problem. Therefore, a dual approach to DNA typing has been adopted, using STR markers to reduce the number of potential sires to a level where all remaining candidates can be tested by multilocus DNA fingerprinting on a single gel, preferably in lanes adjacent to the mother/infant pair. Am. J. Primatol. 44:1–18, 1998. © 1998 Wiley-Liss, Inc.     

Voluntary progression order in captive rhesus macaques

The sequence in which 14 laboratory rhesus macaques left their home enclosure during a routine catching procedure was recorded on 30 occasions during 6 weeks. The animals were trained to voluntarily exit one by one and enter a transport cage for weighing and/or treatment. Mean weekly exit orders cross-correlated significantly, and individuals retained their exit positions with remarkable consistency throughout the study period. An animal's position did not depend on its sex, age, or dominance rank. The oldest female never failed to enter the transport cage as number 1. When she was prevented from taking the lead, the group was hesitant but eventually proceeded in the usual order. Food was a strong, yet not absolute, incentive for the monkeys to cooperate. If they could not expect a reward, they took more time before proceeding, but did so in the habitual order. The predictability of the exit sequence has practical managerial value because it makes it possible for a single person to quickly catch a selected group member when necessary.     

Social rank and cortisol among female rhesus macaques (Macaca mulatta)

In animal societies, some stressful events can lead to higher levels of physiological stress. Such stressors, like social rank, also predict an increased vulnerability to an array of diseases. However, the physiological relationship between social rank and stress varies between different species, as well as within groups of a single species. For example, dominant individuals are more socially stressed at times, while at other times it is the subordinate ones who experience this stress. Together, these variations make it difficult to assess disease vulnerability as connected to social interactions. In order to learn more about how physiological rank relationships vary between groups of a single species, cortisol measurements from hair samples were used to evaluate the effects of dominance rank on long-term stress levels in despotic and less stringent female rhesus macaque hierarchal groups. In despotic groups, cortisol levels were found not to be correlated with social rank, but a negative correlation was found between social rank and cortisol levels in less stringent hierarchies. Low ranking monkeys in less stringent groups secreted elevated levels of cortisol compared to higher ranking animals. These data suggest that variations in the strictness of the dominance hierarchy are determining factors in rank related stress physiology. The further consideration of nonhuman primate social system diversity and the linear degree of their hierarchies may allow for the development of valid rank-related stress models that will help increase our understanding and guide the development of new therapeutics for diseases related to human socioeconomic status.