Genetic consequences of group living in Mongolian gerbils

Social behavior can shape the local population genetic structure of mammals. Group living can increase pairwise genetic relatedness of mammals at a local level but differentiate the genetic structure at a population level through offspring philopatry and nonrandom mating. Our study aimed to test the hypothesis that social groups of Mongolian gerbils (Meriones unguiculatus) would consist of genetically related individuals due to offspring philopatry and would have distinct genetic structures because of restricted gene flow among social groups and nonrandom mating. We genotyped 327 wild gerbils, live captured from 28 social groups in Inner Mongolia, China, using nine microsatellite loci. The within-group pairwise genetic relatedness coefficient averaged 0.28 ± 0.14 (standard deviation), whereas the average pairwise genetic relatedness coefficient of the whole gerbil population was 0.0 ± 0.2. Additionally, the value of the global F statistic (F(st)) was 0.21, suggesting a substantial genetic differentiation among social groups of Mongolian gerbils. The Bayesian clustering divided the 327 gerbils into 23 distinct genetic clusters. Therefore, our results show that high within-group genetic relatedness and among-group genetic differentiation are the genetic consequences of group living in social mammals because of restricted gene flow, female philopatry, and nonrandom mating within social groups.     

Application of paternity discrimination by DNA polymorphism to the analysis of the social behavior of primates

Paternity in many primate species cannot be established reliably on behavioral grounds. For instance, Japanese macaques (Macaca fuscata) have a multi-male group structure and promiscuous mating patterns. On the other hand, accurate evaluation of male reproductive success is needed to analyze primate behavior. DNA finger-printing techniques were applied to 2 captive groups of Japanese macaques in the Primate Research Institute of Kyoto University for identification of paternity. Also, mating behavior of a captive group was observed in order to compare the reproductive success of each male with that expected on the basis of his observed mating activity. The number of offspring of full adult males was not related to their social rank although the number of copulations with ejaculation was highly correlated with their social rank. Monitoring of the female sexual cycles from the plasma profiles of gonadotropins and ovarian hormones suggested that males could not choose females at days of ovulation. The results of two-free-ranging wild troops, like those of the captive groups, indicated that high-ranking males could not monopolize the paternity of offspring. The results of paternity discrimination in Japanese macaques were compared with results from patas monkeys (Erythrocebus patas) in a discussion of social structure and male reproductive success. Some aspects of polymorphism detection techniques are also discussed.     

Fine-scale population genetic structure in a fission-fusion society

Nonrandom patterns of mating and dispersal create fine-scale genetic structure in natural populations — especially of social mammals — with important evolutionary and conservation genetic consequences. Such structure is well-characterized for typical mammalian societies; that is, societies where social group composition is stable, dispersal is male-biased, and males form permanent breeding associations in just one or a few social groups over the course of their lives. However, genetic structure is not well understood for social mammals that differ from this pattern, including elephants. In elephant societies, social groups fission and fuse, and males never form permanent breeding associations with female groups. Here, we combine 33 years of behavioural observations with genetic information for 545 African elephants ( Loxodonta africana ), to investigate how mating and dispersal behaviours structure genetic variation between social groups and across age classes. We found that, like most social mammals, female matrilocality in elephants creates co-ancestry within core social groups and significant genetic differentiation between groups (Φ_ST = 0.058). However, unlike typical social mammals, male elephants do not bias reproduction towards a limited subset of social groups, and instead breed randomly across the population. As a result, reproductively dominant males mediate gene flow between core groups, which creates cohorts of similar-aged paternal relatives across the population. Because poaching tends to eliminate the oldest elephants from populations, illegal hunting and poaching are likely to erode fine-scale genetic structure. We discuss our results and their evolutionary and conservation genetic implications in the context of other social mammals.     

人工投食行为对非人灵长类社会生态的影响

近年来,国内开展了对几种非人灵长类投食群的研究。借鉴日本猴(Macaca fuscata)、恒河猴(M.mulatta)和黑猩猩(Pan troglodytes)长期积累的研究经验,有利于我们减少人工投食对非人灵长类带来的不利影响,也有利于推动国内非人灵长类社会生态学的深入研究。本文通过比较这三种灵长类野生群和投食群之间的差异,量化地分析了人工投食对灵长类动物社会生态学方面的影响。结果表明在社会行为方面,人工投食会导致灵长类动物的聚集、增加争斗频率、改变个体间等级关系、延缓分群现象、影响活动域和增加新兴行为。在种群数量方面,人工投食会缩短雌性性成熟时间、增加出生率和婴猴存活率、减少成年猴死亡率。而人工投食对雄性性成熟、出生间隔等方面的影响仍需要进一步考证。最后我们讨论了人工投食行为的利弊,并建议应谨慎和妥善地实施人工投食,和对非人灵长类投食群进行合理的监管。     

Mating strategy and reproductive success of male patas monkeys (Erythrocebus patas)

Mating behavior and paternity of offspring of wild patas monkeys were studied at Kala Maloue National Park, Cameroon. Observation of patas groups over three years revealed that multi-male situations occurred after takeover of the position of a resident male. Direct observation of behavior showed that resident males (harem males) occupied only 31% of mating in multi-male situations and 100% in one-male situations. DNA-typing revealed that resident males sired two of four of infants in the one-male situation and four of five in the multi-male situation. Under the two years cycle of the one-male situation and the multi-male situation, calculation shows that resident males sired more offspring than sneakers both in observation and paternity testing. Sneak mating occurred during both one-male and multi-male situations, and resident males performed compensatory mating, with dilution of sneaker sperm; these activities explain the discrepancy found between observation of mating and results of paternity discrimination.     

Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates

Among primate species there is pronounced variation in the relationship between social status and measures of stress physiology. An informal meta-analysis was designed to investigate the basis of this diversity across different primate societies. Species were included only if a substantial amount of published information was available regarding both social behavior and rank-related differences in stress physiology. Four Old World and three New World species met these criteria, including societies varying from small-group, singular cooperative breeders (common marmoset and cotton top tamarin) to large-troop, multi-male, multi-female polygynous mating systems (rhesus, cynomolgus, talapoin, squirrel monkeys, and olive baboon). A questionnaire was formulated to obtain information necessary to characterize the stress milieu for individuals in particular primate societies. We standardized cortisol values within each species by calculating the ratio of basal cortisol concentrations of subordinates to those of dominants in stable dominance hierarchies and expressing the ratio as a percentage (relative cortisol levels). The meta-analysis identified two variables that significantly predicted relative cortisol levels: subordinates exhibited higher relative cortisol levels when they (1). were subjected to higher rates of stressors, and (2). experienced decreased opportunities for social (including close kin) support. These findings have important implications for understanding the different physiological consequences of dominant and subordinate social status across primate societies and how social rank may differ in its behavioral and physiological manifestations among primate societies.     

Demographic components of gene frequency change in free-ranging macaques on Cayo Santiago

Gene frequency profiles from January 1973 to January 1977 for three polymorphic loci were examined in Cayo Santiago rhesus social groups. The effects of demographic components (i.e., births, deaths, immigrations, emigrations, and group fission and fusion) on total change in gene frequencies are assessed. Allelic frequencies at the carbonic anhydrase II, 6-phosphogluconate dehydrogenase, and transferrin loci were analyzed in four social groups. In the two groups that underwent fission and fusion during the study period, the timing of these processes was related to the largest short-term changes in gene frequences. However, immigration and emigration had the greatest effect on total change in gene frequency in all groups during the study period. The relative importance of births and deaths in producing gene frequency change varied among the social groups. These results suggest that the relative importance of the demographic components of gene frequency change in primate populations is determined by behavioral patterns and ecological conditions specific to the population considered.     

The genetic structure of a primate species: Rhesus macaques and other Cercopithecine monkeys

Among rhesus macaques (Macaca mulatta)and other cercopithecine monkeys, social groups occupying adjacent home ranges (i.e., members of the same local population) exchange individuals and genes and thus exhibit marked genetic similarities. To assess the degree to which this pattern extends beyond the local population, the genetic structure of M. mulattaand six other primate species was determined using Nei’s (1973) gene-diversity analysis. The genetic similarities seen among social groups in the Dunga Gali population of M. mulatta (Melnick et al.,1984a) can be seen over the entire species range. Comparison of these results with the structures of other similarly organized primate species indicates that (1) the average social group contains most of its local population’s genetic diversity, (2) the average local population contains the majority of the genetic diversity found in the region to which it belongs, and (3) the proportion of species gene diversity found in the average regional population varies substantially between species. Genetic homogeneity within local and regional populations is probably the product of gene flow. The application of a number of analytical models of selection and gene flow strongly suggests that gene flow, genetic drift, and zoogeography offer a more parsimonious and plausible explanation for interspecific variation in regional differentiation than does stabilizing selection.     

Genetic population structure of the white sifaka (Propithecus verreauxi verreauxi) at Beza Mahafaly Special Reserve,southwest Madagascar (1992-2001)

Gene flow within and between social groups is contingent on behaviourally mediated patterns of mating and dispersal. To understand how these patterns affect the genetic structure of primate populations, long-term data are required. In this study, we analyse 10 years of demographic and genetic data from a wild lemur population (Propithecus verreauxi verreauxi) at Beza Mahafaly Special Reserve, southwest Madagascar. Our goal is to specify how patterns of mating and dispersal determine kinship and genetic diversity among animals in the population. Specifically, we use microsatellite, parentage, and census data to obtain estimates of genetic subdivision (FST), within group homozygosity (FIS), and relatedness (r) within and among social groups in the population. We analyse different classes of individuals (i.e. adults, offspring, males, females) separately in order to discern which classes most strongly influence aspects of population structure. Microsatellite data reveal that, across years, offspring are consistently more heterozygous than expected within social groups (FIS mean = -0.068) while adults show both positive and negative deviations from expected genotypic frequencies within groups (FIS mean = 0.003). Offspring cohorts are more genetically subdivided than adults (FST mean = 0.108 vs. 0.052) and adult females are more genetically subdivided than adult males (FST mean = 0.098 vs. 0.046). As the proportion of females in social groups increases, the proportion of offspring sired by resident males decreases. Offspring are characterized by a heterozygote excess as resident males (vs. nonresident males) sire the majority of offspring within groups. We link these genetic data to patterns of female philopatry, male dispersal, exogamy, and offspring sex-ratio. Overall, these data reveal how mating and dispersal tactics influence the genetic population structure in this species.     

非人灵长类动物种质冷冻保存研究进展和展望

非人灵长类动物是生物多样性的重要组成部分,也是生物医学研究的珍贵实验动物,然而,由于人类活动、栖息地破坏、狩猎和遗传隔离等原因,许多非人灵长类动物的野生种群数量急剧下降,甚至处于灭绝的边缘。种质冷冻保存对拯救非人灵长类动物和保存遗传物质资源具有重要意义。本文综述了新大陆猴、旧大陆猴和巨猿等类群动物精子、卵子、胚胎和性腺组织等种质冷冻保存的研究进展,介绍了狨猴、松鼠猴、恒河猴、食蟹猴和黑猩猩等种质冷冻保存的主要方法,并对未来种质冷冻保存的研究方向进行了讨论。     

Himalayan langurs: Temperate colobines

Four field studies of the langur monkey, Presbytis entellus, living in the Himalaya are compared, in order to uncover shared features of behavior and population structure that may be related to this habitat. Shared demographic characteristics include seasonality in mating and births, predominately multi-male troops at least during some times of the year, relatively large home ranges, low population densities with few intertroop encounters, and seasonal utilization of home ranges with distance maintenance between groups. Shared social characteristics include behavioral buffers against cold and inclement weather, fluctuation in male membership with greatest instability and lowest numbers during the mating season, a vocal repertoire marked by a unique vocalization of major importance in troop maintenance as well as alterations in the function of species-typical vocalizations, and variations in sexual behavior including variable expression of “typical” female headshake present, increased male initiation of sexual activity and a low incidence of female harrassment of sexual consorts. It is argued that while no single feature may be unique to Himalayan langur populations, the total cluster of features is, and can be related to climatic seasonality in the Himalayan temperate environment, the predominance of a multi-male group structure for some periods, and possibly genetic isolation.     

Social group fission and the origin of intergroup genetic differentiation among the rhesus monkeys of Cayo Santiago.

The serum transferrin locus is used to investigate the roles of the lineal effect of fission, male migration effect of fission, and genetic drift in causing intergroup genetic differentiation among the rhesus macaques of Cayo Santiago. These three mechanisms prove sufficient to explain the degrees of differentiation between the newly formed social groups A, K, and L as of July 1, 1971. The lineal effect of fission provides a baseline of intergroup differentiation which is altered by forces leading to intragroup genetic change, the male migration effect and genetic drift. The importance of population dynamics for the distribution of alleles among subgroups of a population is recognized.     

Socio-genetic structure and mating system of a wild boar population

Wild boars Sus scrofa have a social organization based on female groups that can include several generations of adults and offspring, and are thus likely matrilineal. However, little is known about the degree of relatedness between animals living in such groups or occupying the same core area of spatial activity. Also, polygynous male mating combined with matrilineal female groups can have strong influences on the genetic structure of populations. We used microsatellite genotyping combined with behavioral data to investigate the fine-scale population genetic structure and the mating system of wild boars in a multi-year study at Châteauvillain-Arc-en-Barrois (France). According to spatial genetic autocorrelation, females in spatial proximity were significantly inter-related. However, we found that numerous males contributed to the next generation, even within the same social group. Based on our genetic data and behavioral observations, wild boars in this population appear to have a low level of polygyny associated with matrilineal female groups, and infrequent multiple paternity. Mortality due to hunting may facilitate the breakup of what historically has been a more predominantly polygynous mating system, and likely accelerates the turnover of adults within the matrilineal groups.     

Paternity Recognition in Multi-male Primate Groups

A traditional view of multi-male primate groups has held thatmales provide relatively little direct care to infants, possiblyas a result of low confidence of paternity associated with arelatively promiscuous breeding system. In the last five yearsthis view has changed as a result of a careful documentationof intimate male-infant affiliations in certain species, especiallythe savanna-dwelling baboons (Papio spp.). The occurrence ofthese affiliations raises the question as to whether males carefor their own offspring preferentially and, if so, on what basismale confidence of paternity is mediated. Recent field studiesof baboons suggest that male-infant relationships are mediatedthrough affiliations between the males and the infants' mothers,but the degree to which these male-female affiliations are basedon prior mating experience (hence, paternity) has not been established. Comparative studies of male-infant relations in primates havegiven little attention to the variation in the intensity andform of male care patterns within the set of species that havea multi-male social organization. Among multi-male species,male care of young is reported most often in baboons and barbarymacaques (Macaca sylvanus) and least often in other macaques,chimpanzees (Pan troglodytes), and vervet monkeys (Cercopithecus).This interspecific variation may result both from differencesin the importance of male care to infant survival and from differencesin male confidence of paternity, which in turn may relate toseasonal breeding patterns and, in particular, to the presenceor absence of conspicuous signs of ovulation in females.     

A study of intragroup biological change induced by social group fission in Macaca mulatta using discrete cranial traits

Eight discrete cranial traits are used as biological indicators to investigate the effect of social group fission on intragroup genetic change leading to intergroup differentiation in Macaca mulatta. The timing of discrete cranial trait frequency change and group fission coincide, indicating a possible causal relationship between fission and genetic change. A significant change in the male mating population during and after fission is proposed as the mechanism causing intragroup genetic change, along with the effects of fluctuations in segregation ratios.     

白马雪山自然保护区滇金丝猴数量分布及种群结构的初步观察

滇金丝猴(Rhinopithecus bieti)属于世界珍稀灵长类动物,对它的研究报道仅限于分类地位(彭鸿绶等,1962;彭燕章等,1985;陈服官等,1981)、形态解剖(陈宜峰,1981;彭燕章等,1983;张耀平等,1983)、地理分布及生活习性(李致祥等,1981;木文伟等,1982)等。其分布、数量以及进化地位、生态学等方面的资料甚少。1985年笔者在白马雪山自然保护区对滇金丝猴的数量、分布及种群结构进行了观察。     

Detecting instability in animal social networks: genetic fragmentation is associated with social instability in rhesus macaques

The persistence of biological systems requires evolved mechanisms which promote stability. Cohesive primate social groups are one example of stable biological systems, which persist in spite of regular conflict. We suggest that genetic relatedness and its associated kinship structure are a potential source of stability in primate social groups as kinship structure is an important organizing principle in many animal societies. We investigated the effect of average genetic relatedness per matrilineal family on the stability of matrilineal grooming and agonistic interactions in 48 matrilines from seven captive groups of rhesus macaques. Matrilines with low average genetic relatedness show increased family-level instability such as: more sub-grouping in their matrilineal groom network, more frequent fighting with kin, and higher rates of wounding. Family-level instability in multiple matrilines within a group is further associated with group-level instability such as increased wounding. Stability appears to arise from the presence of clear matrilineal structure in the rhesus macaque group hierarchy, which is derived from cohesion among kin in their affiliative and agonistic interactions with each other. We conclude that genetic relatedness and kinship structure are an important source of group stability in animal societies, particularly when dominance and/or affilative interactions are typically governed by kinship.     

Genetic structure of three populations of rhesus macaques (Macaca mulatta): Implications for genetic management

One of the prime concerns at zoos and at primate breeding facilities is to maintain genetic variability. This can be accomplished by avoiding inbreeding. It is relatively easy to assess genetic variability and the level of inbreeding by using pedigree information and genetic markers. In this study we used genetic markers controlled by 6 independent polymorphic loci (GPI, PGD, CA2, MPI, DIA1, Tf) to ascertain genetic variation in two captive and one wild population of rhesus monkeys. Two other loci ADA and NP were also examined and found to be monomorphic in the three populations. F-statistics and contingency chi-square analyses indicated that there was significant genetic differentiation among the populations. We also found that the mean heterozygosities were very similar in the three populations, in spite of the diverse breeding strategies. These data are important because rhesus monkeys are frequently used for biomedical research; and the genetic markers provide useful information for genetic management of captive colonies of nonhuman primates. © 1992 Wiley-Liss, Inc.     

Loss of oestrus, concealed ovulation and paternity confusion in free-ranging Hanuman langurs.

Ovarian cycles in catarrhine primates are uniquely characterized by prolonged periods of sexual activity in which the timings of ovulation and copulation do not necessarily correspond. According to current hypotheses of primate social evolution, extended sexuality in multi-male groups might represent part of a female strategy to confuse paternity in order to reduce the risk of infanticide by males. We test this hypothesis by examining mating behaviour in relation to timing of ovulation and paternity outcome in a multi-male group of free-living Hanuman langurs. Using faecal progestogen measurements, we first document that female langurs have extended receptive periods in which the timing of ovulation is highly variable. Next, we demonstrate the capacity for paternity confusion by showing that ovulation is concealed from males and that copulations progressively decline throughout the receptive phase. Finally, we demonstrate multiple paternity, and show that despite a high degree of monopolization of receptive females by the dominant male, non-dominant males father a substantial proportion of offspring. We believe that this is the first direct evidence that extended periods of sexual activity in catarrhine primates may have evolved as a female strategy to confuse paternity.     

Behavioral responses of free-ranging rhesus monkeys to food shortage

During early July 1968, a severe food shortage occurred on Cayo Santiago, an island colony of free-ranging rhesus monkeys (Macaca mulatta). The food shortage produced striking changes in the behavior of the monkeys. Within the one social group intensively studied, the total frequencies of grooming, play and fights decreased significantly; the frequency of matings also dropped; body contact, displacements by other groups, and non-displacement movements decreased, but not in statistically significant amounts. Changes in the percentage of total grooming attributable to related and unrelated monkeys reflected the stability of the rhesus matriline. Comparisons made between Cayo Santiago and other primate groups under analogous situations reveal similar responses to food shortage.