Female preferences for male golden snub-nosed monkeys vary with male age and social context

Age is a key factor affecting sexual selection, as many physical and social traits are age-related. Although studies of primate mate choice often consider particular age-related traits, few consider the collective effects of male age. We tested the hypothesis that female golden snub-nosed monkeys Rhinopithecus roxellana prefer prime aged males (10–15 years) over younger and older males. We examined a habituated, provisioned troop during a 3-year study in the Qinling Mountains, China. Prime age males were more likely to be resident males of 1-male units (OMUs) than males of other ages. Since females are free to transfer between OMUs, the number of females per OMU can be indicative of female preferences. We examined the number of females per OMU, and found that it increased with resident male age up to 7–8 years, and declined after 12 years, such that prime age resident males had more females than other resident males. Females also initiated extra-unit copulations with high-ranking prime age males at significantly higher rates than with other males. Nevertheless, females tended to transfer from OMUs with high-ranking, older resident males to those with low-ranking, younger resident males. Thus, females appear to use different strategies when choosing social mates and extra-unit mates (i.e., different social contexts). We speculate that females may perceive early signs of aging in males and trade off the benefits and costs of high rank versus male senescence. This study lays the groundwork for future studies that examine possible direct and indirect benefits of such strategies.     

Impact of male takeover on intra-unit sexual interactions and subsequent interbirth interval in wild Rhinopithecus roxellana

Data were collected on sexual interactions before and after a male takeover of a one-male unit (OMU) of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains, China. The original unit consisted of an adult male, 2 adult and 2 subadult females, 2 female juveniles and a single infant. Following the takeover, the new resident male copulated with 1 adult female, which was not lactating. Subsequent to the disappearance of her infant, the second (lactating female) entered breeding condition and began to solicit copulation with the new resident male. The subadult females also engaged in matings with the new male. The new resident male was observed mating, on 3 occasions, with females in 2 other OMUs. These are the first observations of sexual behaviour in free-ranging Sichuan snub-nosed monkeys after an OMU takeover. Sexual interactions play an important role in establishing relationships between the new male and resident females in the OMU.     

Social dynamics of the golden snub‐nosed monkey (Rhinopithecus roxellana): female transfer and one‐male unit succession

Among primates that form multilevel societies, understanding factors and mechanisms associated with the movement of individuals between groups, clans, and one‐male social units offers important insight into primate reproductive and social strategies. In this research we present data based on an 8‐year field study of a multilevel troop of Sichuan snub‐nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains of China. Our study troop contained 78–126 individuals, and was usually organized into 6–8 one‐male units (OMU). The majority of OMUs were composed of networks of unrelated females and their offspring. We found that 59.7% (43/72) of subadult and adult females in our study troop transferred between OMUs (n=66) or disappeared (n=7) from the troop. In the majority of cases, two or more females transferred together into new OMUs or troops. In R. roxellana, new OMUs formed in several ways. During 2001–2008, 16 adult males appeared in the study troop. Over this period, we observed 13 different males who became harem leaders either by taking over an existing harem or by attracting females from other OMUs into their harem. We also observed four OMUs from a neighboring troop to successfully immigrate into the study troop. The number of individuals in these newly immigrated OMUs was significantly smaller than that number of individuals in resident OMUs. During harem formation, fighting between adult males was rarely observed, and female mate choice appeared to play a crucial role in harem male recruitment and replacement. These results suggest that golden snub‐nosed monkeys are organized in a nonmatrilineal social system. Female mate choice and possibly incest avoidance appear to play important roles in female transfer, male tenure, and OMU stability. Am. J. Primatol. 71:670–679, 2009. © 2009 Wiley‐Liss, Inc.     

The role of kinship in the formation of a primate multilevel society

A small number of mammalian species live in a modular or multilevel society in which several individual social/reproductive units called one-male units (OMUs) are embedded within a large cohesive band. Factors that affect band composition and stability are poorly understood. In this study we examined the role of kinship in the formation and maintenance of a multilevel society in an endangered population of golden snub-nosed monkeys (Rhinopithecus roxellana). From 2005 to 2011, we obtained genetic samples from 86 individuals (including 88.9% of leader males and 80.5% of adult females) living in a band of 8–10 OMUs. We used microsatellite genotyping to identify patterns of relatedness and individual transfer. We found that adult females residing in the same OMU were more closely related to each other than to a random set of females drawn from the band and that females tended to disperse into OMUs that contained female relatives. In addition, adult females who transferred were not more closely related to their previous leader male than to the leader male of their new OMU. These results support the contention that kin bonds contribute importantly to the formation and stability of this primate multilevel society by influencing a female's decision to remain in her current OMU, or during transfer, which new OMU to enter. Am J Phys Anthropol 156:606–613, 2015. © 2014 Wiley Periodicals, Inc.     

Alternative routes to the leader male role in a multi-level society: follower vs. solitary male strategies and outcomes in hamadryas baboons

The nested one-male units (OMUs) of the hamadryas baboon are part of a complex social system in which "leader" males achieve near exclusive mating access by forcibly herding females into permanent consortships. Within this multi-level social system (troops, bands, clans and OMUs) are two types of prereproductive males--the follower and solitary male--whose different trajectories converge on the leader role. Here we compare OMU formation strategies of followers, who associate with a particular OMU and may have social access to females, with those of solitary males, who move freely within the band and do not associate regularly with OMUs. Data were derived from 42 OMU formations (16 by followers and 26 by solitary males) occurring over 8 years in a hamadryas baboon band at the Filoha site in Ethiopia. "Initial units" (IUs) with sexually immature females (IU strategy) were formed by 44% of followers and 46% of solitary males. The remaining followers took over mature females when their leader was deposed (challenge strategy) or disappeared (opportunistic strategy), or via a seemingly peaceful transfer (inheritance strategy). Solitary males took over mature females from other clans and bands, but mainly from old, injured or vanished leaders within their clan (via both the challenge and opportunistic strategies). Former followers of an OMU were more successful at taking over females from those OMUs than any other category of male. Despite this advantage enjoyed by ex-follower leaders, ex-solitary leaders were equally capable of increasing their OMU size at a comparable rate in their first 2 years as a leader. These results demonstrate the potential for males to employ both multiple roles (follower vs. solitary male) and multiple routes (IU, inheritance, challenge, opportunistic) to acquire females and become a leader male in a mating system characterized by female defense polygyny in a competitive arena.     

A study on the social structure and dispersal patterns of hamadryas baboons living in a commensal group at Taif,Saudi Arabia

Three levels of hamadryas social structure—the one male unit (OMU), the band, and the troop—have been observed at all sites studied, but a fourth—the clan—has been observed at only one site, Erer-Gota, Ethiopia, during a longitudinal check of the dispersion of identified individuals. The clan is important since it appears to provide the basis for male philopatry, although comparative data is needed from other sites to confirm this. We studied a huge commensal group of hamadryas baboons (over 600 animals) in Saudi Arabia. We put ear tags on baboons between 1998 and 2004 and analyzed social structure, relying on the interactions of these tagged animals by focusing especially on their dispersal patterns from OMUs. OMU membership tended to be looser than that of the Ethiopian hamadryas. Females tended to shift between OMUs on an individual basis in our study group, whereas the collapse of an OMU was a major occasion of adult female transfer in Ethiopia. We found neither stable bands (a “band” in our study group was defined as a regional assemblage of OMUs) nor clans that lasted for several years. Some OMUs moved and transferred into neighboring areas over both the short and long term. Further, some post-adolescent males appeared to move out of the study area. The ratio of adult females in an OMU in our study group was larger than for any other documented study site, and this may be the reason for enhanced female transfer between OMUs. A large proportion of the adolescent females showed no clear membership to OMUs, and no “initial units” (commonly observed in Ethiopia) were discernible. The ease with which young males acquired adult females at the study site must have disrupted the formation of a clan, a “male-bonded society.”     

Early sexual maturity in male hamadryas baboons (Papio hamadryas hamadryas) and its reproductive implications

We present data on sexual maturity in young hamadryas baboon males (Papio hamadryas hamadryas) and its reproductive consequences in a large captive baboon colony. Hamadryas baboons live in a multilevel social system, with one-male units (OMUs) as the smallest social entity. Male leaders of OMUs are believed to monopolize matings within their OMUs; hence mating is believed to be polygynous and monandrous. In a captive colony of hamadryas baboons, we found evidence that young males less than 4 years old fathered at least 2.5% of 121 offspring born subsequent to vasectomy of all adult males, and males aged 4-5 years fathered at least 16.5% of the offspring. Additional evidence that these young males are able to sire offspring came from a morphological comparison of sperm from hamadryas males of different ages. The sperm of a 48-month-old hamadryas baboon were morphologically indistinguishable from viable sperm from adult males, whereas sperm from a 45-month-old male showed some aberrations. If successful copulations by adolescent males constitute a regular pattern even in free-ranging hamadryas baboons, a hamadryas male's chances to reproduce would not be limited to his role as an OMU leader as previously assumed, and a male's reproductive career would consist of two phases: the adolescent phase, and the OMU leader male phase.     

Female social dynamics in a provisioned free-ranging band of the Sichuan snub-nosed monkey (Rhinopithecus roxellana) in the Qinling Mountains, China

Little information is available on the social dynamics of the Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Here, we provide 5-year observational data on a provisioned free-ranging band in the Qinling Mountains, central China, from October 2001 to December 2005. The results of this study suggested that females place a high priority on maintaining long-term relationships with other female in their one-male units (OMUs). Females had more social interactions with unit members than with nonunit individuals. They showed relatively high rates of affiliation with their unit females, intermediate levels with the resident males, and low levels with individuals outside the unit. Females had few interactions with other resident males. Social interactions, especially affiliative interactions, were more symmetrical between focal females and their unit females than between focal females and the resident males. Thus female social interactions appeared to resemble those of other female-bonded primate societies. On the other hand, female transfers occurred sometimes. We recorded 11 cases of female immigration and 5 cases of female disappearance, 1 case of female intraband shift, and 2 cases of "merging of OMUs," which suggested that unit females might be loose-knit in this species. We discussed influencing factors on female Sichuan snub-nosed monkey social dynamics, by comparing them with those of Hamadryas and gelada baboons that also have multilevel societies.     

Dominance relationships among one-male units in a provisioned free-ranging band of the Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains, China

We studied the dominance relationships among one-male units (OMUs) in a provisioned free-ranging band of the Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains of central China from 2001 to 2005. The band was composed of 6-8 OMUs that stayed in the band for several years. Linear dominance orders could be detected using displacement interactions with directional asymmetry among OMUs in 82.3+/-5% of interactions, and ambiguous and reversed interactions in 17.7+/-5%. The dominance rank of OMUs was positively related with the duration of their stay in the band, and this may be attributed to the association of the resident male with adult females, rather than the fighting ability of resident males, as males do not fight seriously with each other. Subordinate units were observed to merge with dominant units resulting in an elevation of their rank order. The linear dominance relationship among OMUs in the Sichuan snub-nosed monkeys may have evolved as a result of competition for preferred food trees.     

Social System of a Hybrid Baboon Group (Papio anubis × P. hamadryas)

We describe the social organization, mating system, and social structure of a group of hybrid baboons (Papio anubis×P. hamadryas) in Ethiopia's Awash National Park. The group contained elements of both hamadryas and anubis societies. Overall, the group was a multimale, multifemale group that lacked cohesion and frequently formed subgroups. Subgroup formation was more strongly associated with predation risk than food availability. Although there were several hamadryas-like one-male units OMUs within the group, there was no evidence of a hamadryas multilevel society. Male and female members of OMUs were phenotypically more hamadryas-like than non-OMU individuals. The group contained substantial variation in the strength of inter- and intrasexual bonds: some females primarily groomed males while other females primarily groomed females, and the patterns were consistent with the OMU substructure. Despite some promiscuous mating, mating was biased towards the hamadryas condition for all group members. Additionally, rates of immigration and emigration were very low, and mean pairwise relatedness within the group is rising. For measures of intersexual bonding, all members of the group were intermediate between anubis and hamadryas individuals in less hybridized groups. The group was phenotypically and behaviorally more intermediate than it was in the 1970s (Sugawara, K. (1988). Primates 29: 429–448.) and the changes may indicate a relatively young and dynamic hybrid zone.     

人工辅助投食滇金丝猴一雄多雌单元之间的等级序列

群居灵长类动物等级序列是长期进化的结果,也是动物行为生态学研究的热点。灵长类动物个体间通过等级序列,合理的利用自然资源、避免过多的伤亡、保护群体内的幼弱者,从而更好地适应复杂的生态环境。2013年6月至2014年1月,采用焦点动物取样法对白马雪山国家级自然保护区人工辅助投食滇金丝猴群的6个一雄多雌单位之间等级序列进行了研究。通过对一雄多雌单元之间攻击-屈服行为数据分析发现：一雄多雌单位之间存在明显的等级序列（大个子单元＞单疤单元＞红脸单元＞联合国单元＞偏冠单元＞花唇单元）;单元之间成年雄性的攻击行为多于成年雌性;单位之间的等级序列与取食次数、第一序位取食总次数呈显著正相关,与各单元取食总时间无明显相关性;同时,一雄多雌单元之间的等级序列与单元内成年雌性数量呈显著正相关。研究结果符合群居灵长类动物攻击-屈服假说和资源优先占据-雌性高序列偏好假说。     

雄性川金丝猴对雌性的受孕认知与等级识别

社会认知是群居动物适应复杂环境和社会生活能力的体现,致力于理解自身、他人与社会。认知有利于促进利益分配的优化,而行为认知策略则是关注的热点问题。但迄今为止,川金丝猴如何进行社会地位与受孕状态等基础认知尚不清楚。本研究通过投食招引,在个体识别和等级判定的基础上,以栖息于秦岭观音山自然保护区熊猫谷景区的一个半野生川金丝猴群为对象,采用瞬时扫描和焦点动物取样法,观察并收集了猴群中6个一雄多雌单元成年雌雄个体的空间位置、邀配、交配及产仔行为数据,结合食物密度梯度"同心圆"和受孕周期,推测雌性成功受孕的交配时间段,运用配对t-检验统计证实受孕前后雌性的交配实现率差异显著(t=4.527,P=0.001),表现为受孕前雌性邀配行为获取的雄性响应率明显高于受孕后;通过Spearman相关性检验发现,雌性受孕前的交配实现率(R=0.527,P=0.006)及受孕时间(R=0.556,P=0.049)与自身等级均显著正相关,即高等级雌性邀配行为的雄性响应率及与雄性生殖性交配的时间明显高于或早于低等级雌性。结果表明,雄性川金丝猴拥有认知单元内成年雌性受孕状况和等级地位的能力,这种认知能力影响着雄性的性行为方式。     

Copulation patterns in captive hamadryas baboons: a quantitative analysis

For primates, as for many other vertebrates, copulation which results in ejaculation is a prerequisite for reproduction. The probability of ejaculation is affected by various physiological and social factors, for example reproductive state of male and female and operational sex-ratio. In this paper, we present quantitative and qualitative data on patterns of sexual behaviour in a captive group of hamadryas baboons (Papio hamadryas), a species with a polygynous–monandric mating system. We observed more than 700 copulations and analysed factors that can affect the probability of ejaculation. Multilevel logistic regression analysis and Akaike’s information criterion (AIC) model selection procedures revealed that the probability of successful copulation increased as the size of female sexual swellings increased, indicating increased probability of ovulation, and as the number of females per one-male unit (OMU) decreased. In contrast, occurrence of female copulation calls, sex of the copulation initiator, and previous male aggression toward females did not affect the probability of ejaculation. Synchrony of oestrus cycles also had no effect (most likely because the sample size was too small). We also observed 29 extra-group copulations by two non-adult males. Our results indicate that male hamadryas baboons copulated more successfully around the time of ovulation and that males in large OMUs with many females may be confronted by time or energy-allocation problems.     

Territoriality and Male Mating Success in the Dart-poison Frog,Epipedobates femoralis (Dendrobatidae,Anura)

The social and reproductive behaviour of the dart-poison frog, Epipedobates femoralis, was studied in Amazonian Peru for 14 months. Males defended territories with advertisement calls and, ultimately, fighting. Territory size ranged from 0.25 to 26 m² and was positively correlated with duration of residence and calling activity of the owner. Females were not territorial and were never attacked when approaching calling males. Males and females only mated once and females sampled calling males before mating. Male mating success was closely correlated with territory size and calling activity. No correlation was found between male body size and mating success. Territories provide residents with sufficient space for mate attraction and reproduction without interference from rivals. Since territory size is dependent on calling activity which involves high energetic costs, it is suggested that territory size reveals male quality.     

白马雪山自然保护区响古箐滇金丝猴（Rhinopithecus bieti）的交配行为

灵长类交配模式是灵长类社群结构和婚配制度的重要表征之一,其研究有助于了解灵长类社群结构和两性交配策略。2013年11月至2014年10月,我们对云南白马雪山国家级自然保护区一人工辅助投食滇金丝猴群进行了观察研究,采用焦点动物取样法和全事件记录法收集了雌雄个体的交配相关的行为数据,主要包括邀配对象、交配过程、持续时间和回合数,以及参与交配的雌雄对在交配结束后的相互理毛的持续时间和回合数。研究结果表明：研究群滇金丝猴全年均有交配行为,交配高峰期在7-9月,两性参与交配的积极性和对季节变化的响应不同;交配主要由雌性通过邀配发动（76%）,交配高峰期也是雌性邀配的高峰期;雄性爬跨频次（年均0.43次/月,n=5）和射精爬跨比（年均19%,n=5）则在全年无显著变化。交配行为发生的典型表现为：雌性通过小跑或跳跃进入雄性视线范围内,爬伏呈臀向雄性邀配;雌猴爬伏时离雄猴的远近距离不同（<1m vs. 2-5m ： 69% vs. 31%）会影响其邀配成功率（<1 m vs. 2-5 m ：68% vs. 40%）;若一次邀配失败,雌猴可能会连续爬伏邀配（最多4次）,连续多次邀配的成功率显著高于单次邀配（79% vs. 52%）。交配结束后雌性会主动为雄性理毛,但雌性主动理毛与交配是否射精无关。     

Can females gain extra paternal investment by mating with multiple males? A game theoretic approach

Although females may require only one mating to become inseminated, many female animals engage in costly mating with multiple males. One potential benefit of polyandrous mating is gaining parental investment from multiple males. We developed two game theoretic models to explore this possibility. Our first model showed that male care of multiple females' offspring evolves when male help substantially increases offspring fitness, future mating opportunity is limited, and group size is small. In our second model, we assumed that males invest in the offspring of former mates and evaluated the fitness consequences of female monogamous and polyandrous mating strategies. Females benefit only from limited polyandry, that is, mating with several males. Polyandry is discouraged because females must share male investment with other polyandrous females, and paternal care is likely to experience diminishing returns. Females may enhance their access to male investment by competing with rival females and monopolizing investment, however. The results support the argument that females can gain paternal investment by mating with several males in small social groups (e.g., dunnocks Prunella modularis). The results do not support the argument that females can gain paternal investment from pronounced multiple mating in large social groups, however, as observed in many primate species.     

Anogenital distance as a measure of male competitive ability in Rwenzori Angolan colobus

Anogenital distance (AGD) is positively correlated to fetal androgen exposure and developmental masculinization in mammals. Independent of overall body size, AGD shows a strong positive correlation with male fertility and in rodents, AGD is a good indicator of male competitive ability and is associated with female choice. We hypothesized that AGD will also predict male competitive ability in non-human primates. To test this, we measured AGD noninvasively with a parallel laser in a wild population of Angolan colobus monkeys (Colobus angolensis ruwenzorii) in Uganda and correlated to it to their social structure. C. angolensis ruwenzorii form a multilevel society with both one-male/multifemale units (OMUs) and multimale/multifemale units (MMUs). We compared AGD in males from five OMUs and six MMUs and related it to their fecal androgen metabolite concentrations, dominance rank and body size, and to the number of females in their unit. Males in OMUs had greater access to females, so were predicted to have longer AGDs, but this was not found. AGD also did not correlate overall with mean fecal androgen metabolites in MMUs. However, AGD was correlated with dominance rank in MMUs, demonstrating that higher-ranking males in these multimale units had longer AGDs. Body size did not show the same relationship with dominance rank, suggesting that male rank was not just a reflection of absolute male size. Our findings indicate that AGD predicts male competitive ability in this species and that it may be a useful correlate throughout the non-human primates. These results also support the idea that prenatal androgen exposure increases the likelihood of the expression of behaviors that maintain high dominance rank.     

Male Mating Tactics in Captive Rhesus Macaques (Macaca mulatta): The Influence of Dominance, Markets, and Relationship Quality

Male mating success in a multimale–multifemale group can depend on several variables: body condition, dominance, coalitions, “friendship,” or an exchange of services for mating access. Exchange patterns may also be determined by market effects or social relationships. We studied the mating tactics of males in a captive, multimale–multifemale group of rhesus macaques and the resulting patterns of mating and paternity to determine the influence of dominance rank, mating markets, and relationship quality on their mating tactics. Male rank was positively related to the total number of copulations and the number of mating partners, but did not explain male mating distribution completely. Moreover, male fertilization success was not related to male rank. Males did not exchange grooming for mating access on the same day and neither the supply nor the rank (as a proxy for quality) of receptive females affected the amount of male grooming, suggesting that market effects did not explain male mating access. However, there was a positive correlation between long-term grooming patterns of both males and females and mating access, indicating that social relationships were important for male mating access. Paternity data revealed that these social relationships were also important for male reproductive success. We conclude that both male rank and male–female “friendship” determined male mating access in these rhesus macaques, but that “friendship” was more important in determining paternity, emphasizing the importance of intersex social bonds in male mating success in multimale primate societies.     

Social organization of the spotted hyaena Crocuta crocuta. II. Dominance and reproduction

A 4-year study of the social organization of spotted hyaenas in a clan of 60–80 individuals showed that there is a separate dominance hierarchy within each sex. One female and her descendants dominated all others; matrilineal rankings were stable over time because maternal rank is inherited. Cubs of higher ranking females were able to feed at kills in competition with adults more successfully than other cubs, and male offspring of the alpha female were the only males able to dominate adult females. The mating system is highly polygynous: only the behaviourally dominant male was seen to mate, though all other resident males regularly courted females. Among females, there was no correlation between reproductive success and age, size, or social rank. It is postulated that the unusually aggressive sons of the alpha female would probably be highly successful competitors in the context of a polygynous mating system. A primary consequence of female dominance over males is that females and their young have priority of access to food in a highly competitive feeding situation. This competition may have been the selective force that produced female dominance and the associated syndrome of female virilization that is characteristic of the species. Cooperation among related females may be the basis for the matrilineal system, as has been suggested for certain primate species.     

Dominance is not always an honest signal of male quality,but females may be able to detect the dishonesty

Females prefer dominant males as mating partners in numerous species. Male dominance rank is considered as an honest signal of male quality, because only healthy males in good condition are thought to be able to win fights with other males. Here, we tested whether activation of the immune system influences the success of males in male–male competition and mating in the field cricket, Gryllus integer. We activated the immune system of males with a nylon monofilament (to mimic a parasitoid larva), and arranged fights between male pairs to assess male dominance and associated mating success. Activation of the immune system with nylon monofilament substantially enhanced the fighting success of males during male–male competition but had no effect on mating success. However, sham-manipulation (a wound only) did not have any effect on fighting success although females mated more often with dominant males. Our study suggests that when male crickets meet an apparent survival threat they may behave more dominantly, probably owing to terminal investment. Male success during male–male competition is not always an honest signal of males’ quality, but females may be able to detect this dishonesty.