Captivity Is Associated With Gut Mycobiome Composition in Tibetan Macaques (Macaca thibetana)

Although recent studies have revealed that gut fungi may play an important functional role in animal biology and health, little is known concerning the effects of anthropogenic pressures on the gut mycobiome. Here, we examined differences of the gut mycobiome in wild and captive populations of Tibetan macaques (Macaca thibetana) targeting the fungal internal transcribed spacer (ITS) and using next generation sequencing. Our findings demonstrate that the diversity, composition, and functional guild of the Tibetan macaque gut mycobiome differ across populations living in different habitats. We found that Tibetan macaques translocated from the wild into a captive setting for a period of 1 year, were characterized by a reduction in fungal diversity and an increase in the abundance of potential gut fungal pathogens compared to wild individuals. Furthermore, we found that the relative abundance of two main fungal guilds of plant pathogens and ectomycorrhizal fungi was significantly lower in captive individuals compared to those living in the wild. Our results highlight that, in addition to bacteria, gut fungi vary significantly among individuals living in captive and wild settings. However, given limited data on the functional role that fungi play in the host’s gut, as well as the degree to which a host’s mycobiome is seeded from fungi in the soil or ingested during the consumption of plant and animal foods, controlled studies are needed to better understand the role of the local environment in seeding the mycobiome.

Sex-Specific Variation of Social Play in Wild Immature Tibetan Macaques, Macaca thibetana

Theories proposed to explain social play have centered on its function in establishing social relationships critical for adulthood, its function in developing motor skills needed to survive, and promoting cognitive development and social learning. In this study, we compared variations in social play among infant and juvenile male and female Macaca thibetana. Given that this species is characterized by female philopatry and male dispersal, we hypothesized that immature females use social play as a mechanism to develop bonds that persist through adulthood whereas immature males use play to develop social skills needed to successfully enter new groups. The results indicated that social play steadily increased during the infant period and peaked at approximately 12 months of age. There were no significant differences in the frequency or types of social play exhibited between infant males and infant females. During the juvenile period, however, social play was found to decrease with age, with males engaging in social play more frequently than juvenile females. Moreover, whereas juvenile males engaged in more aggressive forms of play, juvenile females engaged in more affiliative forms of play. In addition, juvenile females engaged in higher rates of grooming than juvenile males. These results provide evidence of sex-specific differences and imply the functional variation of social play in Tibetan macaques, with immature males using social play to develop skills needed to enter and enhanced their dominance rank in a new social group and immature females using social play to develop long-term same-sex social bonds in their natal group.

Effects of Hierarchical Steepness on Grooming Patterns in Female Tibetan Macaques (Macaca thibetana)

Hierarchical steepness, defined as status asymmetries among conspecifics living in the same group, is not only used as a main characteristic of animal social relationships, but also represents the degree of discrepancy between supply and demand within the framework of biological market theory. During September and December 2011, we studied hierarchical steepness by comparing variation in grooming patterns in two groups of Tibetan macaques (Macaca thibetana), a primate species characterized by a linear dominance hierarchy. Using a focal sampling method, we collected behavioral data from two provisioned, free-ranging groups (YA1 and YA2) at Mt. Huangshan, China. We found that female dominance hierarchies were steeper in the YA1 group (0.81 based on the proportion of wins-losses and 0.66 based on dyadic dominance indices) than among members of the YA2 group (0.76 based on the proportion of wins-losses and 0.56 based on dyadic dominance indices). Females in the YA1 group groomed more frequently and for longer duration than females in YA2. Further analysis showed that grooming patterns of high- and low-ranking females did not differ between the two groups. However, middle-ranking females in YA1 groomed conspecifics more frequently and for longer duration than middle-ranking females in YA2. Our results suggest that the steepness of a dominance hierarchy plays an important role in the set of social strategies used by middle-ranking females to avoid a reduction in rank, as well as to increase their rank (the dilemma of middle class hypothesis). We suggest that future studies focus on individuals of middle-rank in order to better understand how the dynamics of rank stability and rank changes influence social relationships, and affiliative and competitive interactions in non-human primates.

Sexual Interference Behaviors in Male Adult and Subadult Tibetan Macaques (Macaca thibetana)

Male nonhuman primate sexual interference, which includes copulation interruption and copulation harassment, has been related to reproductive success, but its significance has been challenging to test. Copulation interruption results in the termination of a copulation before ejaculation, whereas copulation harassment does not. We conducted this study using the all-occurrence behavior sampling method on sexual interference behaviors of seven adult and four subadult male Tibetan macaques (Macaca thibetana) in mating and non-mating seasons at Mt. Huangshan, China, from August 2016 to May 2017. Our results showed that males’ individual proportion of copulation interruption and harassment was higher during the mating season than during the non-mating season. In addition, dominant males more often performed interruption, whereas subordinate males more often performed harassment. We found no difference in the individual proportion of copulation interruption or harassment between adult and subadult males. Adult and subadult males both directed copulation interruption and harassment more often toward the mating male than toward the mating female. Lastly, the post-ejaculation phase of copulation was shorter when copulation harassment occurred than when it did not. Our results suggest that sexual interference may be an important mating tactic that adult and subadult males use in male–male sexual competition.

Variation of Gut Microbiome in Free-Ranging Female Tibetan Macaques (Macaca thibetana) across Different Reproductive States

The gut microbiome is expected to adapt to the varying energetic and nutritional pressures in females of different reproductive states. Changes in the gut microbiome may lead to varying nutrient utilizing efficiency in pregnant and lactating female primates. In this study, we examined variation in the gut bacterial community composition of wild female Tibetan macaques (Macaca thibetana) across different reproductive states (cycling, pregnancy and lactation). Fecal samples (n = 25) were collected from ten adult females harvested across different reproductive states. Gut microbial community composition and potential functions were assessed using 16 S rRNA gene sequences. We found significant changes in gut bacterial taxonomic composition, structure and their potential functions in different reproductive states of our study species. In particular, the relative abundance of Proteobacteria increased significantly during pregnancy and lactation. In addition, the relative abundance of Succinivibrionaceae and Succinivibrio (Succinivibrionaceae) were overrepresented in pregnant females, whereas Bifidobacteriaceae and Bifidobacterium (Bifidobacteriaceae) were overrepresented in lactating females. Furthermore, the relative abundance of predicted functional genes of several metabolic pathways related to host’s energy and nutrition, such as metabolism of carbohydrates, cofactors and vitamins, glycans and other amino acids, were enriched in pregnancy and lactation. Our findings suggest that changes in the gut microbiome may play an important role in meeting the energetic needs of pregnant and lactating Tibetan macaques. Future studies of the “microbial reproductive ecology” of primates that incorporate food availability, reproductive seasonality, female reproductive physiology and gut inflammation are warranted.