Gut Microbial Structure And Adaptive Evolution In Wild Tibetan Macaque’s (Macaca Thibetana) Social Group

The mammals gut are colonized by trillions of microorganisms, most of which have co-evolved with the host in a symbiotic relationship.The gut microbiota can provide crucial services to host nutrition, metabolic activity, immune homeostasis and behavioral patterns. When the microbiota is dysbiosis, these services may be disrupted, leading to disorders including obesity, diabetes, and inflammation and behavior disorder. Consequently, understanding the relationships between host and gut microbial communities have emerged as a major topic of research interest in biology.A major effort is underway to understand the factors that can influence the distribution of microbial taxa within and among individuals. On to generally, Individuals acquire gut microbes from their mother, relatives, mates or close community members and food sources during lifespan. Numerous internal and external factors can influence the gut microbial communities, such as host genotype, diet, geography, temperature and social interactions. Despite the existence of numerous studies of the impact of the gut microbiota on human health and disease, much work remains to be done to improve our understanding of the host-microbe relationship in wild mammals, particularly in social level.In this regard, the free-ranging social group of Tibetan macaque (Macaca thibetana) followed about 30 years for behavior research will be ideal to study this question. In this study, we took Tibetan macaque social group as a subject, using the high-throughput sequencing methods to study the gut microbiome of these macaques at group level. The following four questions will be answered: (1) what about the microbiome community composition in Tibetan macaque’s gut? (2) If the community structure (age, sex and kinship) can influence the gut microbiome community composition and structure of wild Tibetan macaque? (3) How the gut microbime influenced by social living? (4) How this macaque’s gut microbes respond to the dynamic changes of the food resources? The main research results are as follows:(1) At phylum level, the Tibetan macaque gut microbiota is largely dominated by Firmicutes and Bacteriodetes. The presence of greater relative abundance of well-known fiber-degrading phylum Firmicutes and Bacteroidetes in this species gut, suggesting a characteristic features that are consistent with a heavily plant-based diet in other primates. The most represented families in Tibetan macaques are Ruminococcaceae, Prevotellaceae and Succinivibrionaceae, which also found in the mammalian gut environment as the most abundant families, and have been associated with degradation of complex plant material. Such an adaptation would be beneficial for Tibetan macaques to eat food (such as leaves, grass and roots) containing high levels of structural polysaccharides. At the genus level, predominant genera of bacteria isolated from the feces were Prevotella and Succinivibrio. Species belonging to Succinivibrio enrich rumen microbial ecosystems and are efficient in fermenting glucose through the production of acetic and succinic acids, as well as in aiding in the metabolization of different types of fatty acids. Species in the genus Prevotella are associated with digestion of hemicellulose, pectin, carbohydrate and simple sugars, such as those found in fruits, cereals and young leaves.(2) At group level, the Tibetan macaque gut microbial composition and structure have no significant difference between the sexes.At the phylum level, did not detect no significant difference were detected between different gender. At genus level, there have a few genus were detected in significant different between the sexes, and the relative abundance is low. In addition, the gut microbiome diversity (Alpha and Beta diversity) of Tibetan macaques between sexes has no significant differentiation. In this macaque group, there have no significant difference between immature and adult in two phylum Firmicutes and Bacteroidetes, this result is different with previous studies. In addition, there also have no significant difference between different age classes. Further more, we haven’t found the age-related gut microbiome community structure differentiation in Tibetan macaque social group. This result revealed that the gut mcirbiome community structure of our study group may exist some other influence factors except for digestive physiology in Tibetan macaque social group. In primate and other mammal’s studies, the phylogenetic concordance between gut communities and host species suggested that the degree of genetic relatedness between individuals would dictate the level of similarity in the compositions of their gut microbial communities by vertical transmission. However, at the group level, there were no significant differences on alpha and beta diversity between the microbial communities of Tibetan macaques and differing relatedness levels, consistent with the results found in Gombe chimpanzees.(3) Previous studies of the human microbiome found that there are significant differences in alpha and beta diversity between the oral and gut habitats. Our results of free-ranging Tibetan macaques are similar to studies of humans in that they show that both the microbial community’s Alpha and Beta diversities are significantly divergent between the oral and gut habitats. In our comparison among individual monkeys, we found significantly higher similarity within oral samples compared to stool samples which indicates possible inter-individual transfer of microbiota and/or similarities in environmental exposure to microbes. The Prevotella as the abundant genus shared by stool and saliva communities has been reported in human studies and it has been suggested oral bacterial populations seed the gut. In our study, a distinctive result is both the stool and oral community’s shared three core-abundance genera including Prevotella, Treponema and Alloprevotella. Our data suggested that these three genera can be transferred between monkeys via an oral route and continuous seed the gut’s co-abundance genera to the gut habitat via their host’s ingestion of microbes. In addition, the gut and oral shared 413 OTUs. Particularly, most partthe majority (89%) of the gut co-abundance genera can be detected in from the oral cavity samples, which provide new evidence to for understanding the fecal-oral transmission in social living primates.(4) In this study, we demonstrate that both the Tibetan macaque gut microbial community composition and diversity (alpha and beta diversity) are varying strongly with seasons. A comparison of the winter and spring results show that the most abundant microbiome genus, Succinivibrio, significantly increased in winter samples. Species belonging to Succinivibrio enrich rumen microbial ecosystems and are efficient in fermenting glucose through the production of acetic and succinic acids as well as in aiding in the metabolization of different types of fatty acids, which may increase energy utilization efficiency for monkeys during winter. The significant increase of Clostridium sensu stricto detected in the Tibetan macaque gut microbiome in winter suggests its potential utility for digesting cellulose and dietary fiber. In spring, the abundance of the genus Prevotella significantly increased. During this time, our study monkeys increase their ingestion of young leaves, which are richer in more easily digestible energy and protein than mature leaves, roots and other vegetative parts. Our PICRUSt analysis also revealed that predicted genes from the metagenome related to glycan biosynthesis and metabolic pathways are significantly increased in winter samples. The predicted genes from the metagenome related to the Carbohydrate Metabolism and Energy Metabolism pathways were also significantly increased in our spring samples. These results indicate that the changes measured in the gut microbial community in spring may be beneficial for a rapid recovery from acute energy and nutrition loss experienced during the cold winter months. Lower inter-individual similarity within winter samples and higher than within spring samples still were detected. A possible explanation is that the strong food competition between individuals during food limitation period result in difference of food resources acquisition, but, with enhance of food available in spring, dietary intake of individuals have higher convergence because of the decline of food competition between individuals.