1. Introduction
The gut microbiota is composed of bacteria, archaea, viruses, and eukaryotic microbes, which have great potential to influence host physiology in both healthy and diseased states (Wang et al., 2023). Over the course of evolution, a stable relationship of mutual adaptation and cooperation has developed between animals and their gut microbes, and co-evolution has been achieved (Ley et al., 2008). The structure of the gut microbial community in animals is the result of the co-evolution of animals and their environment. Although the gut microbial community affects physiological functions of animals, it is highly susceptible to changes in various endogenous and exogenous factors (Bennett et al., 2016). Multiple studies have shown that the high plasticity of gut microbes makes their structure and function susceptible to changes in dietary structure, phylogenetic relationships, and the geographical environment (Zhao & Wang, 2024), and phylogenetic development exerts a greater impact on the host gut microbial community than diet and geographical environment (Amato et al., 2016). However, some studies have suggested that diet plays a dominant role in determining the composition of the host gut microbiota (Hale et al., 2018; Frankel et al., 2017). A previous study reported that the environment plays a crucial role in shaping the composition of gut microbiota (Gani et al., 2024), and animals living in different environments often exhibit distinct microbial signatures (Alberdi et al., 2021). However, only a few studies have addressed the impact of environmental changes on gut microbes, and most of them have focused on relatively few target species (McKenzie et al., 2017).
The heterogeneity of the living environment can directly influence the composition and acquisition of food resources by animals, thereby impacting the diversity of their gut microbiota (Gomez et al., 2015). The heterogeneity of primate habitats is manifested in two main ways: (1) variations between different geographical areas and (2) variations between wild and non-wild populations. A study by Zhao et al. (2018) revealed significant differences in the intestinal microbial composition of Macaca mulatta populations in different geographical environments. In addition, many studies have shown that the microbial composition of captive primates, such as Macaca mulatta (Jia et al., 2022), Macaca thibetana (Xia et al., 2022), Pygathrix nemaeus (Clayton et al., 2018), Rhinopithecus roxellanae (Zhao et al., 2023), and Alouatta pigra (Nakamura et al., 2011), is significantly different from that of wild individuals, with the former showing significantly lower microbial diversity. Feeding on a single set diet may be the main cause of reduced gut microbial diversity among captive individuals (Guo et al., 2023). In addition to food-related factors, captive individuals spend less time socializing and moving due to changes in their lifestyle (Guo et al., 2023), which may reduce the host’s exposure to microbes and reduce their gut microbial diversity. However, studies have also shown the opposite trend; for instance, gorillas in captivity in zoos show higher gut microbial diversity than those living in the wild (Narat et al., 2020). The environment in which primates are held in captivity may also alter the composition of their gut microbiota; for example, the loss of the host’s native microbiota due to reduced dietary fiber consumption under captive conditions (Clayton et al., 2016). It has been suggested that differences in the gut microbiome between wild and captive animals can significantly affect their overall health, particularly in terms of digestive and immune functions (Gani et al., 2024), and the loss of microbial diversity may underlie the increased disease prevalence in captive animals by resulting in microbial communities that are more susceptible to invasion or by altering host immune function (Kohl et al., 2014).
The Guizhou snub-nosed monkey (Rhinopithecus brelichi ) is a primate belonging to the Cercopithecidae (Colobinae), and is one of the 25 most endangered primates globally (Yang et al., 2023; Huang et al., 2024). It is only found in the Fanjing Mountain National Nature Reserve (FNNR) in Guizhou Province, China, and its wild population is small in number and distribution range (Jia et al., 2022). Owing to habitat loss and fragmentation, the population has been isolated, making R. brelichi into a species with only a single continuous population, showing very low genetic diversity and slow population growth, along with a high risk of extinction. In this context, captive breeding is crucial to improve its reproductive success and help its population to recover (Yang et al., 2023). However, R. brelichi fare poorly in captivity and exhibit chronic diarrhea, poor hair coat, pale skin tone, low reproductive success, and a general failure to thrive (Hale et al., 2019). Gut microbial disorders or changes in the composition of the gut microbiome are closely related to host health. As captivity increases the contact of primates with humans, it may lead to an increase in potential pathogens in the primates’ gut microbiota, thereby increasing the risk of disease (Clayton et al., 2016). Dietary differences are also an important cause of differences in gut microbes between wild and captive primates (Sun et al., 2023). R. brelichi is a typical leaf-eating primate. In the wild, its diet mainly consists of a large amount of leaves (Hale et al., 2019; Zhang et al., 2024), while in captivity, in addition to the leaves of various plants, its diet also includes a variety of fruits (grapes, bananas, dates, citrus, sweet potato, apple, pear, kiwi, mango, cantaloupe, peach), vegetables (lettuce, romaine, carrot, pumpkin, and eggplant), sources of protein (eggs and peanuts), and coarse grains, which are not available to its counterparts in the wild. Therefore, for the ex situ conservation of these wild animals and scientific management of their captive counterparts, it is essential to understand how the lifestyle alters the gut microbial composition, revealing interactions between the gut microbiota and host.
In this study, the gut microbiota of wild and captive R. brelichi was evaluated using noninvasive sampling of feces and high-throughput sequencing based on the 16S rRNA gene. Extensive studies confirmed that there are differences in the gut microbial community structure between wild and captive primates, which may be related to their diet, lifestyle, and other factors. This study aimed to provide an understanding of the composition and function of the gut microbiota in wild and captive R. brelichi . This study was conducted with the aim of answering the following research questions: Are there differences in gut microbial composition, diversity, and function between wild and captive R. brelichi ? What accounts for these differences? Are the changes in the gut microbiota of captive monkeys relevant to their health?