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?