Insights Into Variations in the Gut Virome of Tibetan Macaques (Macaca thibetana) Across Wild, Captive, and Semi-Provisioned Environments

Abstract

Viruses are integral components of the mammalian gut ecosystem, playing crucial roles in regulating the gut microbiome and maintaining host health. However, the impact of human activity on the gut virome of mammals remains poorly understood. This study investigated the gut viromes of Tibetan macaques (Macaca thibetana), a primate species endemic to China, under three distinct human-influenced environments (wild, semi-provisioned, and captive) using metagenomic sequencing. Our results revealed that semi-provisioned macaques supported the highest viral diversity, while captive and wild groups exhibited lower diversity, with distinct functional shifts among groups. Furthermore, the co-variation and highly coupled KEGG functional profiles between viral and bacterial communities suggest they function as an integrated synergistic network, where changes in one directly impact the metabolic output of the other. Co-occurrence network analysis further demonstrated that the virus-bacterium interaction network in the captive group was the most fragile, with a structure indicative of a high risk of micro-ecosystem imbalance. Microbial system imbalance is characterized by alterations in both community composition and function, resulting in diminished resilience and stability, which may ultimately compromise host intestinal health. Our results demonstrate that captivity and provisioning drive divergence in the Tibetan macaque gut virome. The fragile, skewed networks in captive individuals highlight a potential cost to microbial health, which may underlie broader health and adaptation risks such as heightened pathogen susceptibility and diminished capacity to cope with environmental perturbations. Thus, monitoring the virome offers a novel early-warning system, informing strategies to enhance welfare and conservation outcomes.