Primate phageomes are structured by superhost phylogeny and environment

Area of Science:

• Microbiology
• Evolutionary Biology
• Primate Ecology

Background:

• The human gut microbiome, including bacterial and bacteriophage (phage) communities, profoundly influences health.
• The evolutionary and ecological origins of human-associated phage communities remain largely unknown.

Purpose of the Study:

• To investigate the origins of human-associated phage communities by examining fecal phageomes in wild nonhuman primates.
• To understand how primate social behavior and captivity influence phageome composition and evolution.

Main Methods:

• Analysis of fecal phageomes from 23 wild nonhuman primate taxa across major primate radiations.
• Phylogenetic analysis to identify phage-superhost relationships and codivergence.
• Comparison of phageome composition in wild, captive, and human populations.

Main Results:

• Relatives of most human-associated phages were identified in wild primates, indicating ancient associations.
• Distinct phageome compositions were observed across primate taxa, showing phylosymbiotic signals and evidence of phage-superhost codivergence.
• Primate social behavior structured phageomes within species, while captivity led to a replacement of wild-associated phages with human-associated ones.

Conclusions:

• Primate-phage associations are ancient and have persisted for millions of years, shaped by host phylogeny and social behavior.
• Phage transmission via social interactions (e.g., grooming) plays a key role in shaping these communities.
• Captivity dramatically alters phageome composition, suggesting a loss of ancestral phage communities and acquisition of human-associated ones.