Abstract
Primates exhibit diverse social systems that are intricately linked to their biology, behavior, and evolution, all of which influence the acquisition and maintenance of their gut microbiomes (GMs). However, most studies of wild primate populations focus on taxa with relatively large group sizes, and few consider pair-living species. To address this gap, we investigate how a primate's social system interacts with key environmental, social, and genetic variables to shape the GM in pair-living, red-bellied lemurs (Eulemur rubriventer). Previous research on this species suggests that social interactions within groups influence interindividual microbiome similarity; however, the impacts of other nonsocial variables and their relative contributions to gut microbial variation remain unclear. We sequenced the 16S ribosomal RNA hypervariable V4–V5 region to characterize the GM from 26 genotyped individuals across 11 social groups residing in Ranomafana National Park, Madagascar. We estimated the degree to which sex, social group identity, genetic relatedness, dietary diversity, and home range proximity were associated with variation in the gut microbial communities residing in red-bellied lemurs. All variables except sex played a significant role in predicting GM composition. Our model had high levels of variance inflation, inhibiting our ability to determine which variables were most predictive of gut microbial composition. This inflation is likely due to red-bellied lemurs' pair-living, pair-bonded social system that leads to covariation among environmental, social, and genetic variables. Our findings highlight some of the factors that predict GM composition in a tightly bonded, pair-living species and identify variables that require further study. We propose that future primate microbiome studies should simultaneously consider environmental, social, and genetic factors to improve our understanding of the relationships among sociality, the microbiome, and primate ecology and evolution.
Original language | English (US) |
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Article number | e23657 |
Journal | American journal of primatology |
Volume | 86 |
Issue number | 9 |
DOIs | |
State | Published - Sep 2024 |
Funding
This research was conducted with the permission of Madagascar National Parks (056/13/MEF/SG/DGF/DCB.SAP/SCB), and the logistical support of the Madagascar Institut pour la Conservation des Ecosyst\u00E8mes Tropicaux, Eileen Larney, and the Centre ValBio research station staff. The fieldwork was made possible by expert field technicians and research assistants who helped with data collection: Soafaniry Razanajatovo, Alicia S\u00E1nchez Arroyo, Razafindraibe Dominique, Lahitsara Pierre, Velontsara Jeanne Baptiste, Tombotiana AV, Aura Raulo, Avery Lane. The authors would like to thank the lab staff in the Laboratory for the Evolutionary Endocrinology of Primates at the University of Arizona, especially Allison Hays, for managing sample storage and transport. They would also like to thank the PMEL Lab assistants who conducted the relatedness data analysis: Amanda Mancini, Aparna Chandrashekar, Raquel Lamela\u2010Lopez, and Santiago Cassalet. They would like to thank Tara Mittelberg and Sahana Kuthyar for conducting the 16S microbial analysis. At last, they would like to thank the DNA Services Facility at the University of Illinois Chicago, especially Stefan Green. This research was supported in part through the computation resources and staff contributions provided for the Quest high\u2010performance computing facility at Northwestern University which is jointly supported by the Office of the Provost, the Office for Research, and Northwestern University Information Technology.
Keywords
- gut microbiome
- lemur
- madagascar
- primate evolution
- social system
ASJC Scopus subject areas
- Ecology, Evolution, Behavior and Systematics
- Animal Science and Zoology