Abstract
Group living occurs across the animal kingdom and can shape fundamental aspects of individual biology, including the microbes inhabiting the animal gut. The naked mole-rat, Heterocephalus glaber, exhibits extreme cooperative breeding (eusociality) and presents an ideal opportunity to study the effects of social structure on the mammalian gut microbiota. Within colonies reproduction is limited to few animals, while the remaining members are non-reproductive, form linear dominance hierarchies, and show evidence of task specialization with stable yet plastic behavioral phenotypes. Here, we sequenced the gut bacteria of naked mole-rats across 6 replicate captive colonies and longitudinally during a colony removal experiment. Colony had much larger effects than social phenotype or status on the diversity and composition of gut bacteria. Our longitudinal experiment revealed that over the course of 2 months, the gut bacteria of previously unfamiliar, newly paired animals did not become more similar. In comparison to mice housed in the same facility, the naked mole-rat gut microbiome exhibited substantial compositional differences including the near absence of Lactobacillaceae and the enrichment of Prevotellaceae. Our study provides new insight into the factors shaping gut bacterial communities in social animals and indicates a prominent role of social group membership but not social phenotype.
Significance statement
The social groups to which animals belong can be strong determinants of the composition of their associated gut microbial communities (i.e., gut microbiome). However, less is known about the link between social status within animal groups and the gut microbiome. We studied this relationship in the naked mole-rat, Heterocephalus glaber, which exhibits extreme cooperative breeding (eusociality). Animals within naked mole-rat colonies show clear social hierarchies and evidence of social phenotypes. Across replicate colonies, we found that colony but not social phenotype or status had large effects on the diversity and composition of gut bacteria. During a colony removal experiment, the gut bacteria of newly paired but previously unfamiliar animals did not become more similar over the course of 2 months. Our results show that when decoupled from differences in diet or exposure to microbes, within colony social roles and their accompanying unique physiology and social experience may have little effect on gut microbiota. In contrast, gut bacterial diversity and composition was strongly shaped by colony membership despite being exposed to identical environmental conditions.
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Data availability
All sequencing files have been archived with the National Center for Biotechnology Information Sequence Read Archive (NCBI SRA) under accession PRJNA635135. All data required to reproduce the analyses can be found at https://figshare.com/s/3edbe9c9df1d2832c9ab.
Code availability
All code required to reproduce the analyses can be found at https://figshare.com/s/3edbe9c9df1d2832c9ab.
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Acknowledgements
We thank M.T.J. Johnson for the use of lab space and equipment and T. Phung for assistance in collecting mouse fecal samples. We also thank Albrecht Schulte-Hostedde and three anonymous reviewers whose careful evaluation improved this work.
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This work was supported by the University of Toronto Mississauga Research & Scholarly Activity Fund and a National Science and Engineering Research Council of Canada (NSERC) Discovery Grant RGPIN 2018–04780 and NSERC Discovery Accelerator Supplement RGPAS 2018–522465 (to MMH). CRF was supported by an NSERC PDF, and IT was supported by an NSERC PGS D.
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CRF, IT, and MMH conceptualized the study. IT performed animal experiments and collected samples. CRF performed molecular work and analyzed data. CRF wrote the first draft of the manuscript, and all authors contributed substantially to revisions.
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Fitzpatrick, C.R., Toor, I. & Holmes, M.M. Colony but not social phenotype or status structures the gut bacteria of a eusocial mammal. Behav Ecol Sociobiol 76, 117 (2022). https://doi.org/10.1007/s00265-022-03230-5
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DOI: https://doi.org/10.1007/s00265-022-03230-5