Social behavior can alter the microbiome composition via transmission among social partners, but there have been few controlled experimental studies of gut microbiome transmission among social partners in primates. We collected longitudinal fecal samples from eight unrelated male-female pairs of marmoset monkeys prior to pairing and for 8 weeks following pairing. We then sequenced 16S rRNA to characterize the changes in the gut microbiome that resulted from the pairing. Marmoset pairs had a higher similarity in gut microbiome communities after pairing than before pairing. We discovered sex differences in the degrees of change in gut microbiome communities following pairing. Specifically, the gut microbiome communities in males exhibited greater dissimilarity from the prepairing stage (baseline) than the gut microbiome communities in females. Conversely, females showed a gradual stabilization in the rate of the gut microbiome community turnover. Importantly, we found that the male fecal samples harbored more female-source gut microbes after pairing, especially early in pairing (paired test, P < 0.05), possibly linked to sex bias in the frequencies of social behavior. From this controlled study, we report for the first time that pair-living primates undergo significant changes in gut microbiome during pairing and that females transmit more microbes to their partners than males do. The potential biases influencing which microbes are transmitted on the basis of sex and whether they are due to sex biases in other behavioral or physiological features need to be widely investigated in other nonhuman primates and humans in the future. IMPORTANCE In this controlled study, we collected longitudinal fecal samples from 16 male and female marmoset monkeys for 2 weeks prior to and for 8 weeks after pairing in male-female dyads. We report for the first time that marmoset monkeys undergo significant changes to the gut microbiome following pairing and that these changes are sex-biased; i.e., females transmit more microbes to their social partners than males do. Marmosets exhibit pair bonding behavior such as spatial proximity, physical contact, and grooming, and sex biases in these behavioral patterns may contribute to the observed sex bias in social transmission of gut microbiomes.
Bibliographical noteFunding Information:
We are grateful to Devin Rose and Caroline Smith for helping with the experiment. We are thankful to members of the French laboratory for helping with sample collection and providing feedback during manuscript preparation. The Callitrichid Research Center is supported in part by NIH (HD089147). L.Z., A.C.M., A.K.B., D.K., and J.A.F. designed the research. H.R.H. collected the fecal samples. L.Z. carried out the experiment. L.Z., M.J.S.V.H., and Q.Y. did the sequencing. L.Z., J.B.C., A.C.M., and D.K. performed the data analysis. L.Z., J.A.F., and D.K. wrote the manuscript. All of us contributed to the discussion. We declare that we have no conflicts of interest relevant to the manuscript.
© 2020 Zhu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.
Copyright 2020 Elsevier B.V., All rights reserved.
- Common marmosets
- Gut microbiome transmission
- Longitudinal sampling
- Pair-bond formation
- Sex bias
- Social behavior
- Social transmission