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Maternal effects on early-life gut microbiome maturation in a wild nonhuman primate

View ORCID ProfileAlice Baniel, View ORCID ProfileLauren Petrullo, Arianne Mercer, View ORCID ProfileLaurie Reitsema, Sierra Sams, View ORCID ProfileJacinta C. Beehner, View ORCID ProfileThore J. Bergman, View ORCID ProfileNoah Snyder-Mackler, View ORCID ProfileAmy Lu
doi: https://doi.org/10.1101/2021.11.06.467515
Alice Baniel
1Center for Evolution and Medicine, Arizona State University, Tempe, AZ, 85281, USA
2School of Life Sciences, Arizona State University, Tempe, AZ, 85287, USA
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  • For correspondence: alice.baniel@gmail.com amy.lu@stonybrook.edu nsnyderm@asu.edu
Lauren Petrullo
3Department of Psychology, University of Michigan, Ann Arbor, MI 48109, USA
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Arianne Mercer
4Department of Psychology, University of Washington, Seattle, WA 98195, USA
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Laurie Reitsema
5Department of Anthropology, University of Georgia, Athens, GA 30602, USA
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Sierra Sams
4Department of Psychology, University of Washington, Seattle, WA 98195, USA
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Jacinta C. Beehner
3Department of Psychology, University of Michigan, Ann Arbor, MI 48109, USA
6Department of Anthropology, University of Michigan, Ann Arbor, MI 48109, USA
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Thore J. Bergman
3Department of Psychology, University of Michigan, Ann Arbor, MI 48109, USA
7Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA
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Noah Snyder-Mackler
1Center for Evolution and Medicine, Arizona State University, Tempe, AZ, 85281, USA
2School of Life Sciences, Arizona State University, Tempe, AZ, 85287, USA
8School for Human Evolution and Social Change, Arizona State University, Tempe, AZ, 85287, USA
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  • For correspondence: alice.baniel@gmail.com amy.lu@stonybrook.edu nsnyderm@asu.edu
Amy Lu
9Department of Anthropology, Stony Brook University, Stony Brook, NY, 11794, USA
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  • ORCID record for Amy Lu
  • For correspondence: alice.baniel@gmail.com amy.lu@stonybrook.edu nsnyderm@asu.edu
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ABSTRACT

Early-life gut microbial colonization is an important process shaping host physiology, immunity and long-term health outcomes in humans and other animals. However, our understanding of this dynamic process remains poorly investigated in wild animals, where developmental mechanisms can be better understood within ecological and evolutionary relevant contexts. Using 16s rRNA amplicon sequencing on 525 fecal samples from a large cohort of infant and juvenile geladas (Theropithecus gelada), we characterized gut microbiome maturation during the first three years of life and assessed the role of maternal effects in shaping offspring microbiome assembly. Microbial diversity increased rapidly in the first months of life, followed by more gradual changes until weaning. As expected, changes in gut microbiome composition and function with increasing age reflected progressive dietary transitions: in early infancy when infants rely heavily on their mother’s milk, microbes that facilitate milk glycans and lactose utilization dominated, while later in development as graminoids are progressively introduced into the diet, microbes that metabolize plant complex polysaccharides became dominant. Furthermore, the microbial community of nursing infants born to first-time (primiparous) mothers was more “milk-oriented” compared to similarly-aged infants born to experienced (multiparous) mothers. Comparisons of matched mother-offspring fecal samples to random dyads did not support vertical transmission as a conduit for these maternal effects, which instead could be explained by slower phenotypic development (and associated slower gut microbiome maturation) in infants born to first-time mothers. Together, our findings highlight the dynamic nature of gut colonization in early life and the role of maternal effects in modulating this trajectory in a wild primate.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://github.com/GeladaResearchProject/Baniel-et-al_2022_Infant-gut-microbiome

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted November 07, 2021.
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Maternal effects on early-life gut microbiome maturation in a wild nonhuman primate
Alice Baniel, Lauren Petrullo, Arianne Mercer, Laurie Reitsema, Sierra Sams, Jacinta C. Beehner, Thore J. Bergman, Noah Snyder-Mackler, Amy Lu
bioRxiv 2021.11.06.467515; doi: https://doi.org/10.1101/2021.11.06.467515
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Maternal effects on early-life gut microbiome maturation in a wild nonhuman primate
Alice Baniel, Lauren Petrullo, Arianne Mercer, Laurie Reitsema, Sierra Sams, Jacinta C. Beehner, Thore J. Bergman, Noah Snyder-Mackler, Amy Lu
bioRxiv 2021.11.06.467515; doi: https://doi.org/10.1101/2021.11.06.467515

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