Age Patterning in Wild Chimpanzee Gut Microbiota Diversity Reveals Differences from Humans in Early Life

Aspen T. Reese, Sarah R. Phillips, Leah A. Owens, Emily M. Venable, Kevin E. Langergraber, Zarin P. Machanda, John C. Mitani, Martin N. Muller, David P. Watts, Richard W. Wrangham, Tony L. Goldberg, Melissa Emery Thompson, Rachel N. Carmody

Research output: Contribution to journalArticlepeer-review

24 Scopus citations

Abstract

Survival in primates is facilitated by commensal gut microbes that ferment otherwise indigestible plant matter, resist colonization by pathogens, and train the developing immune system.1,2 However, humans are unique among primates in that we consume highly digestible foods, wean early, mature slowly, and exhibit high lifelong investments in maintenance.3–6 These adaptations suggest that lifetime trajectories of human-microbial relationships could differ from those of our closest living relatives. Here, we profile the gut microbiota of 166 wild chimpanzees aged 8 months to 67 years in the Kibale National Park, Uganda and compare the patterns of gut microbial maturation to those previously observed in humans. We found that chimpanzee gut microbial alpha-diversity, composition, density, interindividual variation, and within-individual change over time varied significantly with age. Notably, gut microbial signatures in infants <2 years old were distinct across all five metrics. Infant chimpanzee guts were enriched in some of the same taxa prevalent in infant humans (e.g., Bifidobacterium, Streptococcus, and Bacteroides), and chimpanzee gut microbial communities, like those of humans, exhibited higher interindividual variation in infancy versus later in life. However, in direct contrast to human infants, chimpanzee infants harbored surprisingly high-diversity rather than low-diversity gut bacterial communities compared with older conspecifics. These data indicate differential trajectories of gut microbiota development in humans and chimpanzees that are consistent with interspecific differences in lactation, diet, and immune function. Probing the phenotypic consequences of differential early-life gut microbial diversity in chimpanzees and other primates will illuminate the life history impacts of the hominid-microbiome partnership.

Original languageEnglish (US)
Pages (from-to)613-620.e3
JournalCurrent Biology
Volume31
Issue number3
DOIs
StatePublished - Feb 8 2021

Keywords

  • aging
  • chimpanzee
  • development
  • diversity
  • gut microbiota
  • infancy
  • maturation
  • microbiome
  • primate
  • weaning

ASJC Scopus subject areas

  • General Neuroscience
  • General Biochemistry, Genetics and Molecular Biology
  • General Agricultural and Biological Sciences

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