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

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.

Keywords: aging; chimpanzee; development; diversity; gut microbiota; infancy; maturation; microbiome; primate; weaning.

Figure 1:. Gut microbial community alpha-diversity varies among chimpanzee age groups.

(A) Observed OTU richness of individual chimpanzees as a factor of age group. (B) Shannon index of individual chimpanzees as a factor of age group. Large circles are means; bars show standard deviations. P values reported for linear mixed effects model likelihood tests. * indicates P<0.05 contrast for estimated marginal means of linear mixed effects model. See also Data S1 and Table S2.

Figure 2:. Gut microbial community composition varies among chimpanzee age groups.

(A) Nonmetric multidimensional scaling (NMDS) ordination plot illustrates differences in gut microbial community composition, based on Bray-Curtis dissimilarities as a factor of age group. Ellipses illustrate standard deviation for age groups. (B) Bray-Curtis dissimilarities between individual chimpanzees and each adult chimpanzee as a factor of age group. (C) Bray-Curtis dissimilarities between individual chimpanzees and other members of their age group, as a factor of age group. Large circles are means; bars show standard deviations. P values reported for (A) PERMANOVA and (B,C) bootstrapped Kruskal-Wallis. * indicates P<0.05 contrast for estimated marginal means of linear mixed effects model. See also Figures S1-S3, Data S1 and Table S2.

Figure 3:. Change over time in an individual’s gut microbial community composition depends on age and transition between age groups.

(A) Bray-Curtis dissimilarities for an individual chimpanzee compared to itself over time (with greater than one year between samples) as a factor of age group. (B) Bray-Curtis dissimilarities for an individual chimpanzee compared to itself over time (with greater than one year between samples) as a factor of whether the elapsed time led to them transitioning between two age groups. Large circles are means; bars show standard deviations. P values reported for linear mixed effects model likelihood tests. * indicates P<0.05 contrast for estimated marginal means of linear mixed effects model. See also Data S1 and Table S2.

Figure 4:. Several bacterial taxa associated with human infants (as per Ref. ) were also enriched in chimpanzee infants.

Relative abundance of bacterial taxa by chimpanzee age group. Large circles are means; bars show standard deviations. P values reported for linear mixed effects model likelihood tests. * indicates P<0.05 contrast for estimated marginal means of linear mixed effects model. See also Data S1 and Tables S1, S2.