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. 2018 Oct;12(10):2559-2574.
doi: 10.1038/s41396-018-0166-1. Epub 2018 Jun 28.

Factors Influencing Bacterial Microbiome Composition in a Wild Non-Human Primate Community in Taï National Park, Côte d'Ivoire

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Free PMC article

Factors Influencing Bacterial Microbiome Composition in a Wild Non-Human Primate Community in Taï National Park, Côte d'Ivoire

Jan F Gogarten et al. ISME J. .
Free PMC article

Abstract

Microbiomes impact a variety of processes including a host's ability to access nutrients and maintain health. While host species differences in microbiomes have been described across ecosystems, little is known about how microbiomes assemble, particularly in the ecological and social contexts in which they evolved. We examined gut microbiome composition in nine sympatric wild non-human primate (NHP) species. Despite sharing an environment and interspecific interactions, individuals harbored unique and persistent microbiomes influenced by host species, social group, and parentage, but surprisingly not by social relationships among members of a social group. We found a branching order of host-species networks constructed using the composition of their microbiomes as characters, which was incongruent with known NHP phylogenetic relationships, with chimpanzees (Pan troglodytes verus) sister to colobines, upon which they regularly prey. In contrast to phylogenetic clustering found in all monkey microbiomes, chimpanzee microbiomes were unique in that they exhibited patterns of phylogenetic overdispersion. This reflects unique ecological processes impacting microbiome composition in chimpanzees and future studies will elucidate the aspects of chimpanzee ecology, life history, and physiology that explain their unique microbiome community structure. Our study of contemporaneous microbiomes of all sympatric diurnal NHP in an ecosystem highlights the diverse dispersal routes shaping these complex communities.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Fig. 1
Fig. 1
a Tree of microbiome community structure estimated with heuristic maximum parsimony using the abundance based scores of bacterial abundance as characters. Each terminal branch represents a particular sample, with the colors indicating the NHP species that gave rise to the sample. Black branches indicate internal branches that are shared by different NHP hosts. Bootstrap support is shown for clades and the root position was supported by our TempEst analysis. b Phylogeny of the primate hosts based on 11 mitochondrial and 6 autosomal genes made available through the 10kTrees project [82]. c Unrooted network built using SplitsTree4 and the unifrac dissimilarity matrix as input, with terminal branches colored as in (b)
Fig. 2
Fig. 2
a Abundance of bacterial phyla for core bacterial oligotypes (i.e., those shared by at least 80% of individuals in a host species, with the number of reads rarified to the minimum in any sample in the dataset or 4158 reads), shown separately for each NHP species. b Non-metric multidimensional scaling (NMDS) ordination of mangabey gut bacterial oligotype abundance data by social group (Bray–Curtis distance, stress value = 0.24; Mantel test: nsamples = 257, nindividuals = 87, different group = 0.0737, same group = 0.0862, P < 0.001). c NMDS ordination of chimpanzee gut bacterial oligotype abundance data (Bray–Curtis distance, stress value = 0.19) by social group (Mantel test: nsamples = 98, nindividuals = 64, UniFrac different group = 0.439, UniFrac same group = 0.408, P < 0.001). d NMDS ordination of gut bacterial oligotype abundance data by host species (Bray–Curtis distance, stress value = 0.068) of gut bacterial oligotype abundance data by NHP species. Ellipses indicate the 95% confidence ellipse when more than two samples were available for a particular NHP species or social group
Fig. 3
Fig. 3
Comparison of weighted UniFrac dissimilarities between samples from sooty mangabeys in the Audrenissrou group, (a) when stemming from the same or different individuals (Mantel-like permutation test: nsamples = 229, nindividuals = 59, different individuals = 0.0737, same individual = 0.0610, P < 0.001), (b) between samples of the same individual sooty mangebeys in different or the same years (nsamples = 146, between sampling year = 0.0658, within sampling years = 0.0559; Wilcoxon test, T+ = 348, N = 26, P < 0.001), (c) for the same sooty mangabeys individuals sampled in the same versus different sampling years (nsamples = 229, nindividuals = 59, different individuals different years = 0.0749, same individual different years = 0. 0658, P < 0.001), (d) when stemming from sooty mangebey mother–offspring pairs or from non-mother–offspring pairs (Mantel test: nsamples = 117, nmother–offspring pairs = 18, non-mother–offspring pair = 0.0705, mother–offspring pair = 0.0637, P = 0.033), and (e) between samples from chimpanzees in the South group (nsamples = 47, nindividuals = 24, different individuals = 0.0933, same individual = 0.0672, P < 0.001) and (f) chimpanzees in the North group (nsamples = 23, nindividuals = 12, different individuals = 0.101, same individual = 0.0836, P = 0.037) when stemming from the same or different individuals. The middle horizontal line represents the median while the rectangle shows the quartiles and the vertical line represents the 2.5th and 97.5th percentiles. Dashed lines in (b) indicate the paired nature of the dataset, connecting the dissimilarity for samples from each individual from the same or different sampling years
Fig. 4
Fig. 4
Standardized effect size of mean phylogenetic distance based on null model simulations of the bacterial community in each fecal sample, separated by host species. The solid middle horizontal line of the rectangles represents the median, the rectangle shows the quartiles, and the vertical line represents the 2.5th and 97.5th percentiles, while the values for each sample are indicated by overlapping gray circles. Values above the dashed line are those exhibiting phylogenetic overdispersion (i.e., communities composed of bacterial oligotypes that are less related than expected under the null model), while those below the line exhibit phylogenetic clumping (i.e., communities composed of oligotypes that are more related than expected under the null model)
Fig. 5
Fig. 5
Standardized effect size of mean phylogenetic distance based on null model simulations of the bacterial community in each fecal sample using different bacterial source pools. a For sooty mangabeys for each individual that was included in a mother–offspring pair, we used a source pool including only the bacteria found in any sample of a repeatedly sampled individual. We also considered a mother–offspring pool, using a source pool of only the bacteria found in any sample of the respective mother–offspring pair. For the group pool we used a source pool of only the bacteria found in the social group, for the host species, using a source pool of only the bacteria found in any sooty mangabey sample, and for the primate pool a source pool of all bacteria found in this study. b For chimpanzees we conducted a similar analysis; we did not include mother–offspring pairs and rather conducted the group analysis for each of the two groups for which we had repeated sampling of individuals. In addition, we included a source pool level that consisted of bacteria found in any colobine or chimpanzee sample. The solid middle horizontal line of the rectangles represents the median, the rectangle shows the quartiles, and the vertical line represents the 2.5th and 97.5th percentiles, while the values for each sample are indicated by overlapping gray circles. Values above the dashed line are those exhibiting phylogenetic overdispersion while those below the line exhibit phylogenetic clumping

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