Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes

Abstract

Over the past decade several studies have reported that the gut microbiomes of mammals with similar dietary niches exhibit similar compositional and functional traits. However, these studies rely heavily on samples from captive individuals and often confound host phylogeny, gut morphology, and diet. To more explicitly test the influence of host dietary niche on the mammalian gut microbiome we use 16S rRNA gene amplicon sequencing and shotgun metagenomics to compare the gut microbiota of 18 species of wild non-human primates classified as either folivores or closely related non-folivores, evenly distributed throughout the primate order and representing a range of gut morphological specializations. While folivory results in some convergent microbial traits, collectively we show that the influence of host phylogeny on both gut microbial composition and function is much stronger than that of host dietary niche. This pattern does not result from differences in host geographic location or actual dietary intake at the time of sampling, but instead appears to result from differences in host physiology. These findings indicate that mammalian gut microbiome plasticity in response to dietary shifts over both the lifespan of an individual host and the evolutionary history of a given host species is constrained by host physiological evolution. Therefore, the gut microbiome cannot be considered separately from host physiology when describing host nutritional strategies and the emergence of host dietary niches.

Fig. 1

Host dietary niche has a weak effect on primate gut microbiota composition. Principal coordinates analysis (PCoA; a unweighted and b weighted UniFrac distances) of 16S rRNA gene amplicon data illustrates stronger clustering of non-human primate fecal samples by host phylogenetic clade (unweighted UniFrac: PERMANOVA F_3,153 = 26.4, r² = 0.29, p < 0.01; weighted UniFrac: PERMANOVA F_3,153 = 21.7, r² = 0.27, p < 0.01) than diet (unweighted UniFrac: PERMANOVA F_1,153 = 13.1, r² = 0.05, p < 0.01; weighted UniFrac: PERMANOVA F_1,153 = 9.2, r² = 0.04, p < 0.01). Large spheres represent folivorous primates and small spheres represent non-folivorous primates. Folivores are shaded in the phylogenetic tree. (Note that T. gelada consumes grass, which shares many nutritional challenges with leaves.)

Fig. 2

Folivorous primates share few gut microbiota traits at the taxonomic level. A phylogenetic tree summarizes the results of the linear mixed effects analysis applied to balances. The circular heatmaps surrounding the tree plot the proportions of microbes across all of the samples, with the outmost ring containing samples from folivorous species and the inner ring containing samples from non-folivorous species. Three significant balances (p-value <0.01) differentiate the gut microbiota of folivorous primates from non-folivorous primates. Darker shades represent enrichment of that particular microbial clade

Fig. 3

Host dietary niche has a weak effect on primate gut microbiota functional potential. a Principal coordinates analysis (PCoA; Bray-Curtis dissimilarity) of MetaCyc reaction pathway data illustrates weak clustering of non-human primate fecal samples by diet (PERMANOVA F_1,93 = 8.7, r² = 0.07, p < 0.01). b PCoA illustrating Procrustes analysis of 16S rrNA gene amplicon data (unweighted UniFrac distance) and Metacyc reaction pathway data (Bray-Curtis dissimilarity). For both datasets, host phylogenetic clade is the strongest driver of sample clustering patterns. Sample sizes indicated in parentheses

Fig. 4

Folivorous primates share few gut microbiota traits at the functional level. MetaCyc reaction pathways with differential relative abundances between folivorous and non-folivorous primates according to linear mixed effects models show few patterns. Positive values illustrate enrichment in folivorous primates while negative values illustrate enrichment in non-folivorous primates