Differences in the bacterial communities inhabiting mammalian gut microbiomes tend to reflect the phylogenetic relatedness of their hosts, a pattern dubbed phylosymbiosis. Although most research on this pattern has compared the gut microbiomes of host species across biomes, understanding the evolutionary and ecological processes that generate phylosymbiosis requires comparisons across phylogenetic scales and under similar ecological conditions. We analysed the gut microbiomes of 14 sympatric small mammal species in a semi‐arid African savanna, hypothesizing that there would be a strong phylosymbiotic pattern associated with differences in their body sizes and diets. Consistent with phylosymbiosis, microbiome dissimilarity increased with phylogenetic distance among hosts, ranging from congeneric sets of mice and hares that did not differ significantly in microbiome composition to species from different taxonomic orders that had almost no gut bacteria in common. While phylosymbiosis was detected among just the 11 species of rodents, it was substantially weaker at this scale than in comparisons involving all 14 species together. In contrast, microbiome diversity and composition were generally more strongly correlated with body size, dietary breadth, and dietary overlap in comparisons restricted to rodents than in those including all lineages. The starkest divides in microbiome composition thus reflected the broad evolutionary divergence of hosts, regardless of body size or diet, while subtler microbiome differences reflected variation in ecologically important traits of closely related hosts. Strong phylosymbiotic patterns arose deep in the phylogeny, and ecological filters that promote functional differentiation of cooccurring host species may disrupt or obscure this pattern near the tips.
Mammalian gut microbiomes differ within and among hosts. Hosts that occupy a broad range of environments may exhibit greater spatiotemporal variation in their microbiome than those constrained as specialists to narrower subsets of resources or habitats. This can occur if widespread host encounter a variety of ecological conditions that act to diversify their gut microbiomes and/or if generalized host species tend to form large populations that promote sharing and maintenance of diverse microbes. We studied spatiotemporal variation in the gut microbiomes of three co‐occurring rodent species across an environmental gradient in a Kenyan savanna. We hypothesized: (1) the taxonomic, phylogenetic, and functional compositions of gut microbiomes as predicted using the Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt) differ significantly among host species; (2) microbiome richness increases with population size for all host species; and (3) host species exhibit different levels of seasonal change in their gut microbiomes, reflecting different sensitivities to the environment. We evaluated changes in gut microbiome composition according to host species identity, site, and host population size using three years of capture–mark–recapture data and 351 microbiome samples. Host species differed significantly in microbiome composition, though the two species with more specialized diets and higher demographic sensitivities showed only slightly greater microbiome variability than those of a widespread dietary generalist. Total microbiome richness increased significantly with host population size for all species, but only one of the more specialized species also exhibited greater individual‐level microbiome richness in large populations. Across co‐occurring rodent species with diverse diets and life histories, large host population sizes were associated both with greater population‐level microbiome richness (sampling effects) and turnover in the relative abundance of bacterial taxa (environmental effects), but there was no consistent pattern for individual‐level richness (individual specialization). Together, our results show that maintenance of large host populations contributes to the maintenance of gut microbiome diversity in wild mammals.
more » « less- PAR ID:
- 10507639
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Ecosphere
- Volume:
- 15
- Issue:
- 5
- ISSN:
- 2150-8925
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract -
more » « less
Abstract The gut microbiomes of mammals appear to mirror their hosts’ phylogeny, suggesting host-driven microbial community assembly. Yet, much of this evidence stems from comparative studies of distinct wild or captive populations that lack data for disentangling the relative influences of shared phylogeny and environment. Here, we present phylogenetic and multivariate analyses of gut microbiomes from six sympatric (i.e., co-occurring) mammal species inhabiting a 1-km2 area in western Madagascar—three lemur and three non-primate species—that consider genetic, dietary, and ecological predictors of microbiome functionality and composition. Host evolutionary history, indeed, appears to shape gut microbial patterns among both closely and distantly related species. However, we also find that diet—reliance on leaves versus fruit—is the best predictor of microbiome similarity among closely related lemur species, and that host substrate use—ground versus tree—constrains horizontal transmission via incidental contact with feces, with arboreal species harboring far more distinct communities than those of their terrestrial and semi-terrestrial counterparts.
-
Kormas, Konstantinos Aristomenis (Ed.)ABSTRACT The study of the mammalian microbiome serves as a critical tool for understanding host-microbial diversity and coevolution and the impact of bacterial communities on host health. While studies of specific microbial systems (e.g., in the human gut) have rapidly increased, large knowledge gaps remain, hindering our understanding of the determinants and levels of variation in microbiomes across multiple body sites and host species. Here, we compare microbiome community compositions from eight distinct body sites among 17 phylogenetically diverse species of nonhuman primates (NHPs), representing the largest comparative study of microbial diversity across primate host species and body sites. Analysis of 898 samples predominantly acquired in the wild demonstrated that oral microbiomes were unique in their clustering, with distinctive divergence from all other body site microbiomes. In contrast, all other body site microbiomes clustered principally by host species and differentiated by body site within host species. These results highlight two key findings: (i) the oral microbiome is unique compared to all other body site microbiomes and conserved among diverse nonhuman primates, despite their considerable dietary and phylogenetic differences, and (ii) assessments of the determinants of host-microbial diversity are relative to the level of the comparison (i.e., intra-/inter-body site, -host species, and -individual), emphasizing the need for broader comparative microbial analyses across diverse hosts to further elucidate host-microbial dynamics, evolutionary and biological patterns of variation, and implications for human-microbial coevolution. IMPORTANCE The microbiome is critical to host health and disease, but much remains unknown about the determinants, levels, and evolution of host-microbial diversity. The relationship between hosts and their associated microbes is complex. Most studies to date have focused on the gut microbiome; however, large gaps remain in our understanding of host-microbial diversity, coevolution, and levels of variation in microbiomes across multiple body sites and host species. To better understand the patterns of variation and evolutionary context of host-microbial communities, we conducted one of the largest comparative studies to date, which indicated that the oral microbiome was distinct from the microbiomes of all other body sites and convergent across host species, suggesting conserved niche specialization within the Primates order. We also show the importance of host species differences in shaping the microbiome within specific body sites. This large, comparative study contributes valuable information on key patterns of variation among hosts and body sites, with implications for understanding host-microbial dynamics and human-microbial coevolution.more » « less
-
Meyer, Axel (Ed.)Adaptive radiations offer an excellent opportunity to understand the eco-evolutionary dynamics of gut microbiota and host niche specialization. In a laboratory common garden, we compared the gut microbiota of two novel derived trophic specialist pupfishes, a scale-eater and a molluscivore, to closely related and distant outgroup generalist populations, spanning both rapid trophic evolution within 10 kya and stable generalist diets persisting over 11 Mya. We predicted an adaptive and highly divergent microbiome composition in the trophic specialists reflecting their rapid rates of craniofacial and behavioral diversification. We sequenced 16S rRNA amplicons of gut microbiomes from lab-reared adult pupfishes raised under identical conditions and fed the same high protein diet. In contrast to our predictions, gut microbiota largely reflected phylogenetic distance among species, rather than generalist or specialist life history, in support of phylosymbiosis. However, we did find significant enrichment of Burkholderiaceae bacteria in replicated lab-reared scale-eater populations. These bacteria sometimes digest collagen, the major component of fish scales, supporting an adaptive shift. We also found some enrichment of Rhodobacteraceae and Planctomycetia in lab-reared molluscivore populations, but these bacteria target cellulose. Overall phylogenetic conservation of microbiome composition contrasts with predictions of adaptive radiation theory and observations of rapid diversification in all other trophic traits in these hosts, including craniofacial morphology, foraging behavior, aggression, and gene expression, suggesting that the functional role of these minor shifts in microbiota will be important for understanding the role of the microbiome in trophic diversification.more » « less
-
more » « less
Vertebrates host complex microbiomes that impact their physiology. In many taxa, including colourful wood-warblers, gut microbiome similarity decreases with evolutionary distance. This may suggest that as host populations diverge, so do their microbiomes, because of either tight coevolutionary dynamics, or differential environmental influences, or both. Hybridization is common in wood-warblers, but the effects of evolutionary divergence on the microbiome during secondary contact are unclear. Here, we analyse gut microbiomes in two geographically disjunct hybrid zones between blue-winged warblers (
Vermivora cyanoptera ) and golden-winged warblers (Vermivora chrysoptera ). We performed 16S faecal metabarcoding to identify species-specific bacteria and test the hypothesis that host admixture is associated with gut microbiome disruption. Species identity explained a small amount of variation between microbiomes in only one hybrid zone. Co-occurrence of species-specific bacteria was rare for admixed individuals, yet microbiome richness was similar among admixed and parental individuals. Unexpectedly, we found several bacteria that were more abundant among admixed individuals with a broader deposition of carotenoid-based plumage pigments. These bacteria are predicted to encode carotenoid biosynthesis genes, suggesting birds may take advantage of pigments produced by their gut microbiomes. Thus, host admixture may facilitate beneficial symbiotic interactions which contribute to plumage ornaments that function in sexual selection.
