An official website of the United States government
Abstract 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.
more »
« less
Gut microbial ecology of Philippine gekkonids: ecoevolutionary effects on microbiome compositions
Abstract Given the rapidly changing landscapes of habitats across the globe, a sound understanding of host-associated microbial communities and the ecoevolutionary forces that shape them is needed to assess general organismal adaptability. Knowledge of the symbiotic endogenous microbiomes of most reptilian species worldwide remains limited. We sampled gut microbiomes of geckos spanning nine species and four genera in the Philippines to (i) provide baseline data on gut microbiota in these host species, (ii) test for significant associations between host phylogenetic relationships and observed microbial assemblages, potentially indicative of phylosymbiosis, and (iii) identify correlations between multiple ecoevolutionary factors (e.g. species identity, habitat tendencies, range extents, and maximum body sizes) and gut microbiomes in Philippine gekkonids. We recovered no significant association between interspecific host genetic distances and observed gut microbiomes, providing limited evidence for phylosymbiosis in this group. Philippine gekkonid microbiomes were associated most heavily with host species identity, though marked variation among conspecifics at distinct sampling sites indicates that host locality influences gut microbiomes as well. Interestingly, individuals grouped as widespread and microendemic regardless of host species identity displayed significant differences in alpha and beta diversity metrics examined, likely driven by differences in rare OTU presence between groups. These results provide much needed insight in host-associated microbiomes in wild reptiles and the ecoevolutionary forces that structure such communities.
more »
« less
- Award ID(s):
- 1657648
- PAR ID:
- 10470896
- Publisher / Repository:
- Oxford Academic
- Date Published:
- Journal Name:
- FEMS Microbiology Ecology
- Volume:
- 98
- Issue:
- 12
- ISSN:
- 1574-6941
- Page Range / eLocation ID:
- fiac124
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract BackgroundInter-population variation in host-associated microbiota reflects differences in the hosts’ environments, but this characterization is typically based on studies comparing few populations. The diversity of natural habitats and captivity conditions occupied by any given host species has not been captured in these comparisons. Moreover, intraspecific variation in gut microbiota, generally attributed to diet, may also stem from differential acquisition of environmental microbes—an understudied mechanism by which host microbiomes are directly shaped by environmental microbes. To more comprehensively characterize gut microbiota in an ecologically flexible host, the ring-tailed lemur (Lemur catta; n = 209), while also investigating the role of environmental acquisition, we used 16S rRNA sequencing of lemur gut and soil microbiota sampled from up to 13 settings, eight in the wilderness of Madagascar and five in captivity in Madagascar or the U.S. Based on matched fecal and soil samples, we used microbial source tracking to examine covariation between the two types of consortia. ResultsThe diversity of lemur gut microbes varied markedly within and between settings. Microbial diversity was not consistently greater in wild than in captive lemurs, indicating that this metric is not necessarily an indicator of host habitat or environmental condition. Variation in microbial composition was inconsistent both with a single, representative gut community for wild conspecifics and with a universal ‘signal of captivity’ that homogenizes the gut consortia of captive animals. Despite the similar, commercial diets of captive lemurs on both continents, lemur gut microbiomes within Madagascar were compositionally most similar, suggesting that non-dietary factors govern some of the variability. In particular, soil microbial communities varied across geographic locations, with the few samples from different continents being the most distinct, and there was significant and context-specific covariation between gut and soil microbiota. ConclusionsAs one of the broadest, single-species investigations of primate microbiota, our study highlights that gut consortia are sensitive to multiple scales of environmental differences. This finding begs a reevaluation of the simple ‘captive vs. wild’ dichotomy. Beyond the important implications for animal care, health, and conservation, our finding that environmental acquisition may mediate aspects of host-associated consortia further expands the framework for how host-associated and environmental microbes interact across different microbial landscapes.more » « less
-
Suen, Garret (Ed.)ABSTRACT The gut microbiome is a symbiotic microbial community associated with the host and plays multiple important roles in host physiology, nutrition, and health. A number of factors have been shown to influence the gut microbiome, among which diet is considered to be one of the most important; however, the relationship between diet composition and gut microbiota in wild mammals is still not well recognized. Herein, we characterized the gut microbiota of bats and examined the effects of diet, host taxa, body size, gender, elevation, and latitude on the gut microbiota. The cytochrome C oxidase subunit I (COI) gene and 16S rRNA gene amplicons were sequenced from the feces of eight insectivorous bat species in southern China, includingMiniopterus fuliginosus,Aselliscus stoliczkanus,Myotis laniger,Rhinolophus episcopus,Rhinolophus osgoodi,Rhinolophus ferrumequinum,Rhinolophus affinis,andRhinolophus pusillus. The results showed that the composition of gut microbiome and diet exhibited significant differences among bat species. Diet composition and gut microbiota were significantly correlated at the order, family, genus, and operational taxonomic unit levels, while certain insects had a marked effect on the gut microbiome at specific taxonomic levels. In addition, elevation, latitude, body weight of bats, and host species had significant effects on the gut microbiome, but phylosymbiosis between host phylogeny and gut microbiome was lacking. These findings clarify the relationship between gut microbiome and diet and contribute to improving our understanding of host ecology and the evolution of the gut microbiome in wild mammals. IMPORTANCEThe gut microbiome is critical for the adaptation of wildlife to the dynamic environment. Bats are the second-largest group of mammals with short intestinal tract, yet their gut microbiome is still poorly studied. Herein, we explored the relationships between gut microbiome and food composition, host taxa, body size, gender, elevation, and latitude. We found a significant association between diet composition and gut microbiome in insectivorous bats, with certain insect species having major impacts on gut microbiome. Factors like species taxa, body weight, elevation, and latitude also affected the gut microbiome, but we failed to detect phylosymbiosis between the host phylogeny and the gut microbiome. Overall, our study presents novel insights into how multiple factors shape the bat’s gut microbiome together and provides a study case on host-microbe interactions in wildlife.more » « less
-
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
-
Abstract Phylosymbiosis is an association between host-associated microbiome composition and host phylogeny. This pattern can arise via the evolution of host traits, habitat preferences, diets, and the co-diversification of hosts and microbes. Understanding the drivers of phylosymbiosis is vital for modelling disease-microbiome interactions and manipulating microbiomes in multi-host systems. This study quantifies phylosymbiosis in Appalachian salamander skin in the context of infection by the fungal pathogen Batrachochytrium dendrobatidis (Bd), while accounting for environmental microbiome exposure. We sampled ten salamander species representing >150M years of divergence, assessed their Bd infection status, and analysed their skin and environmental microbiomes. Our results reveal a significant signal of phylosymbiosis, whereas the local environmental pool of microbes, climate, geography, and Bd infection load had a smaller impact. Host-microbe co-speciation was not evident, indicating that the effect stems from the evolution of host traits influencing microbiome assembly. Bd infection is correlated with host phylogeny and the abundance of Bd-inhibitory bacterial strains, suggesting that the long-term evolutionary dynamics between salamander hosts and their skin microbiomes affect the present-day distribution of the pathogen, along with habitat-linked exposure risk. Five Bd-inhibitory bacterial strains showed unusual generalism: occurring in most host species and habitats. These generalist strains may enhance the likelihood of probiotic manipulations colonising and persisting on hosts. Our results underscore the substantial influence of host-microbiome eco-evolutionary dynamics on environmental health and disease outcomes.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/femsec/fiac124
