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.
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
- NSF-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
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Abstract Background Inter-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.Results The 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.
Conclusions As 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.
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Abstract Objectives Environmental and ecological factors, such as geographic range, anthropogenic pressure, group identity, and feeding behavior are known to influence the gastrointestinal microbiomes of great apes. However, the influence of individual host traits such as age and sex, given specific dietary and social constraints, has been less studied. The objective of this investigation was to determine the associations between an individual's age and sex on the diversity and composition of the gut microbiome in wild western lowland gorillas.
Materials and Methods Publicly available 16S rRNA data generated from fecal samples of different groups of
Gorilla gorilla gorillan = 28) and high fruit (wet,n = 82) seasons. Microbial community analyses (alpha and beta diversity and analyses of discriminant taxa), in tandem with network‐wide approaches, were used to (a) mine for specific age and sex based differences in gut bacterial community composition and to (b) asses for gut community modularity and bacterial taxa with potential functional roles, in the context of seasonal food variation, and social group affiliation.Results Both age and sex significantly influenced gut microbiome diversity and composition in wild western lowland gorillas. However, the largest differences were observed between infants and adults in habituated groups and between adults and immature gorillas within all groups, and across dry and wet seasons. Specifically, although adults always showed greater bacterial richness than infants and immature gorillas, network‐wide analyses showed higher microbial community complexity and modularity in the infant gorilla gut. Sex‐based microbiome differences were not evident among adults, being only detected among immature gorillas.
Conclusions The results presented point to a dynamic gut microbiome in
Gorilla spp., associated with ontogeny and individual development. Of note, the gut microbiomes of breastfeeding infants seemed to reflect early exposure to complex, herbaceous vegetation. Whether increased compositional complexity of the infant gorilla gut microbiome is an adaptive response to an energy‐limited diet and an underdeveloped gut needs to be further tested. Overall, age and sex based gut microbiome differences, as shown here, maybe mainly attributed to access to specific feeding sources, and social interactions between individuals within groups. -
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
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Abstract Aim Identification of the processes that generate and maintain species diversity within the same region can provide insight into biogeographic patterns at broader spatiotemporal scales. Hawkfishes in the genus
Paracirrhites are a unique taxon to explore with respect to niche differentiation, exhibiting diagnostic differences in coloration, and an apparent center of distribution outside of the Indo–Malay–Philippine (IMP) biodiversity hotspot for coral reef fishes. Our aim is to use next‐generation sequencing methods to leverage samples of a taxon at their center of maximum diversity to explore phylogenetic relationships and a possible mechanism of coexistence.Location Flint Island, Southern Line Islands, Republic of Kiribati.
Methods A comprehensive review of museum records, the primary literature, and unpublished field survey records was undertaken to determine ranges for four “arc‐eye” hawkfish species in the
Paracirrhites species complex and a potential hybrid. Fish from fourParacirrhites species were collected from Flint Island in the Southern Line Islands, Republic of Kiribati. Hindgut contents were sequenced, and subsequent metagenomic analyses were used to assess the phylogenetic relatedness of the host fish, the microbiome community structure, and prey remains for each species.Results Phylogenetic analyses conducted with recovered mitochondrial genomes revealed clustering of
P. bicolor withP. arcatus andP. xanthus withP. nisus , which were unexpected on the basis of previous morphological work in this species complex. Differences in taxonomic composition of gut microbial communities and presumed prey remains indicate likely separation of foraging niches.Main Conclusions Our findings point toward previously unidentified relationships in this cryptic species complex at its proposed center of distribution. The three species endemic to the Polynesian province (
P. nisus ,P. xanthus , andP. bicolor ) cluster separately from the more broadly distributedP. arcatus on the basis of relative abundance of metazoan sequences in the gut (presumed prey remains). Discordance between gut microbial communities and phylogeny of the host fish further reinforce the hypothesis of niche separation.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/femsec/fiac124
