Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades

Youngblut, Nicholas D.; Reischer, Georg H.; Walters, William A.; Schuster, Nathalie; Walzer, Chris; Stalder, Gabrielle; Ley, Ruth E.; Farnleitner, Andreas H.

doi:10.1101/484006

Cited by 99 publications

(171 citation statements)

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“…Diet and host taxonomy are major drivers of assemblies of gut microbial communities across diverse animal taxa, including insects [4][5][6][7], spiders [8], sh [9,10], frogs [11], mammals [12,13], and birds [14][15][16][17][18]. In vertebrates, most work to understand the importance of these factors stems from mammals and birds [12,17,19,20], with intriguing differences between the two [19,20]. Although microbiome composition in mammals is affected by diet [21][22][23][24][25][26], mammalian gut microbiomes are tightly associated with host phylogeny [19,20], often accompanied by taxon-speci c diets [12].…”

Section: Introductionmentioning

confidence: 99%

“…In vertebrates, most work to understand the importance of these factors stems from mammals and birds [12,17,19,20], with intriguing differences between the two [19,20]. Although microbiome composition in mammals is affected by diet [21][22][23][24][25][26], mammalian gut microbiomes are tightly associated with host phylogeny [19,20], often accompanied by taxon-speci c diets [12]. In contrast, although bird taxonomy, such as host family, is associated with certain microbiome characteristics [15,16], microbial compositions tend to not be strongly associated with host phylogeny [16,20].…”

Section: Introductionmentioning

confidence: 99%

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Flexibility and resilience of Great tit (Parus major) gut microbiomes to changing diets

Bodawatta

Freiberga

Puzejova

et al. 2020

Preprint

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Background: Gut microbial communities play important roles in nutrient management and can change in response to host diets. The extent of this flexibility and the concomitant resilience is largely unknown in wild animals. To begin untangling the dynamics of avian-gut microbiome symbiosis associated with diet changes, we exposed Parus major (Great tits) fed with a standard diet (seeds and mealworms) to either a mixed (seeds, mealworms and fruits), a seed, or a mealworm diet for four weeks, and examined the flexibility of gut microbiomes to these compositionally different diets. To assess microbiome resilience (recovery potential), all individuals were subsequently reversed to a standard diet for another four weeks. Cloacal microbiomes were collected weekly and characterised through sequencing the v4 region of the 16S rRNA gene using Illumina MiSeq. Results: Initial microbiomes changed significantly with the diet manipulation but the communities did not differ significantly between the three diet groups (mixed, seed and mealworm), despite multiple diet-specific changes of specific bacterial genera. Reverting birds to the standard diet led to only a partial recovery in gut community compositions. The majority of the bacterial taxa that increased significantly during diet manipulation decreased in relative abundances after reversion to the standard diet; however, bacterial taxa that decreased during the manipulation rarely increased after diet reversal.Conclusions: The gut microbial response and partial resilience to dietary changes support that gut bacterial communities of P. major play a role in accommodating dietary changes experienced by wild avian hosts. This may be a contributing factor to the relaxed association between microbiome composition and bird phylogeny. Our findings further imply that interpretations of wild bird gut microbiome analyses from single-time point sampling, especially for omnivorous species or species that have changing seasonal diets, should be done with caution. The partial community recovery implies that ecologically relevant diet changes (e.g., seasonality and migration) open up gut niches that may be filled by previously abundant microbes or replaced by different symbiont lineages, which has important implications for the integrity and specificity of long-term avian-symbiont associations.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Flexibility and resilience of Great tit (Parus major) gut microbiomes to changing diets

Bodawatta

Freiberga

Puzejova

et al. 2020

Preprint

View full text Add to dashboard Cite

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“…It is often challenging, however, to apply results from laboratory studies toward understanding the natural patterns of microbiome composition and structure in genetically diverse host populations exposed to spatial and temporal variability. Additionally, laboratory animals do not generally harbor microbiomes found in their wild counterparts, making it difficult to study the ecology and evolution of many host-microbe relationships 9 . Human studies can span a somewhat wider range of genetic and environmental variation, but these studies are often limited in depth due to the difficulty of collecting important covariates from healthy individuals.…”

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confidence: 99%

Bighorn sheep gut microbiomes associate with genetic and spatial structure across a metapopulation

Couch

Arnold

Crowhurst

et al. 2020

Sci Rep

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Studies in laboratory animals demonstrate important relationships between environment, host traits, and microbiome composition. However, host-microbiome relationships in natural systems are understudied. Here, we investigate metapopulation-scale microbiome variation in a wild mammalian host, the desert bighorn sheep (Ovis canadensis nelsoni). We sought to identify over-represented microbial clades and understand how landscape variables and host traits influence microbiome composition across the host metapopulation. To address these questions, we performed 16S sequencing on fecal DNA samples from thirty-nine bighorn sheep across seven loosely connected populations in the Mojave Desert and assessed relationships between microbiome composition, environmental variation, geographic distribution, and microsatellite-derived host population structure and heterozygosity. We first used a phylogenetically-informed algorithm to identify bacterial clades conserved across the metapopulation. Members of genus Ruminococcaceae, genus Lachnospiraceae, and family Christensenellaceae R7 group were among the clades over-represented across the metapopulation, consistent with their known roles as rumen symbionts in domestic livestock. Additionally, compositional variation among hosts correlated with individual-level geographic and genetic structure, and with population-level differences in genetic heterozygosity. This study identifies microbiome community variation across a mammalian metapopulation, potentially associated with genetic and geographic population structure. Our results imply that microbiome composition may diverge in accordance with landscape-scale environmental and host population characteristics.

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“…Given the long and intertwined evolutionary history between primates and their commensal microbes, understanding the factors that govern gut microbiome (GMB) composition across primate lineages has become an important research focus (Clayton et al, ; Ley et al, ; Youngblut et al, ). Particular emphasis has been given to the influences of feeding strategy, current diet, and phylogeny (Clayton et al, ).…”

Section: Introductionmentioning

confidence: 99%

“…Although often correlated, these two dietary characteristics are not invariably linked (Chapman & Chapman, ). Because feeding strategy frequently follows phylogenetic patterns, disentangling the respective roles of these factors is an ongoing challenge in GMB research (Amato et al, ; Youngblut et al, ). Nocturnal strepsirrhines, an ecologically diverse group of primates, represent a promising study system in which to comparatively examine these factors and their impact on GMB composition.…”

Section: Introductionmentioning

confidence: 99%

A comparative study of gut microbiomes in captive nocturnal strepsirrhines

Bornbusch

Greene

McKenney

et al. 2019

American J Primatol

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Feeding strategy and diet are increasingly recognized for their roles in governing primate gut microbiome (GMB) composition. Whereas feeding strategy reflects evolutionary adaptations to a host's environment, diet is a more proximate measure of food intake. Host phylogeny, which is intertwined with feeding strategy, is an additional, and often confounding factor that shapes GMBs across host lineages.Nocturnal strepsirrhines are an intriguing and underutilized group in which to examine the links between these three factors and GMB composition. Here, we compare GMB composition in four species of captive, nocturnal strepsirrhines with varying feeding strategies and phylogenetic relationships, but nearly identical diets.We use 16S rRNA sequences to determine gut bacterial composition. Despite similar husbandry conditions, including diet, we find that GMB composition varies significantly across host species and is linked to host feeding strategy and phylogeny.The GMBs of the omnivorous and the frugivorous species were significantly more diverse than were those of the insectivorous and exudativorous species. Across all hosts, GMBs were enriched for bacterial taxa associated with the macronutrient resources linked to the host's respective feeding strategy. Ultimately, the reported variation in microbiome composition suggests that the impacts of captivity and concurrent diet do not overshadow patterns of feeding strategy and phylogeny. As our understanding of primate GMBs progresses, populations of captive primates can provide insight into the evolution of host-microbe relationships, as well as inform future captive management protocols that enhance primate health and conservation.

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Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades

Cited by 99 publications

References 68 publications

Flexibility and resilience of Great tit (Parus major) gut microbiomes to changing diets

Flexibility and resilience of Great tit (Parus major) gut microbiomes to changing diets

Bighorn sheep gut microbiomes associate with genetic and spatial structure across a metapopulation

A comparative study of gut microbiomes in captive nocturnal strepsirrhines

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