Social groups constrain the spatiotemporal dynamics of wild sifaka gut microbiomes

Perofsky, Amanda C.; Meyers, Lauren Ancel; Abondano, Laura A.; Fiore, Anthony Di; Lewis, Rebecca J.

doi:10.1111/mec.16193

Cited by 23 publications

(30 citation statements)

References 108 publications

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“…On average, individuals were more similar to themselves over time than to other individuals sampled simultaneously. This is in contrast to recent findings from group-living primates, which showed spatiotemporal dynamics at the group rather than individual level ( Perofsky et al, 2021 ). Such individuality could be explained by genetic differences ( Benson et al, 2010 ), or persistent environmental or behavioural differences, for example, in habitat, dietary preferences or parasite burden.…”

Section: Discussioncontrasting

confidence: 99%

Synchronous Seasonality in the Gut Microbiota of Wild Mouse Populations

et al. 2022

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The gut microbiome performs many important functions in mammalian hosts, with community composition shaping its functional role. However, the factors that drive individual microbiota variation in wild animals and to what extent these are predictable or idiosyncratic across populations remains poorly understood. Here, we use a multi-population dataset from a common rodent species (the wood mouse, Apodemus sylvaticus), to test whether a consistent “core” gut microbiota is identifiable in this species, and to what extent the predictors of microbiota variation are consistent across populations. Between 2014 and 2018 we used capture-mark-recapture and 16S rRNA profiling to intensively monitor two wild wood mouse populations and their gut microbiota, as well as characterising the microbiota from a laboratory-housed colony of the same species. Although the microbiota was broadly similar at high taxonomic levels, the two wild populations did not share a single bacterial amplicon sequence variant (ASV), despite being only 50km apart. Meanwhile, the laboratory-housed colony shared many ASVs with one of the wild populations from which it is thought to have been founded decades ago. Despite not sharing any ASVs, the two wild populations shared a phylogenetically more similar microbiota than either did with the colony, and the factors predicting compositional variation in each wild population were remarkably similar. We identified a strong and consistent pattern of seasonal microbiota restructuring that occurred at both sites, in all years, and within individual mice. While the microbiota was highly individualised, some seasonal convergence occurred in late winter/early spring. These findings reveal highly repeatable seasonal gut microbiota dynamics in multiple populations of this species, despite different taxa being involved. This provides a platform for future work to understand the drivers and functional implications of such predictable seasonal microbiome restructuring, including whether it might provide the host with adaptive seasonal phenotypic plasticity.

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Section: Discussioncontrasting

confidence: 99%

Synchronous Seasonality in the Gut Microbiota of Wild Mouse Populations

et al. 2022

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“…In our study population, individual identity explained the largest part of the variance in gut bacterial composition, and samples collected from the same host were more similar than samples from different hosts. The small effect size of the intra- vs. interindividual comparison is consistent with previous results showing that personal signature is less obvious when samples collected from the same individuals long apart in time are compared with samples collected in the same period from different individuals [ 35 , 43 ].…”

Section: Discussionsupporting

confidence: 90%

“…Host identity arises as a strong predictor of microbiota composition [ 15 , 32 , 40 , 41 , 43 , 45 , 53 – 57 ], diversity, and even stability [ 11 , 41 , 54 , 58 , 59 ] in both humans and nonhuman animals. In our study population, individual identity explained the largest part of the variance in gut bacterial composition, and samples collected from the same host were more similar than samples from different hosts.…”

Section: Discussionmentioning

confidence: 99%

“…The rapid increase in intraindividual composition dissimilarity in our study aligns with findings in humans showing that samples collected a week apart were not more similar than those collected 3 months apart [ 58 ] rather than with evidence of a constant signature [ 56 ]. In humans, antibiotic medication may be a prominent cause of bacterial turnover [ 58 , 63 ], whereas in wild nonhuman primates, natural environmental factors may cause the rapid decrease in individual microbiota signature [ 43 , 59 ]. For example, season had the second most important influence on composition in our subjects, reflecting the previously established influence of diet, rainfall, or circadian rhythms on the microbiota [ 24 , 40 ].…”

Section: Discussionmentioning

confidence: 99%

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Aging gut microbiota of wild macaques are equally diverse, less stable, but progressively personalized

et al. 2022

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Background Pronounced heterogeneity of age trajectories has been identified as a hallmark of the gut microbiota in humans and has been explained by marked changes in lifestyle and health condition. Comparatively, age-related personalization of microbiota is understudied in natural systems limiting our comprehension of patterns observed in humans from ecological and evolutionary perspectives. Results Here, we tested age-related changes in the diversity, stability, and composition of the gut bacterial community using 16S rRNA gene sequencing with dense repeated sampling over three seasons in a cross-sectional age sample of adult female Assamese macaques (Macaca assamensis) living in their natural forest habitat. Gut bacterial composition exhibited a personal signature which became less stable as individuals aged. This lack of stability was not explained by differences in microbiota diversity but rather linked to an increase in the relative abundance of rare bacterial taxa. The lack of age-related changes in core taxa or convergence with age to a common state of the community hampered predicting gut bacterial composition of aged individuals. On the contrary, we found increasing personalization of the gut bacterial composition with age, indicating that composition in older individuals was increasingly divergent from the rest of the population. Reduced direct transmission of bacteria resulting from decreasing social activity may contribute to, but not be sufficient to explain, increasing personalization with age. Conclusions Together, our results challenge the assumption of a constant microbiota through adult life in a wild primate. Within the limits of this study, the fact that increasing personalization of the aging microbiota is not restricted to humans suggests the underlying process to be evolved instead of provoked only by modern lifestyle of and health care for the elderly.

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“…Time spent in close proximity offers opportunities for transfer of gut microbiota, such as through grooming and coprophagy (Graczyk & Cranfield, 2003). An effect of social association on the gut microbiome has previously been identified for a range of primates, including chimpanzees (Degnan et al, 2012;Moeller et al, 2016), baboons (Tung et al, 2015), colobus monkeys (Wikberg et al, 2020), black howler monkeys (Amato et al, 2017), sifakas (Perofsky et al, 2017(Perofsky et al, , 2021, and humans (Dill-McFarland et al, 2019), as well as other group-living animals, e.g. bighorn sheep (Couch et al, 2020).…”

Section: Gut Microbiome Differs Between Populations and Social Groupsmentioning

confidence: 98%

Isolated Grauer’s gorilla populations differ in diet and gut microbiome

Michel

Minocher

Niehoff

et al. 2022

Preprint

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Conservation efforts tend to focus on populations that are genetically differentiated without paying attention to their ecological differentiation. However, isolated populations may be ecologically unique, an important aspect for the design of appropriate conservation measures for endangered species. Here we investigate the interplay between diet and gut microbiome in several geographically isolated and genetically differentiated populations of the critically endangered Grauer's gorilla. We find that dietary and gut microbial profiles are population-specific, likely due to geographic isolation and environmental differences. In addition, social groups within each population also differed in diet and, to a lesser extent, in gut microbial composition and diversity. Individuals at low elevation consumed a larger variety of plant taxa than those at high elevation, consistent with the notion that dietary choice is constrained by food availability that changes with elevation. Despite no detectable correlation between the diet and gut microbiome in richness or evenness, dietary and gut microbial composition covaried significantly. As we did not find evidence for an effect of genetic relatedness on the composition of the gut microbiome of Grauer's gorillas, this pattern is likely a result of long-term social, ecological, and geographic factors acting on both diet and microbiome. These results reveal that isolated and genetically distinct populations of Grauer's gorillas are also ecologically distinct, highlighting the need to dedicate separate conservation efforts for each population.

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Social groups constrain the spatiotemporal dynamics of wild sifaka gut microbiomes

Cited by 23 publications

References 108 publications

Synchronous Seasonality in the Gut Microbiota of Wild Mouse Populations

Synchronous Seasonality in the Gut Microbiota of Wild Mouse Populations

Aging gut microbiota of wild macaques are equally diverse, less stable, but progressively personalized

Isolated Grauer’s gorilla populations differ in diet and gut microbiome

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