Circadian rhythms of hosts and their gut microbiomes: Implications for animal physiology and ecology

Schmid, Dominik W.; Capilla‐Lasheras, Pablo; Dominoni, Davide M.; Müller‐Klein, Nadine; Sommer, Simone; Risely, Alice

doi:10.1111/1365-2435.14255

Cited by 5 publications

(7 citation statements)

References 118 publications

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“…Such processes in shorebirds are also observed during summer weight gain in hibernating bears, highlighting the influence of the microbiome in shaping core survival processes of multiple host species (Sommer et al 2016 ). These data thus support the hypothesis that the migratory process is a disturbance, albeit an extreme one, leading to changes in the selective pressures on a community, which in turn result in compositional shifts in the microbiota (Schmid et al 2023 ). Nonetheless, as stated above, with successive migratory events the ‘average’ habitat becomes closer to the migratory habitat—which may result in movement-associated changes falling within the intermediate disturbance hypothesis.…”

Section: Introductionsupporting

confidence: 83%

“…Although microbial communities are highly dynamic, and have been observed to undergo daily (Zarrinpar et al 2014 , Zhang et al 2023 ) or seasonal cycles (Huang et al 2022 , Schmid et al 2023 ), there remains strong evidence for priority effects on microbial communities (Martínez et al 2018 , Leopold and Busby 2020 ). However, the influence of priority effects may be linked to both the degree of disturbance induced by long distance movements (e.g.…”

Section: A Framework For Microbiome Interactions With Long-distance M...mentioning

confidence: 99%

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Long-distance movement dynamics shape host microbiome richness and turnover

Pearman,

Duffy,

Gemmell

et al. 2024

FEMS Microbiology Ecology

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Host-associated microbial communities are shaped by host migratory movements. These movements can have contrasting impacts on microbiota, and understanding such patterns can provide insight into the ecological processes that contribute to community diversity. Furthermore, long-distance movements to new environments are anticipated to occur with increasing frequency due to host distribution shifts resulting from climate change. Understanding how hosts transport their microbiota with them could be of importance when examining biological invasions. Although microbial community shifts are well-documented, the underlying mechanisms that lead to the restructuring of these communities remain relatively unexplored. Using literature and ecological simulations, we develop a framework to elucidate the major factors that lead to community change. We group host movements into two types—regular (repeated/cyclical migratory movements, as found in many birds and mammals) and irregular (stochastic/infrequent movements that do not occur on a cyclical basis, as found in many insects and plants). Ecological simulations and prior research suggest that movement type and frequency, alongside environmental exposure (e.g. internal/external microbiota) are key considerations for understanding movement-associated community changes. From our framework, we derive a series of testable hypotheses, and suggest means to test them, to facilitate future research into host movement and microbial community dynamics.

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Section: Introductionsupporting

confidence: 83%

Section: A Framework For Microbiome Interactions With Long-distance M...mentioning

confidence: 99%

Long-distance movement dynamics shape host microbiome richness and turnover

Pearman,

Duffy,

Gemmell

et al. 2024

FEMS Microbiology Ecology

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“…For example, a study on wild meerkats showed that diurnal shifts in GM composition outweighed an association between the GM and host chronological age [33]. Circadian GM dynamics have been identi ed in human and wild animal studies, and may be driven by differences in foraging regimes and dietary intake throughout the day [33,92]. In the Seychelles warbler, the genera Lactococcus and Enterococcus showed the largest increases in abundance between samples collected in the morning and afternoon.…”

Section: Discussionmentioning

confidence: 99%

“…In the Seychelles warbler, the genera Lactococcus and Enterococcus showed the largest increases in abundance between samples collected in the morning and afternoon. Both genera are lactic acid producing bacteria and play an important role in dietary carbohydrate fermentation [93]; as such, these genera may gradually increase in response to an in ux of nutrients as individuals start to forage [92]. However, both genera are also found in insect microbiomes [94][95][96] and so it is possible that these taxa accumulate passively as feeding increases throughout the day and are mainly transient colonisers of the GM that don't carry out a fermentative function.…”

Section: Discussionmentioning

confidence: 99%

Assessing longitudinal gut microbiome dynamics in relation to age and senescence in a wild animal population

Worsley,

Davies,

Lee

et al. 2023

Preprint

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Background In humans, gut microbiome (GM) differences are often correlated with, and sometimes causally implicated in, ageing. However, it is unclear how these findings translate in wild animal populations. Furthermore, studies that investigate how GM dynamics change within individuals (as opposed to among individuals), and with declines in physiological condition, are needed to fully understand links between chronological age, senescence, and the GM, but have rarely been done. Here, we use longitudinal data collected from a closed population of Seychelles warblers (Acrocephalus sechellensis) to investigate how bacterial GM alpha diversity, composition, and stability are associated with chronological age and the year leading up to death. We hypothesise that GM diversity and composition will differ, and variability will increase, in older adults, particularly in the terminal year prior to death, as it becomes dysregulated due to host senescence. Results GM alpha diversity and composition remained largely invariable with respect to adult age and did not differ in an individual’s terminal year. Furthermore, there was no evidence that the GM became more heterogenous in senescent age groups (individuals older than 6 years), or in the terminal year. Instead, environmental variables such as season, territory quality, and time of day, were the strongest predictors of GM variation in adult Seychelles warblers. Conclusion We found no evidence to suggest that host senescence is associated with GM restructuring within a natural population. This contrasts with studies on humans, captive animal populations, and some (but not all) studies on non-human primates, suggesting that GM deterioration may not be a universal hallmark of senescence in wild animal species. Further work is needed to disentangle the factors driving variation in GM-senescence relationships across different host taxa.

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“…Data on infection intensity may help distinguish between chronic and acute infections, which is relevant for shaping the type of immune response mounted by the host. Similarly, the order of infections may play a role in how sequentially co-infecting pathogens interact with each other, host immunity and microbiota (Halliday et al, 2017), and certain immune parameters are particularly important for host control over both the gut microbiota and pathogen dynamics (Schmid et al, 2023). Bank voles are an ideal model organism to study these processes experimentally and in the wild because they host a range of pathogens, which differ in the duration and intensity of infection and their transmission ecology, including those that are likely co-transmitted or sequentially transmitted from the same vector (Moutailler et al, 2016).…”

mentioning

confidence: 99%

Co‐infections mask pathogen‐specific associations with the gut microbiota in wild voles

Schmid¹,

Risely

2023

Journal of Animal Ecology

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Animals and plants harbour complex suites of microbes that span the parasitism-mutualism continuum. To date, microbiomes have largely been studied in the context of their interactions with host biology (e.g. host diet or genotype), yet interactions between microbes themselves have profound consequences for host fitness (Gould et al., 2018), disease progression (O'Keeffe et al., 2021), and pathogen evolution and emergence (Drew et al., 2021;Frederickson & Reese, 2021). Pathogenic microbes are particularly important for shaping interaction networks because they are often uniquely able to suppress competitors (Amaro & Martín-González, 2021) and can hijack the host immune system in a way that affects target and non-target microbes (Kamada et al., 2013). Among studies that characterize interactions between commensal and pathogenic microbes, most explore the effect of single pathogens. In nature, however, co-infections with multiple pathogens are the rule rather than the exception (Hoarau et al., 2020). Generalizing microbial interactions in the face of such complexity remains a major challenge, yet is essential to advance our understanding of how host-associated microbiomes shape host ecology and evolution.In their recent publication in the Journal of Animal Ecology, Brila et al. (2022) investigate associations between co-infecting pathogens and commensal gut microbes in wild bank voles Myodes glareolus. The authors pair surveillance data on four systemic pathogenic microbes (two bacterial, one protozoan, and one viral) with faecal

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Circadian rhythms of hosts and their gut microbiomes: Implications for animal physiology and ecology

Cited by 5 publications

References 118 publications

Long-distance movement dynamics shape host microbiome richness and turnover

Long-distance movement dynamics shape host microbiome richness and turnover

Assessing longitudinal gut microbiome dynamics in relation to age and senescence in a wild animal population

Co‐infections mask pathogen‐specific associations with the gut microbiota in wild voles

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