Social convergence of gut microbiomes in vampire bats

Yarlagadda, Karthik; Razik, Imran; Malhi, Ripan S.; Carter, Gerald G.

doi:10.1098/rsbl.2021.0389

Cited by 21 publications

(13 citation statements)

References 53 publications

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“…There are many potential proximate causes of microbiome stability in old age. Communal living may buffer microbiome disturbances by providing a continuous source of microbes that can be socially transmitted (85, 86, 96, 97). In our experiment, diet was kept constant, and bees appear to consume pollen even in old age based on the presence of plant DNA in metagenomes (Fig.…”

Section: Discussionmentioning

confidence: 99%

Microbiome assembly and maintenance across the lifespan of bumble bee workers

Hammer

Easton‐Calabria

Moran

2022

Preprint

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How a host’s microbiome changes over its lifespan can influence development and aging. As these temporal patterns have only been described in detail for humans and a handful of other hosts, an important next step is to compare microbiome dynamics across a broader array of host-microbe symbioses, and to investigate how and why they vary. Here we characterize the temporal dynamics and stability of the bumblebee worker gut microbiome. Bumblebees are a useful symbiosis model given their relatively well-understood life history and simple, host-specific gut bacterial communities. Furthermore, microbial dynamics may influence bumblebee health and pollination services. We combined high-temporal-resolution sampling with 16S rRNA gene sequencing, quantitative PCR, and shotgun metagenomics to characterize gut microbiomes over the adult lifespan of Bombus impatiens workers. To understand how hosts may control (or lose control of) the gut microbiome as they age, we also sequenced hindgut transcriptomes. We found that, at the community level, microbiome assembly is highly predictable and similar to patterns of primary succession observed in the human gut. At the same time, partitioning of strain-level bacterial variants among colonies suggests stochastic colonization events similar to those observed in flies and nematodes. We also find strong differences in temporal dynamics among symbiont species, suggesting ecological differences among microbiome members in colonization and persistence. Finally, we show that both the gut microbiome and host transcriptome—including expression of key immunity genes—stabilize, as opposed to senesce, with age. We suggest that in highly social groups such as bumblebees, maintenance of both microbiomes and immunity contribute to the inclusive fitness of workers, and thus remain under selection even in old age. Our findings provide a foundation for exploring the mechanisms and functional outcomes of bee microbiome succession, and for comparative analyses with other host-microbe symbioses.

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Section: Discussionmentioning

confidence: 99%

Microbiome assembly and maintenance across the lifespan of bumble bee workers

Hammer

Easton‐Calabria

Moran

2022

Preprint

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“…Evidence from Burmese pythons suggests that shifts in the postprandial gut microbiota last for many days (Costello et al, 2010), although this study did not record time sample collection, obscuring whether feeding shifted microbial rhythms as well as composition. In social or gregarious animals, microbiota are often shared (Sarkar et al, 2020) and pathogen exposure is high (Kappeler et al, 2015;McCabe et al, 2015;Yarlagadda et al, 2021). Peaks in pathogen exposure or activation of immunity may therefore not be limited to mealtimes.…”

Section: How Might Gut Microbial Rhythms Reflect Host Ecology and Evo...mentioning

confidence: 99%

“…In social or gregarious animals, microbiota are often shared (Sarkar et al, 2020) and pathogen exposure is high (Kappeler et al, 2015; McCabe et al, 2015; Yarlagadda et al, 2021). Peaks in pathogen exposure or activation of immunity may therefore not be limited to mealtimes.…”

Section: Relevance Of Microbial Oscillations To Outstanding Questions...mentioning

confidence: 99%

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

et al. 2023

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1. Daily light-dark cycles shape the circadian physiology and behaviour of nearly all organisms, with variation in circadian phenotypes having cascading effects on individual fitness, species interactions and species co-evolution.2. Recent evidence that circadian rhythms in host immunity and metabolism are synchronised by the gut microbiota suggest that the circadian dynamics of gut microbes are a crucial component of their function. However, there remains little knowledge or understanding of the diurnal dynamics of gut microbiomes in natural populations or the consequences for host physiology and ecology.3. Here, we summarise the hallmarks of gut microbiota oscillations reported to date and the mechanisms by which they synchronise rhythms in host immunity and metabolism. We outline the consequences for diverse biological processes such as host pathogen susceptibility and seasonal switches in metabolism, and discuss how the breakdown of these circadian interactions, for example during senescence or because of light pollution, may affect wildlife infection risk and disease.4. We also provide practical guidelines for the measurement of microbial oscillations in wildlife, highlighting that whilst faecal samples of wild animals are rarely available over a 24-h period, characterising even parts of the gut microbial cycle can be informative.5. An improved understanding of how gut microbial diurnal rhythms manifest in wildlife is essential to fully comprehend their role in shaping variation in host circadian phenotypes and the consequences for host physiology and ecology.

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“…Social environment has been shown to play an important role in microbiome composition, as skin and gut bacterial communities reflect group membership and social networks in several mammalian (Song et al, 2013;Theis et al, 2013;Leclaire et al, 2014;Tung et al, 2015;Moeller et al, 2016;Yarlagadda et al, 2021) and avian (Kulkarni and Heeb, 2007;Ruiz-Rodríguez et al, 2014;Whittaker et al, 2016;Goodenough et al, 2017;Engel, et al, 2020) species. Indeed, behaviors that promote the transmission of beneficial microbes have been documented in several animal species, such as overmarking or allomarking in scent-marking animals (Buesching et al, 2003;Theis et al, 2008) and coprophagy (Osawa et al, 1993;Kobayashi et al, 2019), though microbe transmission can occur through other social behaviors like grooming and play (Meadow et al, 2013;Perofsky et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Effects of short-term experimental manipulation of captive social environment on uropygial gland microbiome and preen oil volatile composition

Whittaker

Atyam

Burroughs³

et al. 2023

Front. Ecol. Evol.

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IntroductionAvian preen oil, secreted by the uropygial gland, is an important source of volatile compounds that convey information about the sender’s identity and quality, making preen oil useful for the recognition and assessment of potential mates and rivals. Although intrinsic factors such as hormone levels, genetic background, and diet can affect preen oil volatile compound composition, many of these compounds are not the products of the animal’s own metabolic processes, but rather those of odor-producing symbiotic microbes. Social behavior affects the composition of uropygial microbial communities, as physical contact results in microbe sharing. We experimentally manipulated social interactions in captive dark-eyed juncos (Junco hyemalis) to assess the relative influence of social interactions, subspecies, and sex on uropygial gland microbial composition and the resulting preen oil odor profiles.MethodsWe captured 24 birds at Mountain Lake Biological Station in Virginia, USA, including birds from two seasonally sympatric subspecies – one resident, one migratory. We housed them in an outdoor aviary in three phases of social configurations: first in same-sex, same-subspecies flocks, then in male-female pairs, and finally in the original flocks. Using samples taken every four days of the experiment, we characterized their uropygial gland microbiome through 16S rRNA gene sequencing and their preen oil volatile compounds via GC-MS.ResultsWe predicted that if social environment was the primary driver of uropygial gland microbiome composition, and if microbiome composition in turn affected preen oil volatile profiles, then birds housed together would become more similar over time. Our results did not support this hypothesis, instead showing that sex and subspecies were stronger predictors of microbiome composition. We observed changes in volatile compounds after the birds had been housed in pairs, which disappeared after they were moved back into flocks, suggesting that hormonal changes related to breeding condition were the most important factor in these patterns.DiscussionAlthough early life social environment of nestlings and long-term social relationships have been shown to be important in shaping uropygial gland microbial communities, our study suggests that shorter-term changes in social environment do not have a strong effect on uropygial microbiomes and the resulting preen oil volatile compounds.

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Social convergence of gut microbiomes in vampire bats

Cited by 21 publications

References 53 publications

Microbiome assembly and maintenance across the lifespan of bumble bee workers

Microbiome assembly and maintenance across the lifespan of bumble bee workers

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

Effects of short-term experimental manipulation of captive social environment on uropygial gland microbiome and preen oil volatile composition

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