Microbiomes as Metacommunities: Understanding Host-Associated Microbes through Metacommunity Ecology

Miller, Elizabeth T.; Svanbäck, Richard; Bohannan, Brendan J. M.

doi:10.1016/j.tree.2018.09.002

Cited by 203 publications

(220 citation statements)

References 70 publications

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“…Assuming our results hold across epiphytic microbial species to some degree, bee-mediated dispersal would also affect microbial diversity (Allard et al 2018, Miller et al 2018. Indeed, given that nearly all bumble bees dispersed microbes to the corolla and the corolla received the most microbes, our results are consistent with studies showing that the corolla typically hosts more microbial diversity than the pistil and stamens (Junker et al 2011, Pozo et al 2012, Junker and Keller 2015.…”

Section: Discussionsupporting

confidence: 87%

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Movers and shakers: Bumble bee foraging behavior shapes the dispersal of microbes among and within flowers

et al. 2019

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Dispersal is central to the ecology and evolution of spatially structured communities. While flower microbial communities are spatially structured among floral organs, how dispersal vectors distribute microbes among floral organs is unknown. Pollinators are recognized as key microbial vectors, but effects of their different foraging behaviors on transfer dynamics among flowers or different floral organs are not known. We asked how foraging behaviors of a model pollinator (Bombus impatiens) affect acquisition and dispersal of microbes among flower organs. We used monkeyflowers (Mimulus guttatus) to examine dispersal within a natural context and artificial flowers to test how common bee foraging behaviors (nectaring, buzzing, or scrabbling) shaped dispersal of a green fluorescent protein‐labeled bacteria, Pseudomonas fluorescens. Bees acquired 1% of a flower's microbes and dispersed 31% of acquired microbes to the next flower. All bees acquired microbes, and 85% and 76% of bees dispersed microbes to live and artificial flowers, respectively. Microbes acquired from the corolla were mainly deposited on the corolla, followed by the stamens, and least on the nectary/pistil. Bee foraging behavior affected acquisition, with scrabbling for pollen resulting in 23% more microbes acquired than nectaring, and with buzzing for pollen resulting in a 79% slower rate of microbial acquisition relative to scrabbling. Bee foraging behavior also affected deposition but depended on the floral organ: Scrabbling and buzzing for pollen led to greater deposition than nectaring for corolla and stamen but not nectary. Our results have implications for transmission of beneficial and pathogenic microbes among plants and pollinators, and thus the ecology and evolution of floral microbial communities.

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Section: Discussionsupporting

confidence: 87%

“…, Miller et al. ). Indeed, given that nearly all bumble bees dispersed microbes to the corolla and the corolla received the most microbes, our results are consistent with studies showing that the corolla typically hosts more microbial diversity than the pistil and stamens (Junker et al.…”

Section: Discussionmentioning

confidence: 99%

Movers and shakers: Bumble bee foraging behavior shapes the dispersal of microbes among and within flowers

et al. 2019

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“…While the effects of substrate on the fly microbiome are well described (Chandler et al ., ; Staubach et al ., ; Wang and Staubach, ), continental‐scale effects of temperature on a host‐associated microbiome has, to our knowledge, not been described before. Temperature affects environmental microbiomes on a global scale (Zhou et al ., ; Thompson et al ., ) and the effect in Drosophila might reflect the exposure of flies to different environmental microbiomes, supporting a model in which the environmental metacommunities differ and affect composition of the host‐associated community (Adair and Douglas, ; Miller et al ., ). The correlation with monthly temperature at the collection date only showed a non‐significant trend ( P = 0.065).…”

Section: Discussionmentioning

confidence: 97%

“…At the same time, highly specific host genotype‐dependent interactions with the microbiome seem to be at work. This is consistent with newly developed models that combine environmental effects and host feedback on the metacommunity (Adair and Douglas, ) with dispersal and colonization dynamics (Miller et al ., ).…”

Section: Introductionmentioning

confidence: 97%

Common structuring principles of the Drosophila melanogaster microbiome on a continental scale and between host and substrate

Wang

Kapun

Waidele

et al. 2020

Environ Microbiol Rep

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Summary The relative importance of host control, environmental effects and stochasticity in the assemblage of host‐associated microbiomes is being debated. We analysed the microbiome among fly populations that were sampled across Europe by the European Drosophila Population Genomics Consortium (DrosEU). In order to better understand the structuring principles of the natural D. melanogaster microbiome, we combined environmental data on climate and food‐substrate with dense genomic data on host populations and microbiome profiling. Food‐substrate, temperature, and host population structure correlated with microbiome structure. Microbes, whose abundance was co‐structured with host populations, also differed in abundance between flies and their substrate in an independent survey. This finding suggests common, host‐related structuring principles of the microbiome on different spatial scales.

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“…This maternal selection of bacteria influences the first bacteria that will be in contact with the sterile larvae during hatching (Llewellyn, Boutin, Hoseinifar, & Derome, ). Clearly then, a holistic understanding of macro‐organisms biodiversity requires the investigation of their association with microbiota and their co‐evolution (Miller, Svanbäck, & Bohannan, ).…”

Section: Introductionmentioning

confidence: 99%

Evidence for host effect on the intestinal microbiota of whitefish (Coregonus sp.) species pairs and their hybrids

Sevellec

Laporte

Bernatchez

et al. 2019

Ecology and Evolution

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Investigating relationships between microbiota and their host is essential toward a full understanding of how animal adapt to their environment. Lake Whitefish offers a powerful system to investigate processes of adaptive divergence where the dwarf, limnetic species evolved repeatedly from the normal, benthic species. We compared the transient intestinal microbiota between both species from the wild and in controlled conditions, including their reciprocal hybrids. We sequenced the 16s rRNA gene V3‐V4 regions to (a) test for parallelism in the transient intestinal microbiota among sympatric pairs, (b) test for transient intestinal microbiota differences among dwarf, normal, and hybrids reared under identical conditions, and (c) compare intestinal microbiota between wild and captive whitefish. A significant host effect on microbiota taxonomic composition was observed when all lakes were analyzed together and in three of the five species pairs. In captive whitefish, host effect was also significant. Microbiota of both reciprocal hybrids fell outside of that observed in the parental forms. Six genera formed a bacterial core which was present in captive and wild whitefish, suggesting a horizontal microbiota transmission. Altogether, our results complex interactions among the host, the microbiota, and the environment, and we propose that these interactions define three distinct evolutionary paths of the intestinal microbiota.

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Microbiomes as Metacommunities: Understanding Host-Associated Microbes through Metacommunity Ecology

Cited by 203 publications

References 70 publications

Movers and shakers: Bumble bee foraging behavior shapes the dispersal of microbes among and within flowers

Movers and shakers: Bumble bee foraging behavior shapes the dispersal of microbes among and within flowers

Common structuring principles of the Drosophila melanogaster microbiome on a continental scale and between host and substrate

Evidence for host effect on the intestinal microbiota of whitefish (Coregonus sp.) species pairs and their hybrids

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