Morphological and genetic factors shape the microbiome of a seabird species (Oceanodroma leucorhoa) more than environmental and social factors

Pearce, Douglas S.; Hoover, Brian A.; Jennings, Sarah L.; Nevitt, Gabrielle A.; Docherty, Kathryn M.

doi:10.1186/s40168-017-0365-4

Cited by 70 publications

(91 citation statements)

References 101 publications

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“…The heritability of the avian microbiome, and especially in these species, is unknown but there are several pieces of evidence to support that the microbiome may be at least partially heritable. First, there is a negative correlation between genetic distance and microbiome similarity in multiple bird species (e.g., Banks, Cary, & Hogg, ; Pearce, Hoover, Jennings, Nevitt, & Docherty, ), indicating that host genetics exert some control on the microbiome. Second, the members of the microbiome are not a random sample of the environment and this selection, whether direct or indirect, is a property that may be vertically transmitted.…”

Section: Discussionmentioning

confidence: 99%

Evolutionary signal in the gut microbiomes of 74 bird species from Equatorial Guinea

et al. 2020

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How the microbiome interacts with hosts across evolutionary time is poorly understood. Data sets including many host species are required to conduct comparative analyses. Here, we analyzed 142 intestinal microbiome samples from 92 birds belonging to 74 species from Equatorial Guinea, using the 16S rRNA gene. Using four definitions for microbial taxonomic units (97%OTU, 99%OTU, 99%OTU with singletons removed, ASV), we conducted alpha and beta diversity analyses. We found that raw abundances and diversity varied between the data sets but relative patterns were largely consistent across data sets. Host taxonomy, diet and locality were significantly associated with microbiomes, at generally similar levels using three distance metrics. Phylogenetic comparative methods assessed the evolutionary relationship between the microbiome as a trait of a host species and the underlying bird phylogeny. Using multiple ways of defining “microbiome traits”, we found that a neutral Brownian motion model did not explain variation in microbiomes. Instead, we found a White Noise model (indicating little phylogenetic signal), was most likely. There was some support for the Ornstein‐Uhlenbeck model (that invokes selection), but the level of support was similar to that of a White Noise simulation, further supporting the White Noise model as the best explanation for the evolution of the microbiome as a trait of avian hosts. Our study demonstrated that both environment and evolution play a role in the gut microbiome and the relationship does not follow a neutral model; these biological results are qualitatively robust to analytical choices.

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Section: Discussionmentioning

confidence: 99%

Evolutionary signal in the gut microbiomes of 74 bird species from Equatorial Guinea

et al. 2020

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“…Most of the associations between MHC and microbiota were detected in neck and preen feathers, but not in dorsal and ventral feathers. Similarly, in the Leach's storm petrel ( Oceanodroma leucorhoa ), a species phylogenetically closely related to the blue petrel, MHC is associated with microbiota of the preen gland area, but not with that of the brood patch (Pearce et al, ). Compared to ventral and dorsal feathers, neck feathers are highly coated with preen secretions (Supporting information Figure ), which might suggest that the covariation between MHC and neck feather microbiota arises from a proximal mechanism originating in preen secretions.…”

Section: Discussionmentioning

confidence: 99%

“…Multiple studies in mice, rats, fish and humans have found covariation between MHC variation and the composition of bacterial communities in the gut (Bolnick et al, ; Kubinak et al, ; Lanyon et al, ; Lin et al, ; Toivanen, Vaahtovuo, & Eerola, ), but only a single study has so far focused on plumage microbiota (Pearce, Hoover, Jennings, Nevitt, & Docherty, ). To test the potential role of plumage microbiota in the production of MHC–odour signals, we therefore set out to test whether (a) within‐individual MHC diversity and (b) the degree of MHC dissimilarity between individuals correlated with plumage microbiota assemblage in blue petrels ( Halobaena caerulea ).…”

Section: Introductionmentioning

confidence: 99%

Plumage microbiota covaries with the major histocompatibility complex in blue petrels

et al. 2019

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To increase fitness, a wide range of vertebrates preferentially mate with partners that are dissimilar at the major histocompatibility complex (MHC) or that have high MHC diversity. Although MHC often can be assessed through olfactory cues, the mechanism by which MHC genes influence odour remains largely unclear. MHC class IIB molecules, which enable recognition and elimination of extracellular bacteria, have been suggested to influence odour indirectly by shaping odour‐producing microbiota, i.e. bacterial communities. However, there is little evidence of the predicted covariation between an animal's MHC genotype and its bacterial communities in scent‐producing body surfaces. Here, using high‐throughput sequencing, we tested the covariation between MHC class IIB genotypes and feather microbiota in the blue petrel (Halobaena caerulea), a seabird with highly developed olfaction that has been suggested to rely on oduor cues during an MHC‐based mate choice. First, we show that individuals with similar MHC class IIB profiles also have similar bacterial assemblages in their feathers. Then, we show that individuals with high MHC diversity have less diverse feather microbiota and also a reduced abundance of a bacterium of the genus Arsenophonus, a genus in which some species are symbionts of avian ectoparasites. Our results, showing that feather microbiota covary with MHC, are consistent with the hypothesis that individual MHC genotype may shape the semiochemical‐producing microbiota in birds.

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“…Alternatively, genetic variation may encode variable responses in the host immune system to microbes in the environment. In other species, polymorphism in immunity-related genes has been found to affect microbiome composition (Bolnick et al, 2014;Kubinak et al, 2015;Pearce et al, 2017) and responses to pathogenic bacteria (Lazzaro, Sceurman, & Clark, 2004). In addition, genotype-specific immune response, and varying gene expression patterns in response to a potentially pathogenic bacteria, have been observed in the coral Acropora millepora (Wright et al, 2017).…”

Section: Host Genotypementioning

confidence: 99%

“…However, given the strength of host identity in structuring the microbiome, genetic variation within the species may also be significant. Indeed, host genotype influences microbiome composition in several systems, including plants (Wagner et al, 2016), fish (Uren Webster, Consuegra, Hitchings, & Garcia de Leaniz, 2018), amphibians (Griffiths et al, 2018), birds (Pearce, Hoover, Jennings, Nevitt, & Docherty, 2017) and mammals (Benson et al, 2010;Goodrich et al, 2014). However, host genotype and microbial variation have not yet been linked in sponges.…”

Section: Introductionmentioning

confidence: 99%

Host genetics and geography influence microbiome composition in the spongeIrcinia campana

Griffiths

Antwis

Lenzi

et al. 2019

Journal of Animal Ecology

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Marine sponges are hosts to large, diverse communities of microorganisms. These microbiomes are distinct among sponge species and from seawater bacterial communities, indicating a key role of host identity in shaping its resident microbial community. However, the factors governing intraspecific microbiome variability are underexplored and may shed light on the evolutionary and ecological relationships between host and microbiome.Here, we examined the influence of genetic variation and geographic location on the composition of the Ircinia campana microbiome.We developed new microsatellite markers to genotype I. campana from two locations in the Florida Keys, USA, and characterized their microbiomes using V4 16S rRNA amplicon sequencing.We show that microbial community composition and diversity is influenced by host genotype, with more genetically similar sponges hosting more similar microbial communities. We also found that although I. campana was not genetically differentiated between sites, microbiome composition differed by location.Our results demonstrate that both host genetics and geography influence the composition of the sponge microbiome. Host genotypic influence on microbiome composition may be due to stable vertical transmission of the microbial community from parent to offspring, making microbiomes more similar by descent. Alternatively, sponge genotypic variation may reflect variation in functional traits that influence the acquisition of environmental microbes. This study reveals drivers of microbiome variation within and among locations, and shows the importance of intraspecific variability in mediating eco‐evolutionary dynamics of host‐associated microbiomes.

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Morphological and genetic factors shape the microbiome of a seabird species (Oceanodroma leucorhoa) more than environmental and social factors

Cited by 70 publications

References 101 publications

Evolutionary signal in the gut microbiomes of 74 bird species from Equatorial Guinea

Evolutionary signal in the gut microbiomes of 74 bird species from Equatorial Guinea

Plumage microbiota covaries with the major histocompatibility complex in blue petrels

Host genetics and geography influence microbiome composition in the spongeIrcinia campana

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