Evidence of phylosymbiosis in Formica ants

IntroductionInsects share intimate relationships with microbes that play important roles in their biology. Yet our understanding of how host-bound microbial communities assemble and perpetuate over evolutionary time is limited. Ants host a wide range of microbes with diverse functions and are an eme...

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Main Authors: Raphaella Jackson, Patapios A. Patapiou, Gemma Golding, Heikki Helanterä, Chloe K. Economou, Michel Chapuisat, Lee M. Henry
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-05-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1044286/full
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author Raphaella Jackson
Patapios A. Patapiou
Patapios A. Patapiou
Gemma Golding
Heikki Helanterä
Heikki Helanterä
Chloe K. Economou
Michel Chapuisat
Lee M. Henry
author_facet Raphaella Jackson
Patapios A. Patapiou
Patapios A. Patapiou
Gemma Golding
Heikki Helanterä
Heikki Helanterä
Chloe K. Economou
Michel Chapuisat
Lee M. Henry
author_sort Raphaella Jackson
collection DOAJ
description IntroductionInsects share intimate relationships with microbes that play important roles in their biology. Yet our understanding of how host-bound microbial communities assemble and perpetuate over evolutionary time is limited. Ants host a wide range of microbes with diverse functions and are an emerging model for studying the evolution of insect microbiomes. Here, we ask whether phylogenetically related ant species have formed distinct and stable microbiomes.MethodsTo answer this question, we investigated the microbial communities associated with queens of 14 Formica species from five clades, using deep coverage 16S rRNA amplicon sequencing.ResultsWe reveal that Formica species and clades harbor highly defined microbial communities that are dominated by four bacteria genera: Wolbachia, Lactobacillus, Liliensternia, and Spiroplasma. Our analysis reveals that the composition of Formica microbiomes mirrors the phylogeny of the host, i.e., phylosymbiosis, in that related hosts harbor more similar microbial communities. In addition, we find there are significant correlations between microbe co-occurrences.DiscussionOur results demonstrate Formica ants carry microbial communities that recapitulate the phylogeny of their hosts. Our data suggests that the co-occurrence of different bacteria genera may at least in part be due to synergistic and antagonistic interactions between microbes. Additional factors potentially contributing to the phylosymbiotic signal are discussed, including host phylogenetic relatedness, host-microbe genetic compatibility, modes of transmission, and similarities in host ecologies (e.g., diets). Overall, our results support the growing body of evidence that microbial community composition closely depends on the phylogeny of their hosts, despite bacteria having diverse modes of transmission and localization within the host.
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spelling doaj.art-7fe3d240a1704612b278f4738f0b07c42023-05-05T05:26:34ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-05-011410.3389/fmicb.2023.10442861044286Evidence of phylosymbiosis in Formica antsRaphaella Jackson0Patapios A. Patapiou1Patapios A. Patapiou2Gemma Golding3Heikki Helanterä4Heikki Helanterä5Chloe K. Economou6Michel Chapuisat7Lee M. Henry8School of Biological and Behavioural Sciences, Queen Mary University of London, London, United KingdomSchool of Biological and Behavioural Sciences, Queen Mary University of London, London, United KingdomDepartment of Pathobiology and Population Sciences, Royal Veterinary College, Hatfield, United KingdomSchool of Biological and Behavioural Sciences, Queen Mary University of London, London, United KingdomEcology and Genetics Research Unit, University of Oulu, Oulu, FinlandTvärminne Zoological Station, University of Helsinki, Hanko, FinlandSchool of Biological and Behavioural Sciences, Queen Mary University of London, London, United KingdomDepartment of Ecology and Evolution, University of Lausanne, Lausanne, SwitzerlandSchool of Biological and Behavioural Sciences, Queen Mary University of London, London, United KingdomIntroductionInsects share intimate relationships with microbes that play important roles in their biology. Yet our understanding of how host-bound microbial communities assemble and perpetuate over evolutionary time is limited. Ants host a wide range of microbes with diverse functions and are an emerging model for studying the evolution of insect microbiomes. Here, we ask whether phylogenetically related ant species have formed distinct and stable microbiomes.MethodsTo answer this question, we investigated the microbial communities associated with queens of 14 Formica species from five clades, using deep coverage 16S rRNA amplicon sequencing.ResultsWe reveal that Formica species and clades harbor highly defined microbial communities that are dominated by four bacteria genera: Wolbachia, Lactobacillus, Liliensternia, and Spiroplasma. Our analysis reveals that the composition of Formica microbiomes mirrors the phylogeny of the host, i.e., phylosymbiosis, in that related hosts harbor more similar microbial communities. In addition, we find there are significant correlations between microbe co-occurrences.DiscussionOur results demonstrate Formica ants carry microbial communities that recapitulate the phylogeny of their hosts. Our data suggests that the co-occurrence of different bacteria genera may at least in part be due to synergistic and antagonistic interactions between microbes. Additional factors potentially contributing to the phylosymbiotic signal are discussed, including host phylogenetic relatedness, host-microbe genetic compatibility, modes of transmission, and similarities in host ecologies (e.g., diets). Overall, our results support the growing body of evidence that microbial community composition closely depends on the phylogeny of their hosts, despite bacteria having diverse modes of transmission and localization within the host.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1044286/fullphylosymbiosisendosymbiontantmicrobiomeevolution
spellingShingle Raphaella Jackson
Patapios A. Patapiou
Patapios A. Patapiou
Gemma Golding
Heikki Helanterä
Heikki Helanterä
Chloe K. Economou
Michel Chapuisat
Lee M. Henry
Evidence of phylosymbiosis in Formica ants
Frontiers in Microbiology
phylosymbiosis
endosymbiont
ant
microbiome
evolution
title Evidence of phylosymbiosis in Formica ants
title_full Evidence of phylosymbiosis in Formica ants
title_fullStr Evidence of phylosymbiosis in Formica ants
title_full_unstemmed Evidence of phylosymbiosis in Formica ants
title_short Evidence of phylosymbiosis in Formica ants
title_sort evidence of phylosymbiosis in formica ants
topic phylosymbiosis
endosymbiont
ant
microbiome
evolution
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1044286/full
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