Microbiome composition within a sympatric species complex of intertidal isopods (Jaera albifrons)
The increasingly recognised effects of microbiomes on the eco-evolutionary dynamics of their hosts are promoting a view of the "hologenome" as an integral host-symbiont evolutionary entity. For example, sex-ratio distorting reproductive parasites such as Wolbachia are well-studied pivotal...
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Published in | PloS one Vol. 13; no. 8; p. e0202212 |
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Main Authors | , , |
Format | Journal Article |
Language | English |
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29.08.2018
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Abstract | The increasingly recognised effects of microbiomes on the eco-evolutionary dynamics of their hosts are promoting a view of the "hologenome" as an integral host-symbiont evolutionary entity. For example, sex-ratio distorting reproductive parasites such as Wolbachia are well-studied pivotal drivers of invertebrate reproductive processes, and more recent work is highlighting novel effects of microbiome assemblages on host mating behaviour and developmental incompatibilities that underpin or reinforce reproductive isolation processes. However, examining the hologenome and its eco-evolutionary effects in natural populations is challenging because microbiome composition is considerably influenced by environmental factors. Here we illustrate these challenges in a sympatric species complex of intertidal isopods (Jaera albifrons spp.) with pervasive sex-ratio distortion and ecological and behavioural reproductive isolation mechanisms. We deep-sequence the bacterial 16S rRNA gene among males and females collected in spring and summer from two coasts in north-east Scotland, and examine microbiome composition with a particular focus on reproductive parasites. Microbiomes of all species were diverse (overall 3,317 unique sequences among 3.8 million reads) and comprised mainly Proteobacteria and Bacteroidetes taxa typical of the marine intertidal zone, in particular Vibrio spp. However, we found little evidence of the reproductive parasites Wolbachia, Rickettsia, Spiroplasma and Cardinium, suggesting alternative causes of sex-ratio distortion. Notwithstanding, a significant proportion of the variance in microbiome composition among samples was explained by sex (14.1 %), nested within geographic (26.9 %) and seasonal (39.6 %) variance components. The functional relevance of this sex signal was difficult to ascertain given the absence of reproductive parasites, the ephemeral nature of the species assemblages and substantial environmental variability. These results establish the Jaera albifrons species complex as an intriguing system for examining the effects of microbiomes on reproductive processes and speciation, and highlight the difficulties associated with snapshot assays of microbiome composition in dynamic and complex environments. |
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AbstractList | The increasingly recognised effects of microbiomes on the eco-evolutionary dynamics of their hosts are promoting a view of the "hologenome" as an integral host-symbiont evolutionary entity. For example, sex-ratio distorting reproductive parasites such as Wolbachia are well-studied pivotal drivers of invertebrate reproductive processes, and more recent work is highlighting novel effects of microbiome assemblages on host mating behaviour and developmental incompatibilities that underpin or reinforce reproductive isolation processes. However, examining the hologenome and its eco-evolutionary effects in natural populations is challenging because microbiome composition is considerably influenced by environmental factors. Here we illustrate these challenges in a sympatric species complex of intertidal isopods (Jaera albifrons spp.) with pervasive sex-ratio distortion and ecological and behavioural reproductive isolation mechanisms. We deep-sequence the bacterial 16S rRNA gene among males and females collected in spring and summer from two coasts in north-east Scotland, and examine microbiome composition with a particular focus on reproductive parasites. Microbiomes of all species were diverse (overall 3,317 unique sequences among 3.8 million reads) and comprised mainly Proteobacteria and Bacteroidetes taxa typical of the marine intertidal zone, in particular Vibrio spp. However, we found little evidence of the reproductive parasites Wolbachia, Rickettsia, Spiroplasma and Cardinium, suggesting alternative causes of sex-ratio distortion. Notwithstanding, a significant proportion of the variance in microbiome composition among samples was explained by sex (14.1 %), nested within geographic (26.9 %) and seasonal (39.6 %) variance components. The functional relevance of this sex signal was difficult to ascertain given the absence of reproductive parasites, the ephemeral nature of the species assemblages and substantial environmental variability. These results establish the Jaera albifrons species complex as an intriguing system for examining the effects of microbiomes on reproductive processes and speciation, and highlight the difficulties associated with snapshot assays of microbiome composition in dynamic and complex environments. The increasingly recognised effects of microbiomes on the eco-evolutionary dynamics of their hosts are promoting a view of the “hologenome” as an integral host-symbiont evolutionary entity. For example, sex-ratio distorting reproductive parasites such as Wolbachia are well-studied pivotal drivers of invertebrate reproductive processes, and more recent work is highlighting novel effects of microbiome assemblages on host mating behaviour and developmental incompatibilities that underpin or reinforce reproductive isolation processes. However, examining the hologenome and its eco-evolutionary effects in natural populations is challenging because microbiome composition is considerably influenced by environmental factors. Here we illustrate these challenges in a sympatric species complex of intertidal isopods ( Jaera albifrons spp.) with pervasive sex-ratio distortion and ecological and behavioural reproductive isolation mechanisms. We deep-sequence the bacterial 16S rRNA gene among males and females collected in spring and summer from two coasts in north-east Scotland, and examine microbiome composition with a particular focus on reproductive parasites. Microbiomes of all species were diverse (overall 3,317 unique sequences among 3.8 million reads) and comprised mainly Proteobacteria and Bacteroidetes taxa typical of the marine intertidal zone, in particular Vibrio spp. However, we found little evidence of the reproductive parasites Wolbachia , Rickettsia , Spiroplasma and Cardinium , suggesting alternative causes of sex-ratio distortion. Notwithstanding, a significant proportion of the variance in microbiome composition among samples was explained by sex (14.1 %), nested within geographic (26.9 %) and seasonal (39.6 %) variance components. The functional relevance of this sex signal was difficult to ascertain given the absence of reproductive parasites, the ephemeral nature of the species assemblages and substantial environmental variability. These results establish the Jaera albifrons species complex as an intriguing system for examining the effects of microbiomes on reproductive processes and speciation, and highlight the difficulties associated with snapshot assays of microbiome composition in dynamic and complex environments. |
Audience | Academic |
Author | Douglas, Alex Piertney, Stuart B Wenzel, Marius A |
AuthorAffiliation | School of Biological Sciences, University of Aberdeen, Aberdeen, United Kingdom University of Missouri Columbia, UNITED STATES |
AuthorAffiliation_xml | – name: School of Biological Sciences, University of Aberdeen, Aberdeen, United Kingdom – name: University of Missouri Columbia, UNITED STATES |
Author_xml | – sequence: 1 givenname: Marius A orcidid: 0000-0003-0093-368X surname: Wenzel fullname: Wenzel, Marius A organization: School of Biological Sciences, University of Aberdeen, Aberdeen, United Kingdom – sequence: 2 givenname: Alex surname: Douglas fullname: Douglas, Alex organization: School of Biological Sciences, University of Aberdeen, Aberdeen, United Kingdom – sequence: 3 givenname: Stuart B surname: Piertney fullname: Piertney, Stuart B organization: School of Biological Sciences, University of Aberdeen, Aberdeen, United Kingdom |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30157257$$D View this record in MEDLINE/PubMed |
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Copyright | COPYRIGHT 2018 Public Library of Science 2018 Wenzel et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2018 Wenzel et al 2018 Wenzel et al |
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fullname: A Klindworth |
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Snippet | The increasingly recognised effects of microbiomes on the eco-evolutionary dynamics of their hosts are promoting a view of the "hologenome" as an integral... The increasingly recognised effects of microbiomes on the eco-evolutionary dynamics of their hosts are promoting a view of the “hologenome” as an integral... |
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SubjectTerms | Animals Bacteria Bacteria - classification Bacteria - genetics Bacteria - isolation & purification Bacteroidetes - genetics Bacteroidetes - isolation & purification Biology and Life Sciences Cell proliferation Composition Distortion Ecology Ecology and Environmental Sciences Ecosystem Environmental factors Evolution Female Females Genetic Speciation Genetic Variation Genomes Host Microbial Interactions - genetics Infections Intertidal zone Isopoda Isopoda - microbiology Isopods Jaera albifrons Male Males Mating behavior Medicine and Health Sciences Microbiomes Microbiota Microbiota - genetics Natural populations Parasites Phylogeny Physiology Preferences Proteobacteria - genetics Proteobacteria - isolation & purification Reproductive isolation Research and Analysis Methods RNA, Bacterial - genetics RNA, Ribosomal, 16S - genetics rRNA 16S Scotland Sex Sex Factors Sex ratio Speciation Species Sympatric populations Sympatry Waterborne diseases Wolbachia |
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Title | Microbiome composition within a sympatric species complex of intertidal isopods (Jaera albifrons) |
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