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No evidence that gut microbiota impose a net cost on their butterfly host

Gut microbes are believed to play a critical role in most animal life, yet fitness effects and cost–benefit trade‐offs incurred by the host are poorly understood. Unlike most hosts studied to date, butterflies largely acquire their nutrients from larval feeding, leaving relatively little opportunity...

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Autores principales: Ravenscraft, Alison, Kish, Nicole, Peay, Kabir, Boggs, Carol
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6525022/
https://www.ncbi.nlm.nih.gov/pubmed/30803091
http://dx.doi.org/10.1111/mec.15057
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author Ravenscraft, Alison
Kish, Nicole
Peay, Kabir
Boggs, Carol
author_facet Ravenscraft, Alison
Kish, Nicole
Peay, Kabir
Boggs, Carol
author_sort Ravenscraft, Alison
collection PubMed
description Gut microbes are believed to play a critical role in most animal life, yet fitness effects and cost–benefit trade‐offs incurred by the host are poorly understood. Unlike most hosts studied to date, butterflies largely acquire their nutrients from larval feeding, leaving relatively little opportunity for nutritive contributions by the adult's microbiota. This provides an opportunity to measure whether hosting gut microbiota comes at a net nutritional price. Because host and bacteria may compete for sugars, we hypothesized that gut flora would be nutritionally neutral to adult butterflies with plentiful food, but detrimental to semistarved hosts, especially when at high density. We held field‐caught adult Speyeria mormonia under abundant or restricted food conditions. Because antibiotic treatments did not generate consistent variation in their gut microbiota, we used interindividual variability in bacterial loads and operational taxonomic unit abundances to examine correlations between host fitness and the abdominal microbiota present upon natural death. We detected strikingly few relationships between microbial flora and host fitness. Neither total bacterial load nor the abundances of dominant bacterial taxa were related to butterfly fecundity, egg mass or egg chemical content. Increased abundance of a Commensalibacter species did correlate with longer host life span, while increased abundance of a Rhodococcus species correlated with shorter life span. Contrary to our expectations, these relationships were unchanged by food availability to the host and were unrelated to reproductive output. Our results suggest the butterfly microbiota comprises parasitic, commensal and beneficial taxa that together do not impose a net reproductive cost, even under caloric stress.
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spelling pubmed-65250222019-06-17 No evidence that gut microbiota impose a net cost on their butterfly host Ravenscraft, Alison Kish, Nicole Peay, Kabir Boggs, Carol Mol Ecol ORIGINAL ARTICLES Gut microbes are believed to play a critical role in most animal life, yet fitness effects and cost–benefit trade‐offs incurred by the host are poorly understood. Unlike most hosts studied to date, butterflies largely acquire their nutrients from larval feeding, leaving relatively little opportunity for nutritive contributions by the adult's microbiota. This provides an opportunity to measure whether hosting gut microbiota comes at a net nutritional price. Because host and bacteria may compete for sugars, we hypothesized that gut flora would be nutritionally neutral to adult butterflies with plentiful food, but detrimental to semistarved hosts, especially when at high density. We held field‐caught adult Speyeria mormonia under abundant or restricted food conditions. Because antibiotic treatments did not generate consistent variation in their gut microbiota, we used interindividual variability in bacterial loads and operational taxonomic unit abundances to examine correlations between host fitness and the abdominal microbiota present upon natural death. We detected strikingly few relationships between microbial flora and host fitness. Neither total bacterial load nor the abundances of dominant bacterial taxa were related to butterfly fecundity, egg mass or egg chemical content. Increased abundance of a Commensalibacter species did correlate with longer host life span, while increased abundance of a Rhodococcus species correlated with shorter life span. Contrary to our expectations, these relationships were unchanged by food availability to the host and were unrelated to reproductive output. Our results suggest the butterfly microbiota comprises parasitic, commensal and beneficial taxa that together do not impose a net reproductive cost, even under caloric stress. John Wiley and Sons Inc. 2019-04-25 2019-04 /pmc/articles/PMC6525022/ /pubmed/30803091 http://dx.doi.org/10.1111/mec.15057 Text en © 2019 The Authors. Molecular Ecology Published by John Wiley & Sons Ltd This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle ORIGINAL ARTICLES
Ravenscraft, Alison
Kish, Nicole
Peay, Kabir
Boggs, Carol
No evidence that gut microbiota impose a net cost on their butterfly host
title No evidence that gut microbiota impose a net cost on their butterfly host
title_full No evidence that gut microbiota impose a net cost on their butterfly host
title_fullStr No evidence that gut microbiota impose a net cost on their butterfly host
title_full_unstemmed No evidence that gut microbiota impose a net cost on their butterfly host
title_short No evidence that gut microbiota impose a net cost on their butterfly host
title_sort no evidence that gut microbiota impose a net cost on their butterfly host
topic ORIGINAL ARTICLES
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6525022/
https://www.ncbi.nlm.nih.gov/pubmed/30803091
http://dx.doi.org/10.1111/mec.15057
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