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Bacterial communities within Phengaris (Maculinea) alcon caterpillars are shifted following transition from solitary living to social parasitism of Myrmica ant colonies

Bacterial symbionts are known to facilitate a wide range of physiological processes and ecological interactions for their hosts. In spite of this, caterpillars with highly diverse life histories appear to lack resident microbiota. Gut physiology, endogenous digestive enzymes, and limited social inte...

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Autores principales: Szenteczki, Mark A., Pitteloud, Camille, Casacci, Luca P., Kešnerová, Lucie, Whitaker, Melissa R.L., Engel, Philipp, Vila, Roger, Alvarez, Nadir
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/PMC6476763/
https://www.ncbi.nlm.nih.gov/pubmed/31031919
http://dx.doi.org/10.1002/ece3.5010
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author Szenteczki, Mark A.
Pitteloud, Camille
Casacci, Luca P.
Kešnerová, Lucie
Whitaker, Melissa R.L.
Engel, Philipp
Vila, Roger
Alvarez, Nadir
author_facet Szenteczki, Mark A.
Pitteloud, Camille
Casacci, Luca P.
Kešnerová, Lucie
Whitaker, Melissa R.L.
Engel, Philipp
Vila, Roger
Alvarez, Nadir
author_sort Szenteczki, Mark A.
collection PubMed
description Bacterial symbionts are known to facilitate a wide range of physiological processes and ecological interactions for their hosts. In spite of this, caterpillars with highly diverse life histories appear to lack resident microbiota. Gut physiology, endogenous digestive enzymes, and limited social interactions may contribute to this pattern, but the consequences of shifts in social activity and diet on caterpillar microbiota are largely unknown. Phengaris alcon caterpillars undergo particularly dramatic social and dietary shifts when they parasitize Myrmica ant colonies, rapidly transitioning from solitary herbivory to ant tending (i.e., receiving protein‐rich regurgitations through trophallaxis). This unique life history provides a model for studying interactions between social living, diet, and caterpillar microbiota. Here, we characterized and compared bacterial communities within P. alcon caterpillars before and after their association with ants, using 16S rRNA amplicon sequencing and quantitative PCR. After being adopted by ants, bacterial communities within P. alcon caterpillars shifted substantially, with a significant increase in alpha diversity and greater consistency in bacterial community composition in terms of beta dissimilarity. We also characterized the bacterial communities within their host ants (Myrmica schencki), food plant (Gentiana cruciata), and soil from ant nest chambers. These data indicated that the aforementioned patterns were influenced by bacteria derived from caterpillars’ surrounding environments, rather than through transfers from ants. Thus, while bacterial communities are substantially reorganized over the life cycle of P. alcon caterpillars, it appears that they do not rely on transfers of bacteria from host ants to complete their development.
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spelling pubmed-64767632019-04-26 Bacterial communities within Phengaris (Maculinea) alcon caterpillars are shifted following transition from solitary living to social parasitism of Myrmica ant colonies Szenteczki, Mark A. Pitteloud, Camille Casacci, Luca P. Kešnerová, Lucie Whitaker, Melissa R.L. Engel, Philipp Vila, Roger Alvarez, Nadir Ecol Evol Original Research Bacterial symbionts are known to facilitate a wide range of physiological processes and ecological interactions for their hosts. In spite of this, caterpillars with highly diverse life histories appear to lack resident microbiota. Gut physiology, endogenous digestive enzymes, and limited social interactions may contribute to this pattern, but the consequences of shifts in social activity and diet on caterpillar microbiota are largely unknown. Phengaris alcon caterpillars undergo particularly dramatic social and dietary shifts when they parasitize Myrmica ant colonies, rapidly transitioning from solitary herbivory to ant tending (i.e., receiving protein‐rich regurgitations through trophallaxis). This unique life history provides a model for studying interactions between social living, diet, and caterpillar microbiota. Here, we characterized and compared bacterial communities within P. alcon caterpillars before and after their association with ants, using 16S rRNA amplicon sequencing and quantitative PCR. After being adopted by ants, bacterial communities within P. alcon caterpillars shifted substantially, with a significant increase in alpha diversity and greater consistency in bacterial community composition in terms of beta dissimilarity. We also characterized the bacterial communities within their host ants (Myrmica schencki), food plant (Gentiana cruciata), and soil from ant nest chambers. These data indicated that the aforementioned patterns were influenced by bacteria derived from caterpillars’ surrounding environments, rather than through transfers from ants. Thus, while bacterial communities are substantially reorganized over the life cycle of P. alcon caterpillars, it appears that they do not rely on transfers of bacteria from host ants to complete their development. John Wiley and Sons Inc. 2019-04-02 /pmc/articles/PMC6476763/ /pubmed/31031919 http://dx.doi.org/10.1002/ece3.5010 Text en © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Research
Szenteczki, Mark A.
Pitteloud, Camille
Casacci, Luca P.
Kešnerová, Lucie
Whitaker, Melissa R.L.
Engel, Philipp
Vila, Roger
Alvarez, Nadir
Bacterial communities within Phengaris (Maculinea) alcon caterpillars are shifted following transition from solitary living to social parasitism of Myrmica ant colonies
title Bacterial communities within Phengaris (Maculinea) alcon caterpillars are shifted following transition from solitary living to social parasitism of Myrmica ant colonies
title_full Bacterial communities within Phengaris (Maculinea) alcon caterpillars are shifted following transition from solitary living to social parasitism of Myrmica ant colonies
title_fullStr Bacterial communities within Phengaris (Maculinea) alcon caterpillars are shifted following transition from solitary living to social parasitism of Myrmica ant colonies
title_full_unstemmed Bacterial communities within Phengaris (Maculinea) alcon caterpillars are shifted following transition from solitary living to social parasitism of Myrmica ant colonies
title_short Bacterial communities within Phengaris (Maculinea) alcon caterpillars are shifted following transition from solitary living to social parasitism of Myrmica ant colonies
title_sort bacterial communities within phengaris (maculinea) alcon caterpillars are shifted following transition from solitary living to social parasitism of myrmica ant colonies
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6476763/
https://www.ncbi.nlm.nih.gov/pubmed/31031919
http://dx.doi.org/10.1002/ece3.5010
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