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 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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John Wiley & Sons
2019-04
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Subjects: | 16S amplicon sequencing, Butterflies, Lepidoptera, Lycaenidae, Myrmecophily, Spiroplasma, |
Online Access: | http://hdl.handle.net/10261/206255 http://dx.doi.org/10.13039/501100003329 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100011033 http://dx.doi.org/10.13039/100000001 |
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dig-ibe-es-10261-2062552023-01-03T10:43:30Z 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 Pietro Kešnerová, Lucie Whitaker, Melissa R. L. Engel, Philipp Vila, Roger Álvarez, Nadir Swiss National Science Foundation Ministerio de Economía y Competitividad (España) European Commission Agencia Estatal de Investigación (España) National Science Foundation (US) 16S amplicon sequencing Butterflies Lepidoptera Lycaenidae Myrmecophily Spiroplasma 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. MAS was supported by a UNIL Master's Grant, NA was supported by Swiss National Science Foundation grant PP00P3_172899, RV was supported by project CGL2016‐76322‐P (AEI/FEDER, UE), and MRLW was supported by a US National Science Foundation Postdoctoral Research Fellowship in Biology (1309425). 2020-04-02T09:51:15Z 2020-04-02T09:51:15Z 2019-04 2020-04-02T09:51:16Z artículo http://purl.org/coar/resource_type/c_6501 doi: 10.1002/ece3.5010 e-issn: 2045-7758 Ecology and Evolution 9(8): 4452-4464 (2019) http://hdl.handle.net/10261/206255 10.1002/ece3.5010 http://dx.doi.org/10.13039/501100003329 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100011033 http://dx.doi.org/10.13039/100000001 31031919 #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/CGL2016-76322-P Publisher's version Szenteczki, Mark A.; Pitteloud, Camille; Casacci, Luca Pietro; Kešnerová, Lucie; Whitaker, Melissa R. L.; Engel, Philipp; Vila, Roger; Alvarez, Nadir; 2019; Data from: Bacterial communities within Phengaris (Maculinea) alcon caterpillars are shifted following transition from solitary living to social parasitism of Myrmica ant colonies [Dataset]; Dryad; Version 1; https://doi.org/10.5061/dryad.60008mj http:/doi.org/10.1002/ece3.5010 Sí open John Wiley & Sons |
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16S amplicon sequencing Butterflies Lepidoptera Lycaenidae Myrmecophily Spiroplasma 16S amplicon sequencing Butterflies Lepidoptera Lycaenidae Myrmecophily Spiroplasma |
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16S amplicon sequencing Butterflies Lepidoptera Lycaenidae Myrmecophily Spiroplasma 16S amplicon sequencing Butterflies Lepidoptera Lycaenidae Myrmecophily Spiroplasma Szenteczki, Mark A. Pitteloud, Camille Casacci, Luca Pietro Kešnerová, Lucie Whitaker, Melissa R. L. Engel, Philipp Vila, Roger Álvarez, Nadir Bacterial communities within Phengaris (Maculinea) alcon caterpillars are shifted following transition from solitary living to social parasitism of Myrmica ant colonies |
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. |
author2 |
Swiss National Science Foundation |
author_facet |
Swiss National Science Foundation Szenteczki, Mark A. Pitteloud, Camille Casacci, Luca Pietro Kešnerová, Lucie Whitaker, Melissa R. L. Engel, Philipp Vila, Roger Álvarez, Nadir |
format |
artículo |
topic_facet |
16S amplicon sequencing Butterflies Lepidoptera Lycaenidae Myrmecophily Spiroplasma |
author |
Szenteczki, Mark A. Pitteloud, Camille Casacci, Luca Pietro Kešnerová, Lucie Whitaker, Melissa R. L. Engel, Philipp Vila, Roger Álvarez, Nadir |
author_sort |
Szenteczki, Mark A. |
title |
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_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_sort |
bacterial communities within phengaris (maculinea) alcon caterpillars are shifted following transition from solitary living to social parasitism of myrmica ant colonies |
publisher |
John Wiley & Sons |
publishDate |
2019-04 |
url |
http://hdl.handle.net/10261/206255 http://dx.doi.org/10.13039/501100003329 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100011033 http://dx.doi.org/10.13039/100000001 |
work_keys_str_mv |
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