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Pathogen evasion of social immunity

Treating sick group members is a hallmark of collective disease defence in vertebrates and invertebrates alike. Despite substantial effects on pathogen fitness and epidemiology, it is still largely unknown how pathogens react to the selection pressure imposed by care intervention. Using social insec...

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Autores principales: Stock, Miriam, Milutinović, Barbara, Hoenigsberger, Michaela, Grasse, Anna V., Wiesenhofer, Florian, Kampleitner, Niklas, Narasimhan, Madhumitha, Schmitt, Thomas, Cremer, Sylvia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9998270/
https://www.ncbi.nlm.nih.gov/pubmed/36732670
http://dx.doi.org/10.1038/s41559-023-01981-6
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author Stock, Miriam
Milutinović, Barbara
Hoenigsberger, Michaela
Grasse, Anna V.
Wiesenhofer, Florian
Kampleitner, Niklas
Narasimhan, Madhumitha
Schmitt, Thomas
Cremer, Sylvia
author_facet Stock, Miriam
Milutinović, Barbara
Hoenigsberger, Michaela
Grasse, Anna V.
Wiesenhofer, Florian
Kampleitner, Niklas
Narasimhan, Madhumitha
Schmitt, Thomas
Cremer, Sylvia
author_sort Stock, Miriam
collection PubMed
description Treating sick group members is a hallmark of collective disease defence in vertebrates and invertebrates alike. Despite substantial effects on pathogen fitness and epidemiology, it is still largely unknown how pathogens react to the selection pressure imposed by care intervention. Using social insects and pathogenic fungi, we here performed a serial passage experiment in the presence or absence of colony members, which provide social immunity by grooming off infectious spores from exposed individuals. We found specific effects on pathogen diversity, virulence and transmission. Under selection of social immunity, pathogens invested into higher spore production, but spores were less virulent. Notably, they also elicited a lower grooming response in colony members, compared with spores from the individual host selection lines. Chemical spore analysis suggested that the spores from social selection lines escaped the caregivers’ detection by containing lower levels of ergosterol, a key fungal membrane component. Experimental application of chemically pure ergosterol indeed induced sanitary grooming, supporting its role as a microbe-associated cue triggering host social immunity against fungal pathogens. By reducing this detection cue, pathogens were able to evade the otherwise very effective collective disease defences of their social hosts.
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spelling pubmed-99982702023-03-11 Pathogen evasion of social immunity Stock, Miriam Milutinović, Barbara Hoenigsberger, Michaela Grasse, Anna V. Wiesenhofer, Florian Kampleitner, Niklas Narasimhan, Madhumitha Schmitt, Thomas Cremer, Sylvia Nat Ecol Evol Article Treating sick group members is a hallmark of collective disease defence in vertebrates and invertebrates alike. Despite substantial effects on pathogen fitness and epidemiology, it is still largely unknown how pathogens react to the selection pressure imposed by care intervention. Using social insects and pathogenic fungi, we here performed a serial passage experiment in the presence or absence of colony members, which provide social immunity by grooming off infectious spores from exposed individuals. We found specific effects on pathogen diversity, virulence and transmission. Under selection of social immunity, pathogens invested into higher spore production, but spores were less virulent. Notably, they also elicited a lower grooming response in colony members, compared with spores from the individual host selection lines. Chemical spore analysis suggested that the spores from social selection lines escaped the caregivers’ detection by containing lower levels of ergosterol, a key fungal membrane component. Experimental application of chemically pure ergosterol indeed induced sanitary grooming, supporting its role as a microbe-associated cue triggering host social immunity against fungal pathogens. By reducing this detection cue, pathogens were able to evade the otherwise very effective collective disease defences of their social hosts. Nature Publishing Group UK 2023-02-02 2023 /pmc/articles/PMC9998270/ /pubmed/36732670 http://dx.doi.org/10.1038/s41559-023-01981-6 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Stock, Miriam
Milutinović, Barbara
Hoenigsberger, Michaela
Grasse, Anna V.
Wiesenhofer, Florian
Kampleitner, Niklas
Narasimhan, Madhumitha
Schmitt, Thomas
Cremer, Sylvia
Pathogen evasion of social immunity
title Pathogen evasion of social immunity
title_full Pathogen evasion of social immunity
title_fullStr Pathogen evasion of social immunity
title_full_unstemmed Pathogen evasion of social immunity
title_short Pathogen evasion of social immunity
title_sort pathogen evasion of social immunity
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9998270/
https://www.ncbi.nlm.nih.gov/pubmed/36732670
http://dx.doi.org/10.1038/s41559-023-01981-6
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