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Early queen infection shapes developmental dynamics and induces long‐term disease protection in incipient ant colonies

Infections early in life can have enduring effects on an organism's development and immunity. In this study, we show that this equally applies to developing ‘superorganisms’––incipient social insect colonies. When we exposed newly mated Lasius niger ant queens to a low pathogen dose, their colo...

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Autores principales: Casillas‐Pérez, Barbara, Pull, Christopher D., Naiser, Filip, Naderlinger, Elisabeth, Matas, Jiri, Cremer, Sylvia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9298059/
https://www.ncbi.nlm.nih.gov/pubmed/34725912
http://dx.doi.org/10.1111/ele.13907
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author Casillas‐Pérez, Barbara
Pull, Christopher D.
Naiser, Filip
Naderlinger, Elisabeth
Matas, Jiri
Cremer, Sylvia
author_facet Casillas‐Pérez, Barbara
Pull, Christopher D.
Naiser, Filip
Naderlinger, Elisabeth
Matas, Jiri
Cremer, Sylvia
author_sort Casillas‐Pérez, Barbara
collection PubMed
description Infections early in life can have enduring effects on an organism's development and immunity. In this study, we show that this equally applies to developing ‘superorganisms’––incipient social insect colonies. When we exposed newly mated Lasius niger ant queens to a low pathogen dose, their colonies grew more slowly than controls before winter, but reached similar sizes afterwards. Independent of exposure, queen hibernation survival improved when the ratio of pupae to workers was small. Queens that reared fewer pupae before worker emergence exhibited lower pathogen levels, indicating that high brood rearing efforts interfere with the ability of the queen's immune system to suppress pathogen proliferation. Early‐life queen pathogen exposure also improved the immunocompetence of her worker offspring, as demonstrated by challenging the workers to the same pathogen a year later. Transgenerational transfer of the queen's pathogen experience to her workforce can hence durably reduce the disease susceptibility of the whole superorganism.
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spelling pubmed-92980592022-07-21 Early queen infection shapes developmental dynamics and induces long‐term disease protection in incipient ant colonies Casillas‐Pérez, Barbara Pull, Christopher D. Naiser, Filip Naderlinger, Elisabeth Matas, Jiri Cremer, Sylvia Ecol Lett Letters Infections early in life can have enduring effects on an organism's development and immunity. In this study, we show that this equally applies to developing ‘superorganisms’––incipient social insect colonies. When we exposed newly mated Lasius niger ant queens to a low pathogen dose, their colonies grew more slowly than controls before winter, but reached similar sizes afterwards. Independent of exposure, queen hibernation survival improved when the ratio of pupae to workers was small. Queens that reared fewer pupae before worker emergence exhibited lower pathogen levels, indicating that high brood rearing efforts interfere with the ability of the queen's immune system to suppress pathogen proliferation. Early‐life queen pathogen exposure also improved the immunocompetence of her worker offspring, as demonstrated by challenging the workers to the same pathogen a year later. Transgenerational transfer of the queen's pathogen experience to her workforce can hence durably reduce the disease susceptibility of the whole superorganism. John Wiley and Sons Inc. 2021-11-01 2022-01 /pmc/articles/PMC9298059/ /pubmed/34725912 http://dx.doi.org/10.1111/ele.13907 Text en © 2021 The Authors. Ecology Letters published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Letters
Casillas‐Pérez, Barbara
Pull, Christopher D.
Naiser, Filip
Naderlinger, Elisabeth
Matas, Jiri
Cremer, Sylvia
Early queen infection shapes developmental dynamics and induces long‐term disease protection in incipient ant colonies
title Early queen infection shapes developmental dynamics and induces long‐term disease protection in incipient ant colonies
title_full Early queen infection shapes developmental dynamics and induces long‐term disease protection in incipient ant colonies
title_fullStr Early queen infection shapes developmental dynamics and induces long‐term disease protection in incipient ant colonies
title_full_unstemmed Early queen infection shapes developmental dynamics and induces long‐term disease protection in incipient ant colonies
title_short Early queen infection shapes developmental dynamics and induces long‐term disease protection in incipient ant colonies
title_sort early queen infection shapes developmental dynamics and induces long‐term disease protection in incipient ant colonies
topic Letters
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9298059/
https://www.ncbi.nlm.nih.gov/pubmed/34725912
http://dx.doi.org/10.1111/ele.13907
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