Parasite Presence Induces Gene Expression Changes in an Ant Host Related to Immunity and Longevity

Most species are either parasites or exploited by parasites, making parasite–host interactions a driver of evolution. Parasites with complex life cycles often evolve strategies to facilitate transmission to the definitive host by manipulating their intermediate host. Such manipulations could explain...

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Main Authors: Marah Stoldt, Linda Klein, Sara Beros, Falk Butter, Evelien Jongepier, Barbara Feldmeyer, Susanne Foitzik
Format: Article
Language:English
Published: MDPI AG 2021-01-01
Series:Genes
Subjects:
Online Access:https://www.mdpi.com/2073-4425/12/1/95
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spelling doaj-ad55dddcf7ec477bb2e29af568f4c5d92021-01-14T00:04:45ZengMDPI AGGenes2073-44252021-01-0112959510.3390/genes12010095Parasite Presence Induces Gene Expression Changes in an Ant Host Related to Immunity and LongevityMarah Stoldt0Linda Klein1Sara Beros2Falk Butter3Evelien Jongepier4Barbara Feldmeyer5Susanne Foitzik6Institute of Organismic and Molecular Evolution, Johannes Gutenberg University Mainz, 55128 Mainz, GermanyInstitute of Organismic and Molecular Evolution, Johannes Gutenberg University Mainz, 55128 Mainz, GermanyMax Planck Institute for the Biology of Ageing, 50931 Cologne, GermanyInstitute for Molecular Biology, Johannes Gutenberg University Mainz, 55128 Mainz, GermanyInstitute for Evolution and Biodiversity, University of Münster, 48149 Münster, GermanySenckenberg Biodiversity and Climate Research Center (SBiK-F), Molecular Ecology, 60325 Frankfurt, GermanyInstitute of Organismic and Molecular Evolution, Johannes Gutenberg University Mainz, 55128 Mainz, GermanyMost species are either parasites or exploited by parasites, making parasite–host interactions a driver of evolution. Parasites with complex life cycles often evolve strategies to facilitate transmission to the definitive host by manipulating their intermediate host. Such manipulations could explain phenotypic changes in the ant <i>Temnothorax nylanderi</i>, the intermediate host of the cestode <i>Anomotaenia brevis</i>. In addition to behavioral and morphological alterations, infected workers exhibit prolonged lifespans, comparable to that of queens, which live up to two decades. We used transcriptomic data from cestodes and ants of different castes and infection status to investigate the molecular underpinnings of phenotypic alterations in infected workers and explored whether the extended lifespan of queens and infected workers has a common molecular basis. Infected workers and queens commonly upregulated only six genes, one of them with a known anti-aging function. Both groups overexpressed immune genes, although not the same ones. Our findings suggest that the lifespan extension of infected workers is not achieved via the expression of queen-specific genes. The analysis of the cestodes’ transcriptome revealed dominant expression of genes of the mitochondrial respiratory transport chain, which indicates an active metabolism and shedding light on the physiology of the parasite in its cysticercoid stage.https://www.mdpi.com/2073-4425/12/1/95host lifespantranscriptomicshost–parasite interaction<i>Temnothorax nylanderi</i><i>Anomotaenia brevis</i>extended phenotype
collection DOAJ
language English
format Article
sources DOAJ
author Marah Stoldt
Linda Klein
Sara Beros
Falk Butter
Evelien Jongepier
Barbara Feldmeyer
Susanne Foitzik
spellingShingle Marah Stoldt
Linda Klein
Sara Beros
Falk Butter
Evelien Jongepier
Barbara Feldmeyer
Susanne Foitzik
Parasite Presence Induces Gene Expression Changes in an Ant Host Related to Immunity and Longevity
Genes
host lifespan
transcriptomics
host–parasite interaction
<i>Temnothorax nylanderi</i>
<i>Anomotaenia brevis</i>
extended phenotype
author_facet Marah Stoldt
Linda Klein
Sara Beros
Falk Butter
Evelien Jongepier
Barbara Feldmeyer
Susanne Foitzik
author_sort Marah Stoldt
title Parasite Presence Induces Gene Expression Changes in an Ant Host Related to Immunity and Longevity
title_short Parasite Presence Induces Gene Expression Changes in an Ant Host Related to Immunity and Longevity
title_full Parasite Presence Induces Gene Expression Changes in an Ant Host Related to Immunity and Longevity
title_fullStr Parasite Presence Induces Gene Expression Changes in an Ant Host Related to Immunity and Longevity
title_full_unstemmed Parasite Presence Induces Gene Expression Changes in an Ant Host Related to Immunity and Longevity
title_sort parasite presence induces gene expression changes in an ant host related to immunity and longevity
publisher MDPI AG
series Genes
issn 2073-4425
publishDate 2021-01-01
description Most species are either parasites or exploited by parasites, making parasite–host interactions a driver of evolution. Parasites with complex life cycles often evolve strategies to facilitate transmission to the definitive host by manipulating their intermediate host. Such manipulations could explain phenotypic changes in the ant <i>Temnothorax nylanderi</i>, the intermediate host of the cestode <i>Anomotaenia brevis</i>. In addition to behavioral and morphological alterations, infected workers exhibit prolonged lifespans, comparable to that of queens, which live up to two decades. We used transcriptomic data from cestodes and ants of different castes and infection status to investigate the molecular underpinnings of phenotypic alterations in infected workers and explored whether the extended lifespan of queens and infected workers has a common molecular basis. Infected workers and queens commonly upregulated only six genes, one of them with a known anti-aging function. Both groups overexpressed immune genes, although not the same ones. Our findings suggest that the lifespan extension of infected workers is not achieved via the expression of queen-specific genes. The analysis of the cestodes’ transcriptome revealed dominant expression of genes of the mitochondrial respiratory transport chain, which indicates an active metabolism and shedding light on the physiology of the parasite in its cysticercoid stage.
topic host lifespan
transcriptomics
host–parasite interaction
<i>Temnothorax nylanderi</i>
<i>Anomotaenia brevis</i>
extended phenotype
url https://www.mdpi.com/2073-4425/12/1/95
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