Translocation of bacteria from the gut to the eggs triggers maternal transgenerational immune priming in Tribolium castaneum

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Abstract

Invertebrates can be primed to enhance their protection against pathogens they have encountered before. This enhanced immunity can be passed maternally or paternally to the offspring and is known as transgenerational immune priming. We challenged larvae of the red flour beetle Tribolium castaneum by feeding them on diets supplemented with Escherichia coli, Micrococcus luteus or Pseudomonas entomophila, thus mimicking natural exposure to pathogens. The oral uptake of bacteria induced immunity-related genes in the offspring, but did not affect the methylation status of the egg DNA. However, we observed the translocation of bacteria or bacterial fragments from the gut to the developing eggs via the female reproductive system. Such translocating microbial elicitors are postulated to trigger bacterial strain-specific immune responses in the offspring and provide an alternative mechanistic explanation for maternal transgenerational immune priming in coleopteran insects.

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Trans-generational immune priming in a social insect.

Yvonne Kleinlogel, Ben Sadd, Paul Schmid-Hempel … (2005)

Detecting functional homology between invertebrate and vertebrate immunity is of interest in terms of understanding the dynamics and evolution of immune systems. Trans-generational effects on immunity are well known from vertebrates, but their existence in invertebrates remains controversial. Earlier work on invertebrates has interpreted increased offspring resistance to pathogens as trans-generational immune priming. However, interpretation of these earlier studies involves some caveats and thus full evidence for a direct effect of maternal immune experience on offspring immunity is still lacking in invertebrates. Here we show that induced levels of antibacterial activity are higher in the worker offspring of the bumblebee, Bombus terrestris L. when their mother queen received a corresponding immune challenge prior to colony founding. This shows trans-generational immune priming in an insect, with ramifications for the evolution of sociality.

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Maternal transfer of strain-specific immunity in an invertebrate.

Tom J. Little, Benjamin D. O'Connor, Nick Colegrave … (2003)

The most celebrated component of the vertebrate immune system is the acquired response in which memory cells established during primary infection enhance the proliferation of antibodies during secondary infection. Additionally, the strength of vertebrate acquired immune responses varies dramatically depending on the infecting pathogen species or on the pathogen genotype within species. Because invertebrates lack the T-cell receptors and Major Histocompatibility Complex (MHC) molecules that mediate vertebrate adaptive immune responses, they are thought to lack adaptive immunity and be relatively unspecific in their interactions with pathogens. With only innate immunity, invertebrate hosts are believed to be nai;ve at each new encounter with pathogens. Nevertheless, some forms of facultative immunity appear to be important in insects; some individuals have enhanced immunity due to population density, and some social insects benefit when their nest-mates have been exposed to a pathogen or pathogen mimic (; see for a predation example.) Here we provide evidence for acquired strain-specific immunity in the crustacean Daphnia magna infected with the pathogenic bacteria Pasteuria ramosa. Specifically, the fitness of hosts was enhanced when challenged with a bacterial strain their mother had experienced relative to cases when mother and offspring were challenged with different strains.

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Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum.

Gerrit Joop, Timothy J Hilbert, Jens Daniel … (2010)

1. Parasitized females in mammals, fish and birds can enhance the immune defence of their offspring by transferring specific antibodies for the embryo. Likewise, social insect mothers transfer immunity despite the fact that invertebrates lack antibodies. 2. Female trans-generational immune priming is consistent with parental investment theory, because mothers invest more into rearing their offspring than fathers. However, when immune priming is not directly linked to parental care, as is often the case in insects that abandon their eggs after oviposition, both sexes might benefit from protecting their offspring. 3. Using the red flour beetle, Tribolium castaneum, we show that after parental exposure to heat-killed bacteria, trans-generational immune priming occurs through fathers as well as mothers. 4. This novel finding challenges the traditional view that males provide only genes to their offspring in species without paternal care, and raises the possibility of a division of tasks with respect to immune protection between parents.

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Author and article information

Journal

Journal ID (nlm-ta): Biol Lett

Journal ID (iso-abbrev): Biol. Lett

Journal ID (publisher-id): RSBL

Journal ID (hwp): roybiolett

Title: Biology Letters

Publisher: The Royal Society

ISSN (Print): 1744-9561

ISSN (Electronic): 1744-957X

Publication date (Print): December 2015

Publication date PMC-release: December 2015

Volume: 11

Issue: 12

Electronic Location Identifier: 20150885

Affiliations

[1 ]Department of Bioresources, Fraunhofer Institute for Molecular Biology and Applied Ecology , Winchester Strasse 2, 35395 Giessen, Germany

[2 ]Institute for Insect Biotechnology, Justus-Liebig-University of Giessen , Heinrich-Buff-Ring 26-32, 35392 Giessen, Germany

Author notes

e-mail: andreas.vilcinskas@ 123456agrar.uni-giessen.de

Article

Publisher ID: rsbl20150885

DOI: 10.1098/rsbl.2015.0885

PMC ID: 4707703

PubMed ID: 26701756

SO-VID: d0e1b97b-dea5-4fc5-a17e-bf9f460a9ac7

License:

Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

History

Date received : 20 October 2015

Date accepted : 23 November 2015

Funding

Funded by: AAV acknowledges generous funding by the Hessen State Ministry of Higher Education, Research and the Arts (HMWK) via the “LOEWE Center for Insect Biotechnology and Bioresources” by the German Research Foundation for the project “the role of epigenetics in host-parasite-coevolution” (VI 219/3-2) which is embedded within the DFG Priority Program 1399 “Host-Parasite Coevolution - rapid reciprocal adaptations and its genetic basis”.;

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cover-date December, 2015

ScienceOpen disciplines: Life sciences

Keywords: transgenerational immune priming,innate immunity,parental investment,fitness costs,maternal inheritance,tribolium castaneum

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ScienceOpen disciplines: Life sciences

Keywords: transgenerational immune priming, innate immunity, parental investment, fitness costs, maternal inheritance, tribolium castaneum

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Translocation of bacteria from the gut to the eggs triggers maternal transgenerational immune priming in Tribolium castaneum

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Most cited references 17

Trans-generational immune priming in a social insect.

Maternal transfer of strain-specific immunity in an invertebrate.

Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum.

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