Trans-generational immune priming in the mealworm beetle protects eggs through pathogen-dependent mechanisms imposing no immediate fitness cost for the offspring

Dhinaut, Julien; Chogne, Manon; Moret, Yannick

doi:10.1016/j.dci.2017.10.017

Cited by 25 publications

(34 citation statements)

References 48 publications

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“…On the contrary, opportunistic infections, as those provoked by Vibrio alginolyticus, are rather fought by inducible mechanisms [53]. Thus, the higher probability of encountering gram+ bacteria might have favored the evolution of more efficient mechanisms for the detection and transfer of anti-gram+ effectors, as similarly suggested in the insect T. molitor [25,49].…”

Section: Discussionmentioning

confidence: 99%

“…In particular, since TGIP may come at some costs for parents as for offspring, it is highly probable that its occurrence and intensity depend on the local context. In particular, active immune factors transferred to oocytes directly derive from maternal immunity, and thus represent a direct cost to her [24][25][26][27]. Maternal immune investment is thus expected to show some degree of plasticity in relation to the environmental conditions experienced by the mother [28,29].…”

Section: Introductionmentioning

confidence: 99%

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Transgenerational Immune Priming in the Field: Maternal Environmental Experience Leads to Differential Immune Transfer to Oocytes in the Marine Annelid Hediste diversicolor

Bernier

Boidin-Wichlacz

Tasiemski

et al. 2019

Genes

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Transgenerational immune priming (TGIP) is an intriguing form of parental care which leads to the plastic adjustment of the progeny’s immunity according to parental immune experience. Such parental effect has been described in several vertebrate and invertebrate taxa. However, very few empirical studies have been conducted from the field, with natural host-parasite systems and real ecological settings, especially in invertebrates. We investigated TGIP in wild populations of the marine annelid Hediste diversicolor. Females laid eggs in a mud tube and thus shared the local microbial threats with the first developmental stages, thus meeting expectations for the evolution of TGIP. We evidenced that a maternal bacterial challenge led to the higher antibacterial defense of the produced oocytes, with higher efficiency in the case of Gram-positive bacterial challenge, pointing out a prevalent role of these bacteria in the evolutionary history of TGIP in this species. Underlying mechanisms might involve the antimicrobial peptide hedistin that was detected in the cytoplasm of oocytes and whose mRNAs were selectively stored in higher quantity in mature oocytes, after a maternal immune challenge. Finally, maternal immune transfer was significantly inhibited in females living in polluted areas, suggesting associated costs and the possible trade-off with female’s protection.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Transgenerational Immune Priming in the Field: Maternal Environmental Experience Leads to Differential Immune Transfer to Oocytes in the Marine Annelid Hediste diversicolor

Bernier

Boidin-Wichlacz

Tasiemski

et al. 2019

Genes

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“…To date, the mechanisms by which insects achieve TGIP are still largely unknown. The direct transfer of antimicrobial peptides (AMPs) seems to play a major role in the immediate protection of the eggs [ 23 ], but long-term protection appears to require the transfer of “signals” stimulating the offspring’s own immune system [ 24 ]. The nature of these triggering signals is still under debate, specifically whether they are epigenetic modifications [ 25 ] or the direct transfer of bacterial peptides from the mother’s gut to the eggs [ 26 ].…”

Section: A Prerequisite: Disentangle Confounding Effectsmentioning

confidence: 99%

Interaction between Insects, Toxins, and Bacteria: Have We Been Wrong So Far?

Tetreau

2018

Toxins

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Toxins are a major virulence factor produced by many pathogenic bacteria. In vertebrates, the response of hosts to the bacteria is inseparable from the response to the toxins, allowing a comprehensive understanding of this tripartite host-pathogen-toxin interaction. However, in invertebrates, this interaction has been investigated by two complementary but historically distinct fields of research: toxinology and immunology. In this article, I highlight how such dichotomy between these two fields led to a biased, or even erroneous view of the ecology and evolution of the interaction between insects, toxins, and bacteria. I focus on the reason behind such a dichotomy, on how to bridge the fields together, and on confounding effects that could bias the outcome of the experiments. Finally, I raise four questions at the border of the two fields on the cross-effects between toxins, bacteria, and spores that have been largely underexplored to promote a more comprehensive view of this interaction.

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“…Egg protection in insects has received an increasing attention. It has been suggested to occur through endogenous egg defenses by different mechanisms, triggering differential expression of immune-related genes or through parental transfer of protection by the direct transmission of immune effectors to the eggs [ 6 , 13 , 19 – 22 ]. While maternal transgenerational protection has been extensively studied [ 6 ], evidence of paternal offspring immune protection has also been provided [ 23 , 24 ], although the underlying mechanisms might differ.…”

Section: Introductionmentioning

confidence: 99%

“…The mealworm beetle, Tenebrio molitor , is probably the insect for which TGIP has been best described so far [ 30 ]. TGIP effects were revealed through enhanced immune activity in primed eggs [ 16 , 17 , 19 , 31 ], larvae [ 5 ] and adult offspring [ 13 , 15 ]. Enhanced immunity in the offspring may result from the immune priming of either fathers or mothers, although each parental effect involves the enhancement of different immune effectors in the offspring at the adult stage [ 13 ].…”

Section: Introductionmentioning

confidence: 99%

Deciphering the molecular mechanisms of mother-to-egg immune protection in the mealworm beetle Tenebrio molitor

et al. 2020

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In a number of species, individuals exposed to pathogens can mount an immune response and transmit this immunological experience to their offspring, thereby protecting them against persistent threats. Such vertical transfer of immunity, named trans-generational immune priming (TGIP), has been described in both vertebrates and invertebrates. Although increasingly studied during the last decade, the mechanisms underlying TGIP in invertebrates are still elusive, especially those protecting the earliest offspring life stage, i . e . the embryo developing in the egg. In the present study, we combined different proteomic and transcriptomic approaches to determine whether mothers transfer a “signal” (such as fragments of infecting bacteria), mRNA and/or protein/peptide effectors to protect their eggs against two natural bacterial pathogens, namely the Gram-positive Bacillus thuringiensis and the Gram-negative Serratia entomophila . By taking the mealworm beetle Tenebrio molitor as a biological model, our results suggest that eggs are mainly protected by an active direct transfer of a restricted number of immune proteins and of antimicrobial peptides. In contrast, the present data do not support the involvement of mRNA transfer while the transmission of a “signal”, if it happens, is marginal and only occurs within 24h after maternal exposure to bacteria. This work exemplifies how combining global approaches helps to disentangle the different scenarios of a complex trait, providing a comprehensive characterization of TGIP mechanisms in T . molitor . It also paves the way for future alike studies focusing on TGIP in a wide range of invertebrates and vertebrates to identify additional candidates that could be specific to TGIP and to investigate whether the TGIP mechanisms found herein are specific or common to all insect species.

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Trans-generational immune priming in the mealworm beetle protects eggs through pathogen-dependent mechanisms imposing no immediate fitness cost for the offspring

Cited by 25 publications

References 48 publications

Transgenerational Immune Priming in the Field: Maternal Environmental Experience Leads to Differential Immune Transfer to Oocytes in the Marine Annelid Hediste diversicolor

Transgenerational Immune Priming in the Field: Maternal Environmental Experience Leads to Differential Immune Transfer to Oocytes in the Marine Annelid Hediste diversicolor

Interaction between Insects, Toxins, and Bacteria: Have We Been Wrong So Far?

Deciphering the molecular mechanisms of mother-to-egg immune protection in the mealworm beetle Tenebrio molitor

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