Bacteria‐type‐specific biparental immune priming in the pipefish <i>Syngnathus typhle</i>

Beemelmanns, Anne; Roth, Olivia

doi:10.1002/ece3.2391

Cited by 23 publications

(29 citation statements)

References 102 publications

(220 reference statements)

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“…The assessed adaptive immune genes were not affected by the F0-bacteria treatment, potentially due to the on-going maturation of the adaptive immune system in one-week-old pipefish [ 66 ] and/or the rather early time point of sampling (20 h after injection). Yet , our former data implys that the expression of the same immune genes used here positively correlates with an activation of the innate (monocytes) and adaptive (lymphocytes) cellular immune system [ 19 , 40 , 67 ], suggesting that induced gene expression is linked to a physiological impact of TGIP.…”

Section: Discussionmentioning

confidence: 68%

“…In an invertebrate system with only an ejaculate-based connection between father and offspring, the paternal environment influences offspring immune phenotype [ 36 , 39 ]. Further, a strong paternal contribution to immune phenotype of progeny was found in vertebrates with intense paternal care or investment [ 19 , 35 , 40 , 41 ].…”

Section: Introductionmentioning

confidence: 99%

“…So far, it was considered that TGIP in vertebrates is only of major importance during early development, to bridge the time of maturation of the acquired immune system, when selection pressure due to high mortality is greatest [ 55 ]. In contrast, recent studies indicate that in Syngnathus typhle the persistence of immune priming lasts past the maturation of the adaptive immune system in four-month-old juveniles [ 41 ], coupled with a high degree of bacteria specificity [ 40 ]. In the current study we aimed to address the impact of biparental parental immune priming beyond the generation border, affecting the immune dynamics of the grandoffspring generation.…”

Section: Introductionmentioning

confidence: 99%

“…For the evaluation of grandparental sex-specific influences on grandoffspring immunity, either only grandmothers, only grandfathers or both grandparents (grand-biparental) were expsed to the bacteria treatment. In the F2-generation we assessed expression of 44 target genes functionally associated to different pathways of the immune system (innate and adaptive immune system, complement component system) and epigenetic regulation processes (DNA-methylation and histone modifications), to test whether complementing sex-specific contribution as previously found to exist for the F1-generation [ 40 ] may have been trans generationally maintained over two generations. Here, we found strong grandparental effects that influenced the immune gene expression of grandoffspring upon bacterial exposure.…”

Section: Introductionmentioning

confidence: 99%

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Grandparental immune priming in the pipefish Syngnathus typhle

Beemelmanns

Roth

2017

BMC Evol Biol

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BackgroundPhenotypic changes in response to environmental influences can persist from one generation into the next. In many systems parental parasite experience influences offspring immune responses, known as transgenerational immune priming (TGIP). TGIP in vertebrates is mainly maternal and short-term, supporting the adaptive immune system of the offspring during its maturation. However, if fathers and offspring have a close physical connection, evolution of additional paternal immune priming can be adaptive. Biparental TGIP may result in maximized immunological protection. Here, we investigate multigenerational biparental TGIP in the sex-role reversed pipefish Syngnathus typhle by exposing grandparents to an immune challenge with heat-killed bacteria and assessing gene expression (44 target genes) of the F2-generation.ResultsGrandparental immune challenge induced gene expression of immune genes in one-week-old grandoffspring. Similarly, genes mediating epigenetic regulation including DNA-methylation and histone modifications were involved in grandparental immune priming. While grand-maternal impact was strong on genes of the complement component system, grand-paternal exposure changed expression patterns of genes mediating innate immune defense.ConclusionIn a system with male pregnancy, grandparents influenced the immune system of their grandoffspring in a sex-specific manner, demonstrating multigenerational biparental TGIP. The involvement of epigenetic effects suggests that TGIP via the paternal line may not be limited to the pipefish system that displays male pregnancy. While the benefits and costs of grandparental TGIP depend on the temporal heterogeneity of environmental conditions, multigenerational TGIP may affect host-parasite coevolution by dampening the amplitude of Red Queen Dynamics.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-0885-3) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 68%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Grandparental immune priming in the pipefish Syngnathus typhle

Beemelmanns

Roth

2017

BMC Evol Biol

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“…For significant PERMANCOVA factors, univariate analyses served as post hoc tests to identify the impact on each gene. These ANCOVAs used the same model ( aov(x~treatment*challenge + K) ) and a Tukey HSD test if necessary, to depict the direction of the differences among treatments (as done in [ 9 ]). To address the gene expression of juvenile cichlids (III.…”

Section: Methodsmentioning

confidence: 99%

Parental investment matters for maternal and offspring immune defense in the mouthbrooding cichlid Astatotilapia burtoni

2017

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BackgroundParental care, while increasing parental fitness through offspring survival, also bears cost to the care-giving parent. Consequentially, trade offs between parental care and other vitally important traits, such as the immune system seem evident. In co-occurring phases of parental care and immunological challenges negative consequences through a resource allocation trade off on both the parental and the offspring conditions can be predicted. While the immune system reflects parental stress conditions, parental immunological investments also boost offspring survival via the transfer of immunological substances (trans-generational immune priming).We investigated this relationship in the mouthbrooding East African cichlid Astotatilapia burtoni. Prior to mating, females were exposed to an immunological activation, while others remained immunologically naïve. Correspondingly, the immunological status of females was either examined directly after reproduction or after mouthbrooding had ceased. Offspring from both groups were exposed to immunological challenges to assess the extent of trans-generational immune priming. As proxy for immune status, cellular immunological activity and gene expression were determined.ResultsBoth reproducing and mouthbrooding females allocate their resources towards reproduction. While upon reproduction the innate immune system was impeded, mouthbrooding females showed an attenuation of inflammatory components. Juveniles from immune challenged mouthbrooding females showed downregulation of immune and life history candidate genes, implying a limitation of trans-generational plasticity when parents experience stress during the costly reproductive phase.ConclusionOur results provide evidence that both parental investment via mouthbrooding and the rise of the immunological activity upon an immune challenge are costly traits. If applied simultaneously, not only mothers seem to be impacted in their performance, but also offspring are impeded in their ability to react upon a potentially virulent pathogen exposure.Electronic supplementary materialThe online version of this article (10.1186/s12862-017-1109-6) contains supplementary material, which is available to authorized users.

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Parent‐Specific Transgenerational Immune Priming Enhances Offspring Defense—Unless Heat Stress Negates It All

Schneider,

Dubin,

Marten

et al. 2024

Ecology and Evolution

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Transgenerational immune priming (TGIP) adjusts offspring's immune responses based on parental immunological experiences. It is predicted to be adaptive when parent–offspring environmental conditions match, while mismatches negate those advantages, rendering TGIP potentially costly. We tested these cost–benefit dynamics in the pipefish Syngnathus typhle (Syngnathidae). Because of their unique male pregnancy, egg production and rearing occur in different sexes, providing both parents multiple avenues for TGIP. Parental bacteria exposure in our pipefish was simulated through vaccinations with heat‐killed Vibrio aestuarianus before mating the fish to each other or to controls. The resulting offspring were exposed to V. aestuarianus in control or heat stress environments, after which transcriptome and microbiome compositions were investigated. Transcriptomic TGIP effects were only observed in Vibrio‐exposed offspring at control temperatures, arguing for low costs of TGIP in non‐matching microbiota environments. Transcriptomic phenotypes elicited by maternal and paternal TGIP had limited overlap and were not additive. Parentally induced transcriptomic responses were associated with immune functions, and specifically, the paternal response to the innate immune branch, possibly hinting at trained immunity. TGIP of both parents reduced the relative abundance of the experimental Vibrio in exposed offspring, showcasing its ecological benefits. Despite TGIP's significance in matching biotic environments, no TGIP‐associated phenotypes were observed for heat‐treated offspring, illustrating its limitations. Heat spikes caused by climate change thus threaten TGIP benefits, potentially increasing susceptibility to emerging marine diseases. We demonstrate the urgent need to understand how animals cope with climate‐induced changes in microbial assemblages to assess their vulnerability in light of climate change.

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Bacteria‐type‐specific biparental immune priming in the pipefish Syngnathus typhle

Cited by 23 publications

References 102 publications

Grandparental immune priming in the pipefish Syngnathus typhle

Grandparental immune priming in the pipefish Syngnathus typhle

Parental investment matters for maternal and offspring immune defense in the mouthbrooding cichlid Astatotilapia burtoni

Parent‐Specific Transgenerational Immune Priming Enhances Offspring Defense—Unless Heat Stress Negates It All

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