Biparental immune priming in the pipefish Syngnathus typhle

Beemelmanns, Anne; Roth, Olivia

doi:10.1016/j.zool.2016.06.002

Cited by 55 publications

(91 citation statements)

References 70 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In general, expression of immune genes in one‐week‐old F1‐juveniles was predominantly influenced by the paternal bacteria treatment. Likewise, innate immune genes of four‐month‐old juveniles were only affected upon the paternal treatment, and F1‐offspring receiving a homologous Vibrio bacteria challenge as their fathers showed an induced immune cell activity in the head kidney, indicating the transfer of paternal Vibrio specificity (Beemelmanns and Roth ). Males may transfer information about immediate protection cues against prevalent pathogens in their environment through the placenta‐like structure during male pregnancy and/or through epigenetic marks.…”

Section: Discussionmentioning

confidence: 99%

“…The parental pipefish generation was sampled, maintained, and treated as described in Beemelmanns and Roth (2016). Adult individuals received an injection with 50 lL of 10 8 cells/ml heat-killed bacteria as immune challenge (Beemelmanns and Roth 2016). In our experimental design, always one sex of a mating pair was vaccinated with either Vibrio spp.…”

Section: Parental Generation (F0-treatment)mentioning

confidence: 99%

“…With offspring development, TGIP declines (Lindholm et al. ), but its consequences can remain over several generations (Beemelmanns and Roth in review; Ismail et al. ; Norouzitallab et al.…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

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

Beemelmanns

Roth

2016

Ecology and Evolution

Self Cite

View full text Add to dashboard Cite

The transfer of acquired and specific immunity against previously encountered bacteria from mothers to offspring boosts the immune response of the next generation and supports the development of a successful pathogen defense. While most studies claim that the transfer of immunity is a maternal trait, in the sex‐role‐reversed pipefish Syngnathus typhle, fathers nurse the embryos over a placenta‐like structure, which opens the door for additional paternal immune priming. We examined the potential and persistence of bacteria‐type‐specific parental immune priming in the pipefish S. typhle over maturation time using a fully reciprocal design with two different bacteria species (Vibrio spp. and Tenacibaculum maritimum). Our results suggest that S. typhle is able to specifically prime the next generation against prevalent local bacteria and to a limited extent even also against newly introduced bacteria species. Long‐term protection was thereby maintained only against prevailing Vibrio bacteria. Maternal and paternal transgenerational immune priming can complement each other, as they affect different pathways of the offspring immune system and come with distinct degree of specificity. The differential regulation of DNA‐methylation genes upon parental bacteria exposure in premature pipefish offspring indicates that epigenetic regulation processes are involved in transferring immune‐related information across generations. The identified trade‐offs between immune priming and reproduction determine TGIP as a costly trait, which might constrain the evolution of long‐lasting TGIP, if parental and offspring generations do not share the same parasite assembly.

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Parental Generation (F0-treatment)mentioning

confidence: 99%

See 1 more Smart Citation

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

Beemelmanns

Roth

2016

Ecology and Evolution

Self Cite

View full text Add to dashboard Cite

show abstract

“…For primer design, we used a set of pipefish and cichlid candidate genes taken from Diepeveen et al. () and Beemelmanns and Roth () and blasted them against available cichlid transcriptome resources from GenBank (Baldo et al. ; Brawand et al.…”

Section: Methodsmentioning

confidence: 99%

“…To standardize relative gene expression assays, the mean of the two reference genes was subtracted from the mean C t value of the gene of interest, i.e. –Δ C t values were used for statistical analysis (as in (Beemelmanns and Roth )). In total, we thus obtained –Δ C t values for 28 genes.…”

Section: Methodsmentioning

confidence: 99%

Effects of parental care on resource allocation into immune defense and buccal microbiota in mouthbrooding cichlid fishes*

et al. 2018

Self Cite

View full text Add to dashboard Cite

Sexual dimorphism is founded upon a resource allocation trade-off between investments in reproduction versus other life-history traits including the immune system. In species with conventional parental care roles, theory predicts that males maximize their lifetime reproductive success by allocating resources toward sexual selection, while females achieve this through prolonging their lifespan. Here, we examine the interrelation between sexual dimorphism and parental care strategies in closely related maternal and biparental mouthbrooding cichlid fishes from East African Lake Tanganyika. We measured cellular immune parameters, examined the relative expression of 28 immune system and life history-related candidate genes and analyzed the microbiota composition in the buccal cavity. According to our predictions, maternal mouthbrooders are more sexually dimorphic in immune parameters than biparental mouthbrooders, which has possibly arisen through a differential resource allocation into parental care versus secondary sexual traits. Biparental mouthbrooders, on the other hand, which share the costs of parental care, feature an upregulated adaptive immune response and stronger antiviral properties, while their inflammation response is reduced. Overall, our results suggest a differential resource allocation trade-off between the two modes of parental investment.

show abstract

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

Schneider,

Dubin,

Marten

et al. 2024

Ecology and Evolution

View full text Add to dashboard Cite

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.

show abstract

Biparental immune priming in the pipefish Syngnathus typhle

Cited by 55 publications

References 70 publications

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

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

Effects of parental care on resource allocation into immune defense and buccal microbiota in mouthbrooding cichlid fishes*

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

Contact Info

Product

Resources

About