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Bacteria-type-specific biparental immune priming in the pipefish Syngnathus typhle.

ABSTRACT: 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.

SUBMITTER: Beemelmanns A

PROVIDER: S-EPMC5058542 | biostudies-literature | 2016 Sep

REPOSITORIES: biostudies-literature

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

Beemelmanns Anne A Roth Olivia O

Ecology and evolution 20160831 18

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 <i>Syngnathus typhle,</i> fathers nurse the embryos over a placenta-like structure, which opens the door for additional paternal immune priming. We examined the pot ...[more]

PMID: 27777744

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Project description:Empirical evidence of immune priming in arthropods keeps growing, both at the within- and trans-generational level. The evidence comes mostly from work on insects and it remains unclear for some other arthropods whether exposure to a non-lethal dose of a pathogen provides protection during a second exposure with a lethal dose. A poorly investigated group are arachnids, with regard to the benefits of immune priming measured as improved survival. Here, we investigated immune priming in two arachnids: the wolf spider Lycosa cerrofloresiana and the scorpion Centruroides granosus. We injected a third of the individuals with lipopolysaccharides of Escherichia coli (LPS, an immune elicitor), another third were injected with the control solution (PBS) and the other third were kept naive. Four days after the first inoculations, we challenged half of the individuals of each group with an injection of a high dose of E. coli and the other half was treated with the control solution. For scorpions, individuals that were initially injected with PBS or LPS did not differ in their survival rates against the bacterial challenge. Individuals injected with LPS showed higher survival than that of naive individuals as evidence of immune priming. Individuals injected with PBS tended to show higher survival rates than naive individuals, but the difference was not significant-perhaps suggesting a general immune upregulation caused by the wounding done by the needle. For spiders, we did not observe evidence of priming, the bacterial challenge reduced the survival of naive, PBS and LPS individuals at similar rates. Moreover; for scorpions, we performed antibacterial assays of hemolymph samples from the three priming treatments (LPS, PBS and naive) and found that the three treatments reduced bacterial growth but without differences among treatments. As non-model organisms, with some unique differences in their immunological mechanisms as compared to the most studied arthropods (insects), arachnids provide an unexplored field to elucidate the evolution of immune systems.

Dataset Information

Bacteria-type-specific biparental immune priming in the pipefish Syngnathus typhle.

Publications

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

Similar Datasets

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