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

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.