Summary:

The transfer of immunity from mothers to offspring (trans-generational immune priming) yields in an improved offspring immunity and an induced parasite resistance. In teleost this occurs via maternal deposition of antibodies into the egg yolk. As yet, the paternal contribution to offspring immunity was suggested to be negligible because sperm are too small for a transfer over the scope of the DNA. Syngnathids like the sex-role reversed pipefish Syngnathus typhle have evolved a paternal placenta-like structure, in which embryos are nursed. This gives a mechanistic opportunity for paternal transfer of immunity but also implies that offspring are born in the paternal environment and thus share a similar parasite pressure. Hence, strong selection for the evolution of paternal immune priming can be expected.
We experimentally investigated the potential of maternal, paternal and bi-parental immune priming on offspring cell activity and gene expression patterns. We found that offspring’s immune defence was enhanced upon parental bacteria exposure, independent of whether mother, father or both were challenged. This suggests that male pregnancy let to the evolution of bi-parental immune priming. Classically, maternal immune priming is considered to be of higher importance due to the fact that mothers invest more resources in production and care of offspring. However, since in sex-role reversal males do not only have an intense paternal investment but also realize evolutionary maternal traits like a more efficient immune response, selection pressures for paternal immune priming should be stronger. As immune priming is expected to be energetically costly for both parents and offspring, life history parameters provide clarification about incorporated costs and benefits. Further, future data will give insights in the mechanistic basis of bi-parental immune priming and assess what role antibodies, innate immunity and epigenetics play.

Summary:

The red flour beetle, Tribolium castaneum, secretes quinones that control the microbial flora in the surrounding environment. These secretions act as an external immune defense that provides protection against pathogens. At high concentrations, however, these secretions are harmful to the host itself, and selection may thus have optimized the level of expression under natural conditions. Here we show that the expression of external immunity responded to selection during experimental evolution within a few generations. At the same time, one component of internal immune defense (phenoloxidase activity) was compromised in beetles selected for either high or low external defenses. Protection against a natural pathogen was lacking in flour obtained from beetle lines selected for low amounts of secretions. Altogether, this suggests that external and internal immune defenses work together efficiently under natural conditions, while every manipulation on the side of external immune defense comes with costs to the internal immune defense.