Parent-specific transgenerational immune priming enhances offspring defense - unless heat-stress negates it all

Trans-generational immune priming (TGIP) adjusts offspring immune responses based on parental immunological experiences - a form of trans-generational plasticity predicted to be adaptive when parent-offspring environmental conditions match. In contrast, mis-matches between environmental conditions negate those advantages, rendering TGIP costly when mismatched immunological offspring phenotypes are induced. Particularly maternal TGIP was thought to shape offspring immunological preparedness: mothers eggs contain more substance than sperm and, in viviparous species, pregnancy provides additional avenues for immune priming of developing offspring. The syngnathids (pipefishes and seahorses) unique male pregnancy provides an unusual perspective to the ecological relevance of TGIP in a system where egg production and pregnancy occur in different sexes. We simulated parental bacteria exposure in broad nosed pipefish, Syngnathus typhle, through vaccinations with heat-killed Vibrio aestuarianus before mating the fish to each other or control individuals. Resulting offspring were raised, and some exposed to V. aestuarianus, in a control or heat-stress environment, 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 environments. Transcriptomic phenotypes elicited by maternal and paternal TGIP had only limited overlap and were not additive. Both transcriptomic responses were significantly associated to immune functions, and specifically the paternal response to the innate immune branch. TGIP of both parents reduced the relative abundance of the experimental Vibrio in exposed offspring, showcasing its ecological effectiveness. Despite its significance in matching biotic environments, no TGIP-associated phenotypes were observed for heat-treated offspring. Heat-spikes caused by climate change thus threaten TGIP benefits, potentially increasing susceptibility to emerging marine diseases. This highlights the urgent need to understand how animals will cope with climate-induced changes in microbial assemblages by illustrating the importance - and limits - of TGIP in mitigating the impacts of environmental stressors on offspring vulnerability.