Data for: Parent-specific transgenerational immune priming enhances offspring defense – unless heat stress negates it all

Trans-generational 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.