Embryonic hormetic priming modulates later-life thermal tolerance

Understanding the mechanisms explaining thermal tolerance variation is crucial for predicting the impact of climate change on ectotherms, especially those living near their upper thermal limits. Among the various forms of plasticity, developmental plasticity holds promise as an adaptive trait for marine ectotherms to buffer the negative effects of ocean warming; however, its underlying molecular mechanisms remain poorly understood. Here we examine the capacity of two bi-parental progenies of the black-lip pearl oyster, Pinctada margaritifera, to modify their later-life thermal tolerance and performance, through developmental thermal priming. Embryos (3-24 hours post-fertilization) were incubated until hatching at either control (28°C) or warm (32°C; ecological extremes) temperatures, and raised four months under common conditions at 28°C. Our results reveal family-specific effects of early-life thermal priming, significantly enhancing spat thermal tolerance in one family, while reducing it in the other. Main molecular pathways of heat stress response (at the sublethal temperature of 34°C) were conserved across families and independent of the early-life priming treatment. Nevertheless, a network-preservation approach allowed further characterizing the subtle, nested environmental ‘memory’ mediated through network reorganization, particularly in gene regulatory pathways involved in the Unfolding Protein Response (UPR). This study revealed a complex relationship between early environments and later phenotypes, but still holds out the promise of hormetic priming for ecological conservation and aquaculture improvement.