Bonzi L C, Donelson J M, Spinks R K, Munday P L, Ravasi T, Schunter C
The Swire Institute of Marine Science, School of Biological Sciences, The University of Hong Kong, Hong Kong, Hong Kong SAR.
ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland, Australia.
Mol Ecol. 2024 Mar 23:e17328. doi: 10.1111/mec.17328.
The environment experienced by one generation has the potential to affect the subsequent one through non-genetic inheritance of parental effects. Since both mothers and fathers can influence their offspring, questions arise regarding how the maternal, paternal and offspring experiences integrate into the resulting phenotype. We aimed to disentangle the maternal and paternal contributions to transgenerational thermal acclimation in a reef fish, Acanthochromis polyacanthus, by exposing two generations to elevated temperature (+1.5°C) in a fully factorial design and analysing the F2 hepatic gene expression. Paternal and maternal effects showed not only common but also parent-specific components, with the father having the largest influence in shaping the offspring's transcriptomic profile. Fathers contributed to transcriptional transgenerational response to warming through transfer of epigenetically controlled stress-response mechanisms while mothers influenced increased gene expression associated with lipid metabolism regulation. However, the key to acclimation potential was matching thermal experiences of the parents. When both parents were exposed to the same condition, offspring showed increased expression of genes related to structural RNA production and transcriptional regulation, whereas environmental mismatch in parents resulted in maladaptive parental condition transfer, revealed by translation suppression and endoplasmic reticulum stress. Interestingly, the offspring's own environmental experience had the smallest influence on their hepatic transcription profiles. Taken together, our results show the complex nature of the interplay among paternal, maternal and offspring cue integration, and reveal that acclimation potential to ocean warming might depend not only on maternal and paternal contributions but importantly on congruent parental thermal experiences.
一代生物所经历的环境有可能通过亲代效应的非遗传继承影响下一代。由于母亲和父亲都能影响其后代，因此就出现了关于母体、父体和后代经历如何整合到最终表型中的问题。我们旨在通过以完全析因设计让两代棘颊雀鲷（Acanthochromis polyacanthus）暴露于升高的温度（+1.5°C）并分析F2代肝脏基因表达，来厘清母体和父体对跨代热适应的贡献。父体和母体效应不仅表现出共同的成分，也表现出亲本特异性成分，其中父亲对塑造后代的转录组图谱影响最大。父亲通过表观遗传控制的应激反应机制的传递，对变暖的转录跨代反应做出贡献，而母亲则影响与脂质代谢调节相关的基因表达增加。然而，适应潜力的关键在于父母的热经历相匹配。当父母双方都暴露于相同条件时，后代中与结构RNA产生和转录调控相关的基因表达增加，而父母环境不匹配则导致适应不良的亲代条件传递，这通过翻译抑制和内质网应激得以揭示。有趣的是，后代自身的环境经历对其肝脏转录图谱的影响最小。综上所述，我们的结果显示了父体、母体和后代线索整合之间相互作用的复杂性，并揭示了对海洋变暖的适应潜力可能不仅取决于母体和父体的贡献，更重要的是取决于父母一致的热经历。
