Spinks, R. K. | bioRxiv Science

bioRxiv2023

Matching maternal and paternal experiences underpin molecular thermal acclimation

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{degrees}C) in a full factorial design and analyzing the F2 hepatic gene expression. Paternal and maternal effects showed common but also parent-specific components, with the father having the largest influence in shaping the offspring transcriptomic profile. Fathers contributed to transgenerational response to warming through transfer of epigenetically controlled stress-response mechanisms while mothers influenced increased 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 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 offsprings own environmental experience had the smallest influence on their hepatic transcription profiles. Taken together, our results show the complex nature of the interplay between paternal, maternal and offspring cue integration, and reveal that acclimation potential to ocean warming depends not only on maternal and paternal contributions, but importantly on congruent parental thermal experiences.

evolutionary biology↗

bioRxiv2023

Timing specific parental effects of ocean warming in a coral reef fish

Population and species persistence in a rapidly warming world will be determined by an organisms ability to acclimate to warmer conditions, especially across generations. There is potential for transgenerational acclimation, but the importance of ontogenetic timing in the transmission of environmentally induced parental effects remains mostly unknown. We aimed to disentangle the contributions of two critical ontogenetic stages (juvenile development and adult reproduction) to transgenerational plasticity, by exposing the coral reef fish Acanthochromis polyacanthus to simulated ocean warming with natural diel thermal fluctuations across two generations. By using hepatic transcriptomics, we discovered that the developmental environment of the offspring themselves had little effect on their acclimation potential at 2.5 months of life. Instead, the developmental experience of parents increased regulatory RNA production and protein synthesis, which could improve the offsprings response to warming. Conversely, reproduction in warmer water elicited stress response mechanisms, with suppression of translation and mitochondrial respiration. Mismatches between temperatures in the parental ontogenetic thermal experience deeply affected offspring gene expression profiles, and detrimental effects were also evident when warming occurred both during parents development and reproduction. This study reveals that the previous generations developmental temperature contributes substantially to thermal acclimation potential during early life, however prolonged heat stress will likely have adverse effects on the species persistence.

evolutionary biology↗