Matching maternal and paternal experiences underpin molecular thermal acclimation

L C Bonzi; J M Donelson; R K Spinks; P L Munday; T Ravasi; C Schunter

doi:10.1111/mec.17328

Matching maternal and paternal experiences underpin molecular thermal acclimation

Mol Ecol. 2024 Mar 23:e17328. doi: 10.1111/mec.17328. Online ahead of print.

Authors

L C Bonzi¹, J M Donelson^{2

3}, R K Spinks^{2

4}, P L Munday^{2

3}, T Ravasi^{2

5}, C Schunter^{1

6}

Affiliations

¹ The Swire Institute of Marine Science, School of Biological Sciences, The University of Hong Kong, Hong Kong, Hong Kong SAR.
² ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland, Australia.
³ College of Science and Engineering, James Cook University, Townsville, Queensland, Australia.
⁴ Blue Carbon Section, Australian Government Department of Climate Change, Energy, the Environment and Water, Canberra, Australian Capital Territory, Australia.
⁵ Marine Climate Change Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan.
⁶ State Key Laboratory of Marine Pollution and Department of Chemistry, City University of Hong Kong, Hong Kong, Hong Kong SAR.

PMID: 38520127
DOI: 10.1111/mec.17328

Abstract

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.

Keywords: climate change; coral reef fish; gene expression; non‐genetic inheritance; transcriptomics; transgenerational plasticity.

Abstract

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