Matching maternal and paternal experiences underpin molecular thermal acclimation.

climate change coral reef fish gene expression non‐genetic inheritance transcriptomics transgenerational plasticity

Journal

Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478

Informations de publication

Date de publication:
23 Mar 2024
Historique:
revised: 25 01 2024
received: 04 10 2023
accepted: 04 03 2024
medline: 23 3 2024
pubmed: 23 3 2024
entrez: 23 3 2024
Statut: aheadofprint

Résumé

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.

Identifiants

pubmed: 38520127
doi: 10.1111/mec.17328
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e17328

Subventions

Organisme : Sea World Research and Rescue Foundation Marine Vertebrate Grant
ID : SWR/9/2018
Organisme : King Abdullah University of Science and Technology (KAUST) Competitive Research Grant
ID : CRG3 2278
Organisme : Okinawa Institute of Science and Technology (OIST)
Organisme : University of Hong Kong (HKU)
Organisme : Research Grants Council (Hong Kong) General Research Fund
ID : GRF17300721
Organisme : Centre of Excellence for Coral Reef Studies, Australian Research Council

Informations de copyright

© 2024 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

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Auteurs

L C Bonzi (LC)

The Swire Institute of Marine Science, School of Biological Sciences, The University of Hong Kong, Hong Kong, Hong Kong SAR.

J M Donelson (JM)

ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland, Australia.
College of Science and Engineering, James Cook University, Townsville, Queensland, Australia.

R K Spinks (RK)

ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland, Australia.
Blue Carbon Section, Australian Government Department of Climate Change, Energy, the Environment and Water, Canberra, Australian Capital Territory, Australia.

P L Munday (PL)

ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland, Australia.
College of Science and Engineering, James Cook University, Townsville, Queensland, Australia.

T Ravasi (T)

ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland, Australia.
Marine Climate Change Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan.

C Schunter (C)

The Swire Institute of Marine Science, School of Biological Sciences, The University of Hong Kong, Hong Kong, Hong Kong SAR.
State Key Laboratory of Marine Pollution and Department of Chemistry, City University of Hong Kong, Hong Kong, Hong Kong SAR.

Classifications MeSH