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

L. C. Bonzi^*
, J. M. Donelson
, R. K. Spinks
, P. L. Munday
, T. Ravasi
, C. Schunter^*

^*Corresponding author for this work

Research output: Journal Publications and Reviews › RGC 21 - Publication in refereed journal › peer-review

7 Citations (Scopus)

26 Downloads (CityUHK Scholars)

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

Original language	English
Article number	e17328
Number of pages	17
Journal	Molecular Ecology
Volume	34
Issue number	15
Online published	23 Mar 2024
DOIs	https://doi.org/10.1111/mec.17328
Publication status	Published - Aug 2025
Externally published	Yes

Funding

The authors acknowledge the support of the University of Hong Kong (HKU) startup fund (C.S.), Research Grants Council (Hong Kong) General Research Fund (GRF17300721), the King Abdullah University of Science and Technology (KAUST) Competitive Research Grant (CRG3 2278), the Okinawa Institute of Science and Technology (OIST) (T.R.), a Sea World Research and Rescue Foundation Marine Vertebrate Grant (SWR/9/2018; R.S., P.L.M. & J.M.D.) and the ARC Centre of Excellence for Coral Reef Studies.

Research Keywords

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

Publisher's Copyright Statement

This full text is made available under CC-BY-NC 4.0. https://creativecommons.org/licenses/by-nc/4.0/

RGC Funding Information

RGC-funded

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10.1111/mec.17328

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title = "Matching maternal and paternal experiences underpin molecular thermal acclimation",

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. {\textcopyright} 2024 The Authors. Molecular Ecology published by John Wiley \& Sons Ltd.",

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author = "Bonzi, \{L. C.\} and Donelson, \{J. M.\} and Spinks, \{R. K.\} and Munday, \{P. L.\} and T. Ravasi and C. Schunter",

year = "2025",

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journal = "Molecular Ecology",

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AU - Bonzi, L. C.

AU - Donelson, J. M.

AU - Spinks, R. K.

AU - Munday, P. L.

AU - Ravasi, T.

AU - Schunter, C.

PY - 2025/8

Y1 - 2025/8

N2 - 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. © 2024 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

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

KW - climate change

KW - coral reef fish

KW - gene expression

KW - non-genetic inheritance

KW - transcriptomics

KW - transgenerational plasticity

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M3 - RGC 21 - Publication in refereed journal

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JF - Molecular Ecology

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Matching maternal and paternal experiences underpin molecular thermal acclimation

Abstract

Funding

Research Keywords

Publisher's Copyright Statement

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