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

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

doi:10.1101/2023.09.27.559693

Cited by 3 publications

(3 citation statements)

References 89 publications

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“…Samples were processed as already in Bonzi et al (2023). Briefly, total RNA was isolated from homogenized whole livers using a mir Vana miRNA Isolation kit.…”

Section: Methodsmentioning

confidence: 99%

“…If adaptive, non-genetic inheritance through environmentally induced parental effects might enable acclimation to persistent environmental changes, such as global warming (Donelan et al, 2020; Donelson, Salinas, Munday, & Shama, 2018). In a coral reef fish, the spiny chromis Acanthochromis polyacanthus (Bleeker 1855), for instance, studies have shown that parental developmental exposure to elevated temperature can provide transgenerational acclimation to ocean warming and restoration of aerobic scope in offspring through molecular changes in lipid and carbohydrate metabolism, as well as immune system and transcriptional regulation (Bernal, Ravasi, Rodgers, Munday, & Donelson, 2021; Bernal, Schmidt, Donelson, Munday, & Ravasi, 2022; Bonzi et al, 2023; Donelson, Munday, McCormick, & Pitcher, 2012; Ryu, Veilleux, Donelson, Munday, & Ravasi, 2018; Veilleux et al, 2015). The relative importance of fathers and mothers in such acclimation process, however, is unknown, but has implications on adaptive potential.…”

Section: Introductionmentioning

confidence: 99%

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Matching maternal and paternal experiences underpin molecular thermal acclimation

Bonzi,

Donelson,

Spinks

et al. 2023

Preprint

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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 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 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 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.

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“…Samples were processed as already in Bonzi et al (2023). Briefly, total RNA was isolated from homogenized whole livers using a mir Vana miRNA Isolation kit.…”

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Matching maternal and paternal experiences underpin molecular thermal acclimation

Bonzi,

Donelson,

Spinks

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…RNA-seq data can be found under the BioProject PRJNA998209. Electronic supplementary material is available online [89]. Declaration of AI use.…”

mentioning

confidence: 99%

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

Bonzi,

Spinks,

Donelson

et al. 2024

Proc. R. Soc. B.

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Population and species persistence in a rapidly warming world will be determined by an organism’s 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 effects of two critical ontogenetic stages (juvenile development and reproduction) to the new-generation acclimation potential, by exposing the spiny chromis damselfish Acanthochromis polyacanthus to simulated ocean warming across two generations. By using hepatic transcriptomics, we discovered that the post-hatching 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 offspring’s response to warming. Conversely, parental reproduction and offspring embryogenesis in warmer water elicited stress response mechanisms in the offspring, with suppression of translation and mitochondrial respiration. Mismatches between parental developmental and reproductive temperatures deeply affected offspring gene expression profiles, and detrimental effects were evident when warming occurred both during parents’ development and reproduction. This study reveals that the previous generation’s developmental temperature contributes substantially to thermal acclimation potential during early life; however, exposure at reproduction as well as prolonged heat stress will likely have adverse effects on the species’ persistence.

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Matching maternal and paternal experiences underpin molecular thermal acclimation

Bonzi,

Donelson,

Spinks

et al. 2024

Molecular Ecology

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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.

show abstract

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

Cited by 3 publications

References 89 publications

Matching maternal and paternal experiences underpin molecular thermal acclimation

Matching maternal and paternal experiences underpin molecular thermal acclimation

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

Matching maternal and paternal experiences underpin molecular thermal acclimation

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