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Matching maternal and paternal experiences underpin molecular thermal acclimation.

L C Bonzi¹, J M Donelson^2,3, R K Spinks^2,4

¹The Swire Institute of Marine Science, School of Biological Sciences, The University of Hong Kong, Hong Kong, Hong Kong SAR.

Molecular Ecology

|March 23, 2024

Summary

Parental environmental experiences significantly impact offspring acclimation to warming, with fathers playing a larger role. Congruent thermal histories between parents are crucial for adaptive transgenerational responses.

Keywords:

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

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Area of Science:

Environmental epigenetics
Transgenerational inheritance
Reef fish physiology

Background:

Parental environments can influence offspring phenotypes through non-genetic inheritance.
Understanding the integration of maternal, paternal, and offspring experiences is key to predicting adaptive responses.

Purpose of the Study:

To disentangle maternal and paternal contributions to transgenerational thermal acclimation.
To investigate the integration of parental and offspring thermal experiences in reef fish (Acanthochromis polyacanthus).

Main Methods:

A fully factorial design exposed two generations of fish to elevated temperatures (+1.5°C).
Analyzed F2 hepatic gene expression to assess transgenerational effects.
Investigated epigenetic mechanisms and gene expression patterns related to stress and metabolism.

Main Results:

Fathers exerted the largest influence on offspring transcriptomic profiles, transferring epigenetically controlled stress-response mechanisms.
Mothers influenced lipid metabolism gene expression.
Congruent parental thermal experiences enhanced adaptive gene expression (RNA production, transcriptional regulation) in offspring.
Mismatched parental experiences led to maladaptive responses (translation suppression, endoplasmic reticulum stress).
Offspring's own environment had minimal impact on hepatic transcription.

Conclusions:

Parental, particularly paternal, contributions are significant in transgenerational thermal acclimation.
Congruent thermal experiences between parents are critical for successful acclimation.
Ocean warming adaptation may depend on synchronized parental thermal histories, not just individual parental or offspring cues.