Matching maternal and paternal experiences underpin molecular thermal acclimation

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.