Transgenerational effects alter the fitness consequences and genetic architecture of phenotypic plasticity and its regulatory pathways

Parental exposure to environmental stress can influence phenotypic plasticity by offspring developing under that stressor. Transgenerational effects may also reshape natural selection on developmental plasticity by influencing its fitness consequences and expression of its genetic variation. We tested these hypotheses in the purple sea urchin Strongylocentrotus purpuratus , an invertebrate exposed to coastal upwelling (periods of low temperature and pH impacting biomineralization and performance). We conditioned parents and larvae to experimental upwelling and integrated RNA-seq, phenotyping of body size and biomineralization, and measured fitness-correlated traits in a quantitative genetic experiment. Larvae developing under upwelling induced widespread differential expression (DE), decreased biomineralization, and reduced body size. We detected fitness benefits for increased biomineralization and reduced size under upwelling indicative of adaptive plasticity, but only when larvae were spawned from parents exposed to upwelling. Larval DE was largely associated with adaptive phenotypic plasticity. Negative genetic correlation in DE was abundant between genes associated with adaptive plasticity. However, genetic correlations in DE associated with body size plasticity were significantly more positive in larvae from upwelling-exposed parents. These results show that transgenerational effects modify the fitness landscape and genetic architecture of phenotypic plasticity and its regulatory pathways.