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Epigenetic processes are proposed to be a mechanism regulating gene expression during phenotypic plasticity. However, environmentally induced changes in DNA methylation exhibit little-to-no association with differential gene expression in metazoans at a transcriptome-wide level. It remains unexplored whether associations between environmentally induced differential methylation and expression are contingent upon other epigenomic processes such as chromatin accessibility. We quantified methylation and gene expression in larvae of the purple sea urchinStrongylocentrotus purpuratusexposed to different ecologically relevant conditions during gametogenesis (maternal conditioning) and modeled changes in gene expression and splicing resulting from maternal conditioning as functions of differential methylation, incorporating covariates for genomic features and chromatin accessibility. We detected significant interactions between differential methylation, chromatin accessibility, and genic feature type associated with differential expression and splicing.

Differential gene body methylation had significantly stronger effects on expression among genes with poorly accessible transcriptional start sites while baseline transcript abundance influenced the direction of this effect. Transcriptional responses to maternal conditioning were 4–13 × more likely when accounting for interactions between methylation and chromatin accessibility, demonstrating that the relationship between differential methylation and gene regulation is partially explained by chromatin state.

DNA methylation likely possesses multiple associations with gene regulation during transgenerational plasticity inS. purpuratusand potentially other metazoans,but its effects are dependent on chromatin accessibility and underlying genic features.

 

Marine heatwaves (MHWs) are projected to increase in intensity and frequency over the coming decades, and it is imperative to assess the adaptive capacity of marine organisms to these extreme temperature events. Given the nature of MHWs to last days to weeks in a region, these events may have overarching impacts on phenological events like reproduction and development. Here, the role of adult thermal history and transgenerational plasticity may be an important pathway by which MHWs are transduced to impact community structure. In this study, we sought to explore the effects of paternal thermal history in the purple urchin,Strongylocentrotus purpuratus, on a crucial aspect of reproduction, fertilization. Using ecologically relevant temperatures representative of both MHW events that occurred in 2014–2020 and non-MHW temperatures in our region of the California Large Marine Ecosystem, we conditioned maleS. purpuratusfor 28 days to either a high, MHW or a low, non-MHW temperature. Following the temperature acclimation of adults, sperm performance was tested for individual males by conducting fertilization success trials at varying temperatures and sperm concentrations. While sperm appeared robust to elevated temperature during fertilization, sperm produced by high-temperature-acclimated males had overall diminished performance as compared to those acclimated to non-MHW temperatures. These results suggest MHW events will have a negative impact on fertilization in situ forS. purpuratuspopulations. Furthermore, these results highlight the importance of considering both male and female environmental history in projections of reproduction under climate change scenarios.

 

Phenotypic plasticity and adaptive evolution enable population persistence in response to global change. However, there are few experiments that test how these processes interact within and across generations, especially in marine species with broad distributions experiencing spatially and temporally variable temperature and p CO 2 . We employed a quantitative genetics experiment with the purple sea urchin, Strongylocentrotus purpuratus , to decompose family-level variation in transgenerational and developmental plastic responses to ecologically relevant temperature and p CO 2 . Adults were conditioned to controlled non-upwelling (high temperature, low p CO 2 ) or upwelling (low temperature, high p CO 2 ) conditions. Embryos were reared in either the same conditions as their parents or the crossed environment, and morphological aspects of larval body size were quantified. We find evidence of family-level phenotypic plasticity in response to different developmental environments. Among developmental environments, there was substantial additive genetic variance for one body size metric when larvae developed under upwelling conditions, although this differed based on parental environment. Furthermore, cross-environment correlations indicate significant variance for genotype-by-environment interactive effects. Therefore, genetic variation for plasticity is evident in early stages of S. purpuratus , emphasizing the importance of adaptive evolution and phenotypic plasticity in organismal responses to global change.