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Marine heatwave (MHW) events, characterized by periods of anomalous temperatures, are an increasingly prevalent threat to coastal marine ecosystems. Given the seasonal phenology of MHWs, the full extent of their biological consequences may depend on how these thermal stress events align with an organism’s reproductive cycle. In organisms with more complex life cycles (e.g., many marine invertebrate species) the alignment of adult and larval environments may be an important factor determining offspring success, setting the stage for MHW events to influence reproduction and development in situ . Here, the influence of MHW-like temperatures on the early development of the California purple sea urchin, Strongylocentrotus purpuratus , were explored within the context of paternal thermal history. Based on temperature data collected during MHW events seen in Southern California from 2014–2020, adult urchins were acclimated to either MHW or non-MHW temperatures for 28 days before their sperm was used to produce embryos that were subsequently raised under varying thermal conditions. Once offspring reached an early larval stage, the impact of paternal and offspring environments were assessed on two aspects of offspring performance: larval size and thermal tolerance. Exposure to elevated temperatures during early development resulted in larger, more thermally tolerant larvae, with further influences of paternal identity and thermal history, respectively. The alignment of paternal and offspring exposure to MHW temperatures had additional positive benefits on larval thermal tolerance, but this tolerance significantly decreased when their thermal experience mismatched. As the highest recorded temperatures within past MHW events have occurred during the gametogenesis of many kelp forest benthic marine invertebrate species, such as the purple sea urchin, such parental mediated impacts may represent important drivers of future recruitment and population composition for these species. 

Kelp forests of the California Current System have experienced prolonged marine heatwave (MHW) events that overlap in time with the phenology of life history events (e.g., gametogenesis and spawning) of many benthic marine invertebrates. To study the effect of thermal stress from MHWs during gametogenesis in the purple sea urchin ( Strongylocentrotus purpuratus ) and further, whether MHWs might induce transgenerational plasticity (TGP) in thermal tolerance of progeny, adult urchins were acclimated to two conditions in the laboratory – a MHW temperature of 18°C and a non-MHW temperature of 13°C. Following a four-month long acclimation period (October–January), adults were spawned and offspring from each parental condition were reared at MHW (18°C) and non-MHW temperatures (13°C), creating a total of four embryo treatment groups. To assess transgenerational effects for each of the four groups, we measured thermal tolerance of hatched blastula embryos in acute thermal tolerance trials. Embryos from MHW-acclimated females were more thermally tolerant with higher LT 50 values as compared to progeny from non-MHW-acclimated females. Additionally, there was an effect of female acclimation state on offspring body size at two stages of embryonic development - early gastrulae and prism, an early stage echinopluteus larvae. To assess maternal provisioning as means to also alter embryo performance, we assessed gamete traits from the differentially acclimated females, by measuring size and biochemical composition of eggs. MHW-acclimated females had eggs with higher protein concentrations, while egg size and lipid content showed no differences. Our results indicate that TGP plays a role in altering the performance of progeny as a function of the thermal history of the female, especially when thermal stress coincides with gametogenesis. In addition, the data on egg provisioning show that maternal experience can influence embryo traits via egg protein content. Although this is a laboratory-based study, the results suggest that TGP may play a role in the resistance and tolerance of S. purpuratus early stages in the natural kelp forest setting. 

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.

 

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. 

Abstract Background The red sea urchin Mesocentrotus franciscanus is an ecologically important kelp forest herbivore and an economically valuable wild fishery species. To examine how M. franciscanus responds to its environment on a molecular level, differences in gene expression patterns were observed in embryos raised under combinations of two temperatures (13 °C or 17 °C) and two p CO 2 levels (475 μatm or 1050 μatm). These combinations mimic various present-day conditions measured during and between upwelling events in the highly dynamic California Current System with the exception of the 17 °C and 1050 μatm combination, which does not currently occur. However, as ocean warming and acidification continues, warmer temperatures and higher p CO 2 conditions are expected to increase in frequency and to occur simultaneously. The transcriptomic responses of the embryos were assessed at two developmental stages (gastrula and prism) in light of previously described plasticity in body size and thermotolerance under these temperature and p CO 2 treatments. Results Although transcriptomic patterns primarily varied by developmental stage, there were pronounced differences in gene expression as a result of the treatment conditions. Temperature and p CO 2 treatments led to the differential expression of genes related to the cellular stress response, transmembrane transport, metabolic processes, and the regulation of gene expression. At each developmental stage, temperature contributed significantly to the observed variance in gene expression, which was also correlated to the phenotypic attributes of the embryos. On the other hand, the transcriptomic response to p CO 2 was relatively muted, particularly at the prism stage. Conclusions M. franciscanus exhibited transcriptomic plasticity under different temperatures, indicating their capacity for a molecular-level response that may facilitate red sea urchins facing ocean warming as climate change continues. In contrast, the lack of a robust transcriptomic response, in combination with observations of decreased body size, under elevated p CO 2 levels suggest that this species may be negatively affected by ocean acidification. High present-day p CO 2 conditions that occur due to coastal upwelling may already be influencing populations of M. franciscanus . 

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.