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Phenotypic plasticity, within and across generations, is a strategy by which organisms can respond rapidly to environmental change. Epigenetic modifications, such as DNA methylation, have been proposed to be involved in phenotypic plasticity. We examined the potential for the environment to mediate both transgenerational and intragenerational plasticity in DNA methylation and phenotypes in early stages of the purple sea urchin, Strongylocentrotus purpuratus, an ecologically important herbivore in kelp forest ecosystems. This approach involved a controlled laboratory experiment where adult urchins were acclimated during gametogenesis to upwelling (similar to 1300 mu atm pCO(2) & 13 degrees C) or non-upwelling (similar to 650 mu atm pCO(2) & 17 degrees C) conditions that are representative of their kelp forest habitat. Progeny from these adults were raised in either high (similar to 1050 mu atm) or low (similar to 450 mu atm) pCO(2) treatments and sampled at three developmental stages. Differences in condition experienced by mothers were associated with differentially methylated genes in the offspring. However, differences in developmental conditions corresponded to little observable effects on gene methylation in the progeny. Variation in gene body methylation across treatments was correlated with body size of the embryos and larvae, illustrating a potential link between transgenerational phenotypic plasticity and DNA methylation. Overall, our results suggest that epigenetic factors such as DNA methylation have the potential to contribute to phenotypic plasticity in a transgenerational framework, and further, that epigenetic processes may act as a mechanism of rapid response to environmental change.