Heat shock induces delayed development leading to carryover effects in the sea anemone Nematostella vectensis

Exposure to stressful environmental conditions during development can disrupt developmental progression in animals and induce lasting physiological effects. Animals can lessen negative effects of stress through physiological and developmental plasticity, yet these processes and associated molecular mechanisms remain uncharacterized in most species. This is an increasingly urgent question for marine invertebrates, which often have externally developing early life stages that are threatened by climate change. We hypothesized that the sea anemone Nematostella vectensis —a marine invertebrate adapted to highly variable conditions including diel temperature fluctuations of > 20 °C—would exhibit developmental plasticity. To test this, we characterized developmental rates, physiology, and gene expression in N. vectensis larvae and juveniles following exposure to transient sublethal heat shock (1 h at 39 °C, which was 21 °C above ambient of 18 °C) as larvae. Heat shock led to delayed development following return to ambient, with transcriptomic changes indicating a pronounced stress response that included activation of heat shock and innate immunity pathways. Larvae exposed to heat shock also displayed evidence of metabolic disruption including the rapid depletion of lipid stores and a transient decrease in aerobic respiration rate. Further, despite over a week of recovery under ambient conditions, juveniles previously exposed to heat shock as larvae displayed negative carryover effects including reduced sizes and heat tolerance, which were likely the result of heat-induced cellular damage and metabolic disruption. These findings demonstrate that the environment shapes developmental outcomes in N. vectensis , and provide insights into the mechanisms underlying cnidarian developmental plasticity. These results also highlight that even estuarine species adapted to high thermal variability can be negatively affected by hyperthermal stress, emphasizing the importance of rapid intervention to limit further ocean warming.