Early-Life Exposure to Warming Enhances Sea Urchin Heatwave Tolerance but Fails under Extreme Stress

The exposure to environmental stressors early in life can shape organisms to express more tolerant phenotypes to the same conditions during adulthood, a process called developmental plasticity. However, this acquired acclimation ability might depend on the intensity of the stimulus perceived later in life. Here, we took advantage of a purple sea urchin Paracentrotus lividus population developed at abnormally high sea temperature in the proximity of a power plant to test the limits of their developmentally acquired plasticity to increased water temperature. We simulated two marine heatwaves, a category I (moderate) and IV (extreme), and exposed the power plant population as well as a naive population developed in natural sea conditions. We measured their respiration rate and molecular responses to these two heatwaves. Regardless of the population of origin, sea urchins exposed to heatwaves showed higher oxygen consumption, indicating an increase in metabolic rates. At the molecular level, the biggest difference between the two populations was found following the moderate heatwave. Compared to the developmentally acclimated sea urchins, the naive population expressed genes coding for proteins with stress response, chromatin remodeling and RNA splicing functions, while suppressing immune response, revealing that developmental exposures can aid in priming the responses of adults to moderate temperature increases. However, a stronger heatwave leveled the differences between the two populations, with sea urchins from both locations expressing genes involved in proteostasis and detoxification. Nevertheless, regardless of the simulated marine heatwave intensity, sea urchins from the naive population always showed enrichment of the spliceosome pathway compared to power plant urchins, which activated immune response genes instead, reflecting fundamentally different thermal stress-coping strategies shaped by their developmental environments. Overall, our results demonstrate the critical yet context-dependent role of developmental plasticity in shaping the resilience of marine ectotherms to climate change.