Data_Sheet_1_Distinct Bleaching Resilience of Photosynthetic Plastid-Bearing Mollusks Under Thermal Stress and High CO2 Conditions.docx

The impact of temperature on photo-symbiotic relationships has been highly studied in the tropical reef-forming corals but overlooked in less charismatic groups such as solar-powered sacoglossan sea slugs. These organisms display one of the most puzzling symbiotic features observed in the animal kingdom, i.e., their mollusk-plastid association, which enables them to retain photosynthetic active chloroplasts (i.e., kleptoplasts) retrieved from their algae feed sources. Here we analyze the impact of thermal stress (+4°C) and high pCO2 conditions (ΔpH = 0.4) in survival, photophysiology (i.e., bleaching, photosynthetic efficiency, and metabolism) and stress defense mechanisms (i.e., heat shock and antioxidant response) of solar-powered sacoglossan sea slugs, from tropical (Elysia crispata) and temperate (E. viridis) environments. High temperature was the main factor affecting the survival of both species, while pH only affected the survival of the temperate model. The photobiology of E. viridis remained stable under the combined scenario, while photoinhibition was observed for E. crispata under high temperature and high pCO2. In fact, bleaching was observed within all tropical specimens exposed to warming (but not in the temperate ones), which constitutes the first report where the incidence of bleaching in tropical animals hosting photosynthetic symbionts, other than corals, occurs. Yet, the expulsion of kleptoplasts by the tropical sea slug, allied with metabolic depression, constituted a physiological response that did not imply signs of vulnerability (i.e., mortality) in the host itself. Although the temperate species revealed greater heat shock and antioxidant enzyme response to environmental stress, we argue that the tropical (stenotherm) sea slug species may display a greater scope for acclimatization than the temperate (eurytherm) sea slug. E. crispata may exhibit increased capacity for phenotypic plasticity by increasing fitness in a much narrower thermal niche (minimizing maintenance costs), which ultimately may allow to face severe environmental conditions more effectively than its temperate generalist counterpart (E. viridis).

温度对光合共生关系的影响在造礁热带珊瑚中已得到广泛研究，但在太阳能型囊舌海蛞蝓（solar-powered sacoglossan sea slugs）这类关注度较低的类群中却被忽视。这类生物展现出动物界中最令人费解的共生特征之一：软体动物-质体共生关系，使其能够留存从藻类食源中获取的具有光合活性的叶绿体（盗食质体，kleptoplasts）。本研究针对分别采自热带生境的绿叶海天牛（Elysia crispata）与温带生境的（Elysia viridis，简称E. viridis）两类太阳能型囊舌海蛞蝓，分析了热胁迫（升温4℃）与高pCO₂条件（ΔpH=0.4）对其存活、光生理（即白化、光合效率与代谢）以及胁迫防御机制（即热休克响应与抗氧化应答）的影响。研究结果显示，高温是影响两个物种存活的核心因素，而pH仅对温带物种的存活产生显著影响。在复合胁迫条件下，E. viridis的光生理状态保持稳定，而E. crispata在高温与高pCO₂环境下出现光抑制现象。事实上，所有暴露于升温环境的热带个体均出现白化现象（温带个体未出现此类情况），这是首次报道除珊瑚外，携带光合共生体的热带动物发生白化事件。然而，热带囊舌海蛞蝓排出盗食质体并伴随代谢抑制的生理响应，并未使宿主自身出现易感性迹象（即死亡）。尽管温带物种对环境胁迫表现出更强的热休克与抗氧化酶响应，但本研究认为，热带狭温性（stenotherm）囊舌海蛞蝓相比温带广温性（eurytherm）类群，具备更广阔的驯化适应潜力。E. crispata可通过在更狭窄的热生态位中提升适合度（降低维持成本）增强表型可塑性（phenotypic plasticity），最终使其相较于温带广适性同类群（E. viridis），能够更高效地应对极端环境条件。