Data from: Larval UV exposure impairs adult immune function through a trade-off with larval investment in cuticular melanin

Despite the strong impact of ultraviolet (UV) radiation on invertebrates, it is unknown whether it affects immune function across metamorphosis. More generally, the mechanisms on how larval stressors bridge metamorphosis and shape adult fitness in animals with a complex life cycle remain poorly understood. We studied whether cuticular melanin content is upregulated under UV exposure in the larval stage of the damselfly Coenagrion puella and whether this is traded off across metamorphosis against a key component of the invertebrate immune response, the melanotic encapsulation response, in the adult stage. Larvae exposed to UV increased the melanin content in their exoskeleton and metamorphosed later and at a smaller mass than animals reared without UV. Across metamorphosis, this was associated with a reduced melanotic encapsulation response, thereby constituting the first proof for a UV driven impaired immune response in an invertebrate. The demonstrated costs of UV exposure in terms of age and mass at metamorphosis and reduced adult immune response likely translate into reduced adult fitness. Path analysis indicated that the immunosuppressive property of larval UV exposure was not mediated by age and mass at metamorphosis, but instead that the adult immune response was traded off against larval cuticular melanin investment. Melanin-based trade-off across metamorphosis provide a new pathway by which effects of larval stressors are carried over to the adult stage and thereby advances our understanding of the still largely enigmatic mechanisms of carryover effects of larval stressors across metamorphosis. Given the mechanistic base, this carryover effect of larval UV exposure on adult immune function is expected to be general and may constitute a widespread and important cost of UV exposure in invertebrates.

尽管紫外线（UV）辐射对无脊椎动物具有显著影响，但目前尚不清楚其是否会在变态过程中影响免疫功能。更广泛而言，对于具有复杂生命周期的动物而言，幼虫期胁迫因子如何衔接变态过程并塑造成虫适合度的相关机制，目前仍知之甚少。本研究以豆娘（Coenagrion puella）的幼虫为研究对象，探究其在UV辐射暴露下的表皮黑色素含量是否会上调，以及这种上调是否会在变态过程中，与成虫阶段无脊椎动物免疫反应的关键组分——黑化包囊反应产生权衡。经UV辐射暴露的幼虫，其外骨骼黑色素含量显著升高，且与未暴露于UV辐射的个体相比，它们的变态时间更晚，变态时的体重更小。贯穿整个变态过程，这种表皮黑色素含量的上调与成虫黑化包囊反应的减弱存在关联，这也是首个证明UV辐射会导致无脊椎动物免疫功能受损的证据。本研究证实的UV辐射暴露带来的代价——包括变态时的发育时长与体重变化，以及成虫免疫反应减弱——很可能会导致成虫适合度下降。路径分析结果显示，幼虫期UV辐射暴露所带来的免疫抑制效应，并非由变态时的年龄与体重所介导；相反，成虫的免疫反应与幼虫期表皮黑色素的资源投入之间存在权衡关系。变态过程中基于黑色素的权衡关系，为幼虫期胁迫因子的效应如何传递至成虫阶段提供了全新的研究路径，进而推动了我们对幼虫期胁迫因子跨变态传递效应机制的理解，此类机制迄今仍大多不甚明晰。鉴于其具备机制基础，幼虫期UV辐射暴露对成虫免疫功能的这种传递效应，预计具有普遍性，且可能是无脊椎动物因UV辐射暴露而付出的一种广泛存在且重要的代价。