Larval UV exposure impairs adult immune function through a trade‐off with larval investment in cuticular melanin

Abstract

Summary 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 provides 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 basis, 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.

Pace of life syndrome under warming and pollution: integrating life history, behavior, and physiology across latitudes

“…, Debecker et al. ). Detailed descriptions of the protocols for the quantification of physiological variables are presented in the Supporting Information (Appendix ).…”

An Insect with Selective Control of Egg Coloration

“…Eggs themselves could accumulate pigment in response to ambient levels of UV radiation, as has been observed in various life stages of other animals [23,24]. Alternatively, female stink bugs may be able to detect the intensity of incident UV radiation (or visual wavelengths of light correlated with the presence of UV) and use this information to adjust the application of pigment to eggs.…”

“…The upper surface of leaves would then represent ''enemy free space'' [30,31], and applying the pigment when eggs are laid there would minimize the cost of the resulting tradeoff in terms of higher UV radiation exposure. The second condition could be met if there is a significant physiological cost of pigment production, as demonstrated in many other systems [24,32,33]. Laying eggs on the underside of leaves without having to pay the cost for applying pigment-while accepting the risk that eggs could be killed by predators-could be adaptive in some situations, especially if predators are uncommon or females are nutritionally stressed and have less resources to allocate to pigment production.…”

Immune deployment increases larval vulnerability to predators and inhibits adult life‐history traits in a dragonfly

“…Because of the cytotoxic properties of the melanin‐synthesis pathway, this nonspecific immune response can also result in considerable incidental tissue damage (Nappi & Vass, ; Sadd & Siva‐Jothy, ; Khan et al ., ). Moreover, the functioning of the melanin‐synthesis pathway directly carries over from the larval to the adult life stage in arthropods (Debecker et al ., ) and is used in the production of sexually selected coloration (Hooper et al ., ; Lawniczak et al ., ; Wittkopp & Beldade, ), making the overall encapsulation response likely to affect fitness components across life stages as well.…”