Parental exposure modulates the effects of UV‐B on offspring in guppies

Abstract

Summary The environment experienced by parents can alter offspring phenotypes. Such developmental plasticity is beneficial when it optimises offspring responses to their prevailing environment. Plasticity may be detrimental, however, if there is a mismatch between parental and offspring environments, although reversible acclimation within individuals could counteract a developmental mismatch. UV‐B radiation damages cells directly and by increasing reactive oxygen species (ROS) formation. There are indications that the developmental environment can influence ROS defences, which could enhance performance and fitness. In addition, animals exposed to UV‐B can acclimate to increase their antioxidant defences and thereby reduce ROS‐induced damage. Our aim was to test experimentally whether there are transgenerational effects of UV‐B exposure. We tested the hypothesis that parental exposure to UV‐B modulates offspring ROS defence mechanisms to reduce the negative effects of UV‐B in offspring. In a fully factorial experiment, we show that exposing guppies (Poecilia reticulata) to UV‐B increased the resilience of their offspring to the negative effects of UV‐B. When exposed to UV‐B, offspring from parents also exposed to UV‐B had significantly greater sustained swimming performance compared to controls. Higher swimming performance was paralleled by increased catalase activity and glutathione concentrations, and reduced ROS‐induced damage to membranes and proteins. There was no effect of parental exposure to UV‐B on offspring superoxide dismutase activity, resting and active metabolic rates or offspring size. However, parental exposure to UV‐B increased damage to proteins and infection rates by white spot fungus in control (no UV‐B) offspring. Our results showed that UV‐B acts as a signal that can induce developmental modification of phenotypes. Transgenerational matching of offspring phenotypes is likely to have a fitness advantage in environments exposed to UV‐B. However, the trade‐off between the beneficial effects of parental UV‐B exposure on offspring performance when exposed to UV‐B, and the increased susceptibility to infection and protein damage when offspring are not exposed to UV‐B can be important in determining the resilience of populations in variable and modified environments. A lay summary is available for this article.