Natural radioactivity can explain clinal variation in the expression of melanin-based traits

Abstract

A recent study shows that the expression of pheomelanin-based coloration in barn owls follows a continuous gradient across Europe as a result of local adaptation. The selective pressures that promote local adaptation remain, however, unknown. Here we hypothesize and test that natural radioactivity levels follow a similar spatial gradient to that of pheomelanin-based color in Europe and thus represents a potential selective pressure. The rationale is that the production of pheomelanin consumes glutathione (GSH), a key intracellular antioxidant, and that GSH is particularly susceptible to ionizing radiation, which depletes antioxidants. As predicted, the intensity of pheomelanin-based coloration in 18 populations of barn owls was negatively associated with terrestrial γ-dose rates across Europe. Therefore, we propose that natural selection acts against barn owls that present the molecular basis to produce large amounts of pheomelanin in those populations that are exposed to high levels of natural radioactivity, as in these populations individuals would require higher antioxidant resources to combat oxidative stress. This is the first time that natural radioactivity levels are related to the expression of a phenotypic trait.