Natural radioactivity can explain clinal variation in the expression of melanin-based traits
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.
KeywordsFeather melanin Glutathione Natural selection Oxidative stress Pheomelanin Terrestrial γ-dose rates
We thank Xabier Vázquez Pumariño for early discussions on natural radioactivity in Galicia, NW Spain. Ulrich Stöhlker kindly allowed us to use his map of radiation levels in Europe. I.G. was supported by a Marie Curie Intra-European Fellowship of the European Community (PIEF-GA-2009-252145). Financial support to C.A.-A. was obtained from the Spanish Ministry of Science and Innovation (project CGL2009-10883-C02-02) and from Junta de Comunidades de Castilla-La Mancha (project PII1I09-0271-5037). John A. Endler, Andrew Hendry and two anonymous referees made useful suggestions that improved the manuscript.
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