Chronic exposure to low‐dose radiation atChernobyl favours adaptation to oxidative stress in birds

Abstract

Summary 1.Ionizing radiation produces oxidative stress, but organisms can adapt to their exposure with physiological adaptive responses. However, the role of radioadaptive responses in wild populations remains poorly known. 2. At Chernobyl, studies of birds and other taxa including humans show that chronic exposure to radiation depletes antioxidants and increases oxidative damage. Here, we present analyses of levels of the most important intracellular antioxidant (i.e. glutathione, GSH), its redox status, DNA damage and body condition in 16 species of birds exposed to radiation at Chernobyl. We use an approach that allows considering the individual bird as the sampling unit while controlling for phylogenetic effects, thus increasing the statistical power by avoiding the use of species means as done for most previous comparative studies. 3. As a consequence, we found a pattern radically different from previous studies in wild populations, showing that GSH levels and body condition increased, and oxidative stress and DNA damage decreased, with increasing background radiation. Thus, when several species are considered, the overall pattern indicates that birds are not negatively affected by chronic exposure to radiation and may even obtain beneficial hormetic effects following an adaptive response. Analysis of the phylogenetic signal supports the existence of adaptation in the studied traits, particularly in GSH levels and DNA damage. 4. We also show that, under equal levels of radiation, the birds that produce larger amounts of the pigment pheomelanin and lower amounts of eumelanin pay a cost in terms of decreased GSH levels, increased oxidative stress and DNA damage, and poorer body condition. Radiation, however, diminished another potential cost of pheomelanin, namely its tendency to produce free radicals when exposed to radiation, because it induced a change towards the production of less pro-oxidant forms of pheomelanin with higher benzothiazole-to-benzothiazine ratios, which may have facilitated the acclimation of birds to radiation exposure. 5. Our findings represent the first evidence of adaptation to ionizing radiation in wild animals, and confirm that pheomelanin synthesis represents an evolutionary constraint under stressful environmental conditions because it requires GSH consumption.

Transcriptional Upregulation of DNA Damage Response Genes in Bank Voles (Myodes glareolus) Inhabiting the Chernobyl Exclusion Zone

“…Moreover, ATM can be activated by oxidative stress independently from DBS-related activation by the MRN complex (Guo et al, 2010). Antioxidant production likely constitutes a major part of the adaptive response against environmental radioactivity in birds within and around the CEZ (Galván et al, 2014) and in cell lines of fibroblasts from bank voles (Mustonen et al, submitted). Moreover, a change in fur color of bank voles within the CEZ was attributed to downregulation of pheomelanin to reallocate antioxidants to ROS defense (Boratynski et al, 2014).…”

Contamination of Wild Animals: Microhabitat Heterogeneity and Ecological Factors of Radioactive Cesium Exposure in Fukushima

“…Unfortunately, there is very little information on the wildlife in the contaminated area of Abukuma Mountains before the F1NPP accident. It will be desirable to monitor the ecosystem and several principal wildlife species, such as some of the dominant 10 birds (explained previously), S. scrofa and unique primate Macaca fuscata (Hayama et al 2013), until most of the ecosystems and human societies regain stability in five or more decades later (Galvan et al 2014).…”

Melanin Chemistry and the Ecology of Stress

“…This ROS production, however, is reduced in the benzothiazole moiety as compared to the benzothiazine moiety due to the rather stable nature of the former (Wakamatsu et al 2009). Hence, pheomelanins with higher relative contents of benzothiazoles are less prooxidant under radiation exposure (Galván et al 2014 and cited references). The analysis of benzothiazine/ benzothiazole ratios in different biological tissues gives information about the color phenotypes generated by the different pheomelanin moieties.…”

“…Regarding pheomelanins, there is increasing evidence that pheomelanin production represents a cost under environmental conditions or physiological processes that require a high level of protection against ROS production, and it has recently been shown that a shift toward the production of pheomelanins with a higher benzothiazole/benzothiazine ratio facilitates the acclimation of birds to relatively high exposure to ionizing radiation, which produces oxidative stress (Galván et al 2014). Pheomelanin-based colors confer camouflage or concealment and act as signals of individual quality, but certainly not all pheomelanin-based color traits are involved in concealment or signaling.…”

“…Thus, pheomelanogenesis represents a consumption of glutathione, the main intracellular antioxidant and physiological reservoir of cysteine, while cysteine is not consumed during eumelanogenesis (Ito and Wakamatsu 2008). This has led to the realization that producing eumelanin entails different benefits and costs than producing pheomelanin and that pheomelanogenesis may limit the ability to cope with physiological processes or environmental conditions that generate high levels of oxidative stress (Karell et al 2011;Roulin et al 2011;Galván and Møller 2013;Galván et al 2014). However, the diversity of melanins is more than just eumelanin and pheomelanin.…”