Unusual evolution of tree frog populations in the Chernobyl exclusion zone

Abstract

Despite the ubiquity of pollutants in the environment, their long‐term ecological consequences are not always clear and still poorly studied. This is the case concerning the radioactive contamination of the environment following the major nuclear accident at the Chernobyl nuclear power plant. Notwithstanding the implications of evolutionary processes on the population status, few studies concern the evolution of organisms chronically exposed to ionizing radiation in the Chernobyl exclusion zone. Here, we examined genetic markers for 19 populations of Eastern tree frog (Hyla orientalis) sampled in the Chernobyl region about thirty years after the nuclear power plant accident to investigate microevolutionary processes ongoing in local populations. Genetic diversity estimated from nuclear and mitochondrial markers showed an absence of genetic erosion and higher mitochondrial diversity in tree frogs from the Chernobyl exclusion zone compared to other European populations. Moreover, the study of haplotype network permitted us to decipher the presence of an independent recent evolutionary history of Chernobyl exclusion zone's Eastern tree frogs caused by an elevated mutation rate compared to other European populations. By fitting to our data a model of haplotype network evolution, we suspected that Eastern tree frog populations in the Chernobyl exclusion zone have a high mitochondrial mutation rate and small effective population sizes. These data suggest that Eastern tree frog populations might offset the impact of deleterious mutations because of their large clutch size, but also question the long‐term impact of ionizing radiation on the status of other species living in the Chernobyl exclusion zone.

Ionizing radiation and melanism in Chornobyl tree frogs

“…This agrees with the idea that historical exposure to radiation may be behind some of the effects detected in the area across taxa, a topic that deserves further research (Beresford et al, 2020;Hancock et al, 2020). If selection acted on frog coloration, low dispersal and high philopatry to the natal environment characteristic of many amphibians (including the study species; Angelone, 2009), may have favoured the prevalence of dark coloration in the Chornobyl tree frog metapopulation (Car et al, 2022).…”

“…This agrees with the idea that historical exposure to radiation may be behind some of the effects detected in the area across taxa, a topic that deserves further research (Beresford et al, 2020; Hancock et al, 2020). If selection acted on frog coloration, low dispersal and high philopatry to the natal environment characteristic of many amphibians (including the study species; Angelone, 2009), may have favoured the prevalence of dark coloration in the Chornobyl tree frog metapopulation (Car et al, 2022). In addition, amphibians with dark skin coloration often show dark coloration in their internal organs (Franco‐Belussi et al, 2016, 2017), and stressful conditions such as oxygen and food deprivation are known to induce higher cellular pigmentation (Franco‐Belussi et al, 2017).…”

“…100 m) and moist soils (see USDA Foreign Agricultural Service https://ipad.fas.usda.gov/crope xplor er/image view.aspx?regio nid=umb; or Copernicus Soil Moisture Index: https://land.coper nicus.eu/globa l/produ cts/ssm). Both areas are located within the Polesia woodland ecological zone biome (Fileccia et al, 2014), and our previous studies have revealed no geographic barriers, and the existence of gene flow, between H. orientalis inhabiting localities within these two areas (Car et al, 2022). Field and laboratory work were designed to reduce differences in handling time, temperature or experimental procedures between localities and areas.…”

“…However, work on amphibians in radio‐contaminated environments is still scarce (Orizaola, 2022). Recent studies have reported, for example, that radiation exposure was linked to an increase in mutation rates and mitochondrial DNA damage in frogs from radio‐contaminated areas (Car et al, 2022; Gombeau et al, 2020), but a lack of effects of radiation exposure on physiological biomarkers in Chornobyl tree frogs (Burraco, Bonzom, et al, 2021). Here, we examined the differences in dorsal skin coloration of Eastern tree frogs ( Hyla orientalis ) living across a large gradient of radioactive contamination around Chornobyl, and whether the maintenance of skin coloration is physiologically costly in terms of oxidative stress.…”

Ionizing radiation has negligible effects on the age, telomere length, and corticosterone levels of Chornobyl tree frogs

“…This includes unaltered blood biochemistry [12], markers of liver function [30], or the redox status of the frogs [31]. However, we detected an elevated mutation rate in the frogs living in the area compared to other European populations, with notably the presence of stop-gained mutations in the most contaminated areas and changes in the transcriptional profile in genes involved in energetic metabolism [32,33]. In this context, a chronic exposure to (relatively) low levels of ionizing radiation present in the Chornobyl region could have an impact on the lifespan of individuals.…”