Population transcriptogenomics highlights impaired metabolism and small population sizes in tree frogs living in the Chernobyl Exclusion Zone

Abstract

Background Individual functional modifications shape the ability of wildlife populations to cope with anthropogenic environmental changes. But instead of adaptive response, human-altered environments can generate a succession of deleterious functional changes leading to the extinction of the population. To study how persistent anthropogenic changes impacted local species’ population status, we characterised population structure, genetic diversity and individual response of gene expression in the tree frog Hyla orientalis along a gradient of radioactive contamination around the Chernobyl nuclear power plant. Results We detected lower effective population size in populations most exposed to ionizing radiation in the Chernobyl Exclusion Zone that is not compensated by migrations from surrounding areas. We also highlighted a decreased body condition of frogs living in the most contaminated area, a distinctive transcriptomics signature and stop-gained mutations in genes involved in energy metabolism. While the association with dose will remain correlational until further experiments, a body of evidence suggests the direct or indirect involvement of radiation exposure in these changes. Conclusions Despite ongoing migration and lower total dose rates absorbed than at the time of the accident, our results demonstrate that Hyla orientalis specimens living in the Chernobyl Exclusion Zone are still undergoing deleterious changes, emphasizing the long-term impacts of the nuclear disaster.

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

“…In Chornobyl, radiation has decreased considerably from the moment of the accident [50], and nowadays there is controversy about the effects of current radiation levels on wildlife [e.g., 2]. In our study system, Chornobyl tree frogs inhabiting radiocontaminated areas show normal physiological condition [12,30,31,but see 32,33 addressing effects at the genetic or transcriptomic level]. In accordance with our previous physiological approaches in the same study system, we did not find a marked relationship between individual absorbed dose rates and frog age.…”

“…We obtained individual body condition estimates by getting the residuals of the linear relationship between body mass and length [49]. Since body condition is known to correlates with absorbed dose rates in Chornobyl tree frogs [33], we included this parameter in the analyses. To study the relationship between individual absorbed dose rate (i.e., as the predictor variable) and age, we conducted a generalized model with a Poisson distribution, including as fixed factors GPS coordinates where samples were collected to correct by spatial correlation, body condition, and year of sampling.…”

“…We obtained individual body condition estimates by getting the residuals of the linear relationship between body mass and length [49]. Since body condition is known to correlates with absorbed dose rates in Chornobyl tree frogs [33], we included this parameter in the analyses.…”

“…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.…”