International audience | Estimating the consequences of environmental changes, specifically in a global change context, is essential for conservation issues. In the case of pollutants, the interest in using an evolutionary approach to investigate their consequences has been emphasized since the 2000s, but these studies remain rare compared to the characterization of direct effects on individual features. We focused on the study case of anthropogenic ionizing radiation because, despite its potential strong impact on evolution, the scarcity of evolutionary approaches to study the biological consequences of this stressor is particularly true. In this study, by investigating some particular features of the biological effects of this stressor, and by reviewing existing studies on evolution under ionizing radiation, we suggest that evolutionary approach may help provide an integrative view on the biological consequences of ionizing radiation. We focused on three topics: (i) the mutagenic properties of ionizing radiation and its disruption of evolutionary processes, (ii) exposures at different time scales, leading to an interaction between past and contemporary evolution, and (iii) the special features of contaminated areas called exclusion zones and how evolution could match field and laboratory observed effects. This approach can contribute to answering several key issues in radioecology: to explain species differences in the sensitivity to ionizing radiation, to improve our estimation of the impacts of ionizing radiation on populations, and to help identify the environmental features impacting organisms (e.g., interaction with other pollution, migration of populations, anthropogenic environmental changes). Evolutionary approach would benefit from being integrated to the ecological risk assessment process.

The effects of exposure to different levels of ionising radiation were assessed on the genetic, epigenetic and microbiome characteristics of the “hologenome” of earthworms collected at sites within the Chernobyl exclusion zone (CEZ). The earthworms Aporrectodea caliginosa (Savigny, 1826) and Octolasion lacteum (Örley, 1881) were the two species that were most frequently found at visited sites, however, only O. lacteum was present at sufficient number across different exposure levels to enable comparative hologenome analysis. The identification of morphotype O. lacteum as a probable single clade was established using a combination of mitochondrial (cytochrome oxidase I) and nuclear genome (Amplified Fragment Length Polymorphism (AFLP) using MspI loci). No clear site associated differences in population genetic structure was found between populations using the AFLP marker loci. Further, no relationship between ionising radiation exposure levels and the percentage of methylated loci or pattern of distribution of DNA methylation marks was found. Microbiome structure was clearly site dependent, with gut microbiome community structure and diversity being systematically associated with calculated site-specific earthworm dose rates. There was, however, also co-correlation between earthworm dose rates and other soil properties, notably soil pH; a property known to affect soil bacterial community structure. Such co-correlation means that it is not possible to attribute microbiome changes unequivocally to radionuclide exposure. A better understanding of the relationship between radionuclide exposure soil properties and their interactions on bacterial microbiome community response is, therefore, needed to establish whether these the observed microbiome changes are attributed directly to radiation exposure, other soil properties or to an interaction between multiple variables at sites within the CEZ.

Ants can influence ecological processes, such as the transfer of elements or radionuclides, in several ways. For example, they redistribute materials while foraging and maintaining their nests and have an important role in terrestrial food webs. Quantitative data of the transfer of elements into ants is needed, e.g., for developing improved radioecological models. In this study, samples of red wood ants (genus Formica), nest material, litter and soil were collected from a former uranium mining site in Eastern Finland. Concentrations of 33 elements were analyzed by Inductively Coupled Plasma-Mass Spectroscopy/Optical Emission Spectroscopy. Estimated element concentrations in spruce needles were used as a proxy for studying the transfer of elements into ants via aphids because spruces host the most important aphid farms in boreal forests. Empirically determined organism/medium concentration ratios (CRs) are commonly used in radioecological models. Ant/soil CRs were calculated and the validity of the fundamental assumption behind the of use of CRs (linear transfer) was evaluated. Elements that accumulated in ants in comparison to other compartments were cadmium, potassium, phosphorus, sulfur, and zinc. Ant uranium concentrations were low in comparison to soil, litter, or nest material but slightly elevated in comparison to spruce needles. Ant element concentrations were quite constant regardless of the soil concentrations. Non-linear transfer models could therefore describe the soil-to-ant transfer better than conventional CRs.

The issue of potential long-term or hereditary effects for both humans and wildlife exposed to low doses (or dose rates) of ionising radiation is a major concern. Chronic exposure to ionising radiation, defined as an exposure over a large fraction of the organism's lifespan or even over several generations, can possibly have consequences in the progeny. Recent work has begun to show that epigenetics plays an important role in adaptation of organisms challenged to environmental stimulae. Changes to so-called epigenetic marks such as histone modifications, DNA methylation and non-coding RNAs result in altered transcriptomes and proteomes, without directly changing the DNA sequence. Moreover, some of these environmentally-induced epigenetic changes tend to persist over generations, and thus, epigenetic modifications are regarded as the conduits for environmental influence on the genome.Here, we review the current knowledge of possible involvement of epigenetics in the cascade of responses resulting from environmental exposure to ionising radiation. In addition, from a comparison of lab and field obtained data, we investigate evidence on radiation-induced changes in the epigenome and in particular the total or locus specific levels of DNA methylation. The challenges for future research and possible use of changes as an early warning (biomarker) of radiosensitivity and individual exposure is discussed. Such a biomarker could be used to detect and better understand the mechanisms of toxic action and inter/intra-species susceptibility to radiation within an environmental risk assessment and management context.

Ionizing radiation causes a variety of effects, including DNA damage associated to cancers. However, the effects in progeny from irradiated parents is not well documented. Using zebrafish as a model, we previously found that parental exposure to ionizing radiation is associated with effects in offspring, such as increased hatching rates, deformities, increased DNA damage and reactive oxygen species. Here, we assessed short (one month) and long term effects (one year) on gene expression in embryonic offspring (5.5 h post fertilization) from zebrafish exposed during gametogenesis to gamma radiation (8.7 or 53 mGy/h for 27 days, total dose 5.2 or 31 Gy) using mRNA sequencing. One month after exposure, a global change in gene expression was observed in offspring from the 53 mGy/h group, followed by embryonic death at late gastrula, whereas offspring from the 8.7 mGy/h group was unaffected. Interestingly, one year after exposure newly derived embryos from the 8.7 mGy/h group exhibited 2390 (67.7% downregulated) differentially expressed genes. Overlaps in differentially expressed genes and enriched biological pathways were evident between the 53 mGy/h group one month and 8.7 mGy/h one year after exposure, but were oppositely regulated. Pathways could be linked to effects in adults and offspring, such as DNA damage (via Atm signaling) and reproduction (via Gnrh signaling). Comparison with gene expression analysis in directly exposed embryos indicate transferrin a and cytochrome P450 2x6 as possible biomarkers for radiation response in zebrafish. Our results indicate latent effects following ionizing radiation exposure from the lower dose in parents that can be transmitted to offspring and warrants monitoring effects over subsequent generations.

Laboratory radiotracer experiments were conducted to study the uptake, assimilation, and retention of cesium (137Cs) in milkfish (Chanos chanos) from Jakarta Bay. In this study, we have examined the bioaccumulation and distribution of 137Cs in C. chanos obtained from 137Cs-labeled seawater and 137Cs-labeled Artemia sp. feeding. The uptake of 137Cs via seawater displayed a one-compartment model suggesting that the concentration factors of 137Cs within the milkfish (weight 2.46–9.86g) at a steady-state period were between 10.66 and 3.98mLg−1 after 10days of exposure. The depuration rate was observed to be low, with only 22.80–49.14% of 137Cs absorbed by C. chanos, which was absent 6days after exposure. By contrast, depuration occurred quickly for radiolabeled food uptake, reaching 20% of retention within 10days after exposure. Muscles and viscera of the milkfish exhibited the highest degree of end uptake and end depuration of 137Cs from seawater and feeding.