1. Gut microbiota play an important role in host health. Yet, the drivers and patterns of microbiota imbalance (dysbiosis) in wild animals remain largely unexplored. 2. One hypothesised outcome of stress on animal microbiomes is a destabilised microbial community that is characterised by an increase in inter-individual differences compared with microbiomes of healthy animals, which are expected to be (a) temporally stable and (b) relatively similar among individuals. This set of predictions for response of microbiomes to stressors is known as the Anna Karenina principle (AKP) for animal microbiomes. 3. We examine the AKP in a wild mammal inhabiting disturbed environments by conducting a capture-mark-recapture survey of bank voles Myodes glareolus in areas that contrast in levels of radionuclide contamination (Chernobyl, Ukraine). 4. Counter to key predictions of the AKP, bank voles that are not exposed to radionuclides harbour variable (increased inter-individual differences) and temporally dynamic gut microbiota communities, presumably tracking the natural spatiotemporal variation in resources. Conversely, bank voles exposed to radionuclides host more similar gut microbiota communities that are temporally stable, potentially due to a dysbiosis or selection (on host or bacteria) imposed by chronic radiation exposure. 5. The implication of these data is that environmental stress (radiation exposure) can constrain the natural spatial and temporal variation of wild animal gut microbiota.

Telomeres, the protective structures at the ends of chromosomes, can be shortened when individuals are exposed to stress. In some species, the enzyme telomerase is expressed in adult somatic tissues, and potentially protects or lengthens telomeres. Telomeres can be damaged by ionizing radiation and oxidative stress, although the effect of chronic exposure to elevated levels of radiation on telomere maintenance is unknown for natural populations. We quantified telomerase expression and telomere length (TL) in different tissues of the bank vole Myodes glareolus, collected from the Chernobyl Exclusion Zone, an environment heterogeneously contaminated with radionuclides, and from uncontaminated control sites elsewhere in Ukraine. Inhabiting the Chernobyl Exclusion Zone was associated with reduced TL in the liver and testis, and upregulation of telomerase in brain and liver. Thus upregulation of telomerase does not appear to associate with longer telomeres but may reflect protective functions other than telomere maintenance or an attempt to maintain shorter telomeres in a stressful environment. Tissue specific differences in the rate of telomere attrition and apparent radiosensitivity weaken the intra-individual correlation in telomere length among tissues in voles exposed to radionuclides. Our data show that ionizing radiation alters telomere homeostasis in wild animal populations in tissue specific ways.

Wildlife inhabiting environments contaminated by radionuclides face putative detrimental effects of exposure to ionizing radiation, with biomarkers such as an increase in DNA damage and/or oxidative stress commonly associated with radiation exposure. To examine the effects of exposure to radiation on gene expression in wildlife, we conducted a de novo RNA sequencing study of liver and spleen tissues from a rodent, the bank vole Myodes glareolus. Bank voles were collected from the Chernobyl Exclusion Zone (CEZ), where animals were exposed to elevated levels of radionuclides, and from uncontaminated areas near Kyiv, Ukraine. Counter to expectations, we did not observe a strong DNA damage response in animals exposed to radionuclides, although some signs of oxidative stress were identified. Rather, exposure to environmental radionuclides was associated with upregulation of genes involved in lipid metabolism and fatty acid oxidation in the livers – an apparent shift in energy metabolism. Moreover, using stable isotope analysis, we identified that fur from bank voles inhabiting the CEZ had enriched isotope values of nitrogen: such an increase is consistent with increased fatty acid metabolism, but also could arise from a difference in diet or habitat between the CEZ and elsewhere. In livers and spleens, voles inhabiting the CEZ were characterized by immunosuppression, such as impaired antigen processing, and activation of leucocytes involved in inflammatory responses. In conclusion, exposure to low dose environmental radiation impacts pathways associated with immunity and lipid metabolism, potentially as a stress‐induced coping mechanism.

Nuclear accidents underpin the need to quantify the ecological mechanisms which determine injury to ecosystems from chronic low‐dose radiation. Here, we tested the hypothesis that ecological mechanisms interact with ionizing radiation to affect natural populations in unexpected ways. We used large‐scale replicated experiments and food manipulations in wild populations of the rodent, Myodes glareolus, inhabiting the region near the site of the Chernobyl disaster of 1986. We show linear decreases in breeding success with increasing ambient radiation levels with no evidence of any threshold below which effects are not seen. Food supplementation of experimental populations resulted in increased abundances but only in locations where radioactive contamination was low (i.e., below ≈ 1 μSv/h). In areas with higher contamination, food supplementation showed no detectable effects. These findings suggest that chronic low‐dose‐rate irradiation can decrease the stability of populations of key forest species, and these effects could potentially scale to broader community changes with concomitant consequences for the ecosystem functioning of forests impacted by nuclear accidents.

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