Review

Are Organisms Adapting to
Ionizing Radiation at
Chernobyl?
Anders Pape Møller1,2,* and Timothy Alexander Mousseau3
Numerous organisms have shown an ability to survive and reproduce under lowdose ionizing radiation arising from natural background radiation or from
nuclear accidents. In a literature review, we found a total of 17 supposed casesof adaptation, mostly based on common garden experiments with organisms
only deriving from typically two or three sampling locations. We only found one
experimental study showing evidence of improved resistance to radiation.
Finally, we examined studies for the presence of hormesis (i.e., superior ﬁtness
at low levels of radiation compared with controls and high levels of radiation),but found no evidence to support its existence. We conclude that rigorous
experiments based on extensive sampling from multiple sites are required.
Chernobyl, Fukushima, and Resistance to Ionizing Radiation
The year 2016 demarks the 5th and 30th anniversaries of the Fukushima and Chernobyl nuclear
disasters, respectively, and there is growing public and scientiﬁc interest concerning the impacts ofsuch accidents on natural systems, given the likelihood of additional accidents in the future [1]. In
addition, there is considerable heterogeneity in natural levels of ionizing background radiation
across the globe, with signiﬁcant negative effects on numerous organisms, including humans [2].
Hence, it is not surprising that not only many microorganisms [3–5], but also eukaryotes, have
evolved an ability to tolerate, resist, or even beneﬁt from such radiation [2]. Furthermore, there isreason to believe that adaptation to other stressors, such as ultraviolet (UV) radiation, can facilitate
the evolution of resistance to ionizing radiation. Thus, microorganisms that do well in Chernobyl arealso those that do well on sunlight-exposed surfaces elsewhere ([6] S. Jenkinson et al., unpublished data, 2016). Therefore, adaptation to ionizing radiation can arise either from an increase in
the frequency of alleles that were already present before the accident at Chernobyl, due toadaptation to other stressors, or de novo from mutations. There is every reason to expect evolutionof resistance to radiation, even among organisms that have only been irradiated since recent
nuclear accidents, such as that at Chernobyl in 1986, because the intervening period of 30 years is
sufﬁcient for changes in phenotype in standard selection experiments for all organisms apart fromthose with the longest generation times. Such effects of radiation will depend on exposure toradionuclides, as reﬂected by internal dose (Box 1). In the past, novel radioactive sources, such as
those caused by asteroids and eruption of volcanoes, will have caused signiﬁcant levels ofdeleterious mutations resulting in reduced viability and, thus, preventing large fractions of populations from evolving signiﬁcant levels of resistance to radiation. There is also reason to believe that
populations of animals were exposed to such a high level of radiation that it could have reduced
their population size and imposed signiﬁcant directional selection (Box 2).
Ionizing radiation directly increases the frequency of chromosome breakage, although it also has
indirect effects via oxidative stress that causes DNA mutations (Box 3). Since mutations
ultimately are the source of novel genetic variants, ionizing radiation could contribute to evolution

Trends in Ecology & Evolution, April 2016, Vol. 31, No. 4

TrendsIn total,17 studies have suggested thatthey have demonstrated adaptation toionizing radiation from Chernobyl, while
in fact only two of these fulﬁll the criteria
for evolutionary adaptation.
Lack of evidence of adaptation mainly
derived from the lack of replication andof rigorous experimental design.
There was no evidence of hormesis,
with organisms at low levels of radiation
performing better than at typical background radiation in uncontaminatedareas.

1
Ecologie Systématique Evolution,
CNRS, University Paris-Sud,
AgroParisTech, Université ParisSaclay, 91400 Orsay, France
2
Laboratoire d’Ecologie, Systématiqueet Evolution, CNRS UMR 8079,
Université Paris-Sud, Bâtiment 362, F91405 Orsay Cedex, France
3
Department of Biological Sciences,
University of South Carolina,
Columbia, SC 29208, USA*Correspondence:
anders.moller@u-psud.fr (A.P. Møller).

http://dx.doi.org/10.1016/j.tree.2016.01.005© 2016 Elsevier Ltd. All rights reserved.

281

Box 1. Dose Rates and Populations
In the ﬁrst study of its sort, Garnier-Laplace et al. [58] calculated dose rates for 57 species of birds (almost 7000
individuals) living in Fukushima following the nuclear disaster of 12 March, 2011. Doses were calculated based onradiological conditions at the point of observation and corrected for by including ecological and life-history attributes of agiven species. Dose was used to predict the total number of birds, while statistically controlling for potentially confounding environmental variables (e.g., habitat type, elevation, presence of water bodies, ambient meteorologicalconditions, and time of day). Total dose was found to be a strong predictor of abundances (P < 0.0001), which showeda proportional decline with increasing doses with no indications of a threshold or intermediate optimum. Overall, the
ED50% (i.e., the total absorbed dose causing a 50% reduction in the total number of birds) was estimated to be 0.55 Gy.
This value can be compared with a value of 0.05 Gy as background radiation in uncontaminated areas around Fukushima
before the accident in 2011 [59] Figure I.

Predicted total number of birds

15

10

5

ED50%= 0.55 Gy[0.45; 0.70] Gy

0
0

0.01

10

10000

Total dose (Gy)Figure I. Log Logistic Model Fitted to Randomly Predicted Total Number of Birds Derived from a Global
General Linear Mixed model, and Its ED50% Prediction and Associated 95% Conﬁdence Interval ED50% Is
the Total Absorbed Dose Causing a 50% Reduction in the Total Number of Birds. Adapted from [58].

by speeding up evolutionary change. For example, radiation was used as early as 1925 to induce
novel variants for plant breeding and agriculture [7,8], and the genes encoding such variants
were subsequently selected in selection experiments. Some scientists have even speculated
that adaptation to low-dose radiation per se could facilitate evolution. These hypothetical effects
also relate to the notion of radiation hormesis, which suggests that low doses can have beneﬁcial
effects on organisms, for example via induced DNA repair [9–11]. Here, we not only review theliterature on the evolution of resistance to ionizing radiation, but also address the potential
underlying mechanisms and experimental designs used to assess the genetic and environmental effects on adaptation to radiation.

Adaptation to Radiation
Several studies have concluded that there is evidence of adaptation to low-dose radiation at
Chernobyl (Table 1). These range from proteomic analyses of plants showing changes in theamounts of proteins produced [12,13] and studies of DNA methylation that affect whether agene is expressed [17] to other physiological mechanisms [12,14]. There is also evidence
consistent with adaptation through the intracellular antioxidant glutathione, showing that somespecies of birds that do best under conditions of ionizing radiation have evolved the highest
levels of glutathione [15]. Perhaps the most clear-cut evidence for adaptations concerns
resistance to radioactivity in generalist bacteria, which are widely distributed across Europe [16].

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Box 2. Are There Effects of Radiation on Populations?
A recent study [60] suggested that some large mammals, particularly those normally under signiﬁcant hunting pressure,
were thriving inside the Belarusian part of the Chernobyl Exclusion Zone (Figure I). The data presented only showed apartial rebound of some mammals following the initial highly deleterious effects of the disaster, while the data forcontemporary population densities were primarily collected in regions of relatively low radioactivity while ignoring large
regions of intermediate and high radiation levels in both Belarus and Ukraine (e.g., the region in and around the so-called‘Red Forest’), thus lowering the statistical power of any potential tests for radiation effects. In addition, there was noattempt to estimate the internal dose of the species concerned. Furthermore, attempts made to correct for confounding
factors, such as habitat type or human habitation, were inadequate and conducted at a geographic scale likely to
obscure any relations with radiation effects, which are highly heterogeneous. Finally, no rigorous attempt was made tocompare suggested population trends to those from other wildlife refuges in Europe. Overall, the reported ﬁndings do notaddress the issue of whether populations have adapted to the radiological conditions found inside the Chernobyl zone.

100

EIk

10

1
100
1000
10000
Contamina!on density kBq m–2(B)
Track counts/10 km

Track counts/10 km

(A)

100

Wolf

10

1
100
1000
10000
Contamina!on density kBq m–2

Figure I. The Number of Track Counts Of Elk (A) and Wolves (B) in the Belarusian Part of the Chernobyl
Exclusion Zone. Data points represent annual estimates. Adapted from [60].

Adaptation is a biological concept that has many different meanings in ﬁelds as diverse as
evolution, physiology, and neuroscience [17–20]. Most biologists consider that, for evolutionary
adaptation to apply, there should be evidence of an increase in ﬁtness across all environments, andthat changes in phenotype over space (selection and the increase in ﬁtness) should be associatedwith a change in genotype frequency [20]. Thus, an adaptation sensu stricto requires that there is atleast a local or even a global ﬁtness optimum. This deﬁnition also implies that pre-adaptations thathave evolved in a context other than the focal phenomenon do not qualify as evolutionary
adaptations [21]. By contrast, physiologists consider design features of phenotypes that facilitate
the performance of even a single individual in a given environment to sufﬁce as physiological
adaptations [22]. Thus, physiological adaptation reﬂects the extent to which an individual performs
optimally in a given environment, therefore focusing on acclimation to the speciﬁc environment andthe required physiological responses [22]. Such physiological mechanisms can be inherited
through epigenetics (i.e., mechanisms, such as methylation, which affect whether a speciﬁc
nucleotide is expressed, but not the actual nucleotide at a speciﬁc locus) that can apply evenacross generations. Adaptation in neuroscience implies the temporal change in response of asensory system to a speciﬁc stimulus. However, here, we only consider evolutionary adaptations.
Irrespective of the deﬁnition of adaptation, there is an explicit or implicit assumption that there are
one or more environmental gradients that characterize the extent of optimality of the environment.
The process of adaptation by natural selection requires several key elements. First, there mustbe phenotypic variation among individuals within a population in their ability to perform in
response to the selective agent (in this case radiation). Second, there must be a genetic basis
underlying any observed variation in performance. Third, variation in performance must be
heritable; that is, offspring must resemble parents as a consequence of inheriting the genetic
factors responsible for variation in performance (e.g., [20]).
It seems likely that all organisms currently living have adapted to some degree to the consequences of ionizing radiation, given the near-ubiquity of past or current elevated backgroundradiation on the planet, which in the past was even higher than at present (e.g., [2]). However, it

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Box 3. Effects of Radiation from Chernobyl on Mutations
Given past and present interest in the long-term effects of ionizing radiation on genetic materials (i.e., DNA), it is perhaps
surprising that there have been relatively few studies directly addressing this question and few attempts to review andsynthesize the current state of knowledge concerning impacts on natural populations. Møller and Mousseau [61] used a
meta-analysis of 45 published studies covering 30 different species, including humans, to investigate the impacts ofChernobyl-derived radiation on measures of genetic damage. The overall conclusion was that there are large effects ofradioactivity stemming from the Chernobyl accident on measures of genetic damage with an overall effect size of E = 0.67
(95% conﬁdence interval = 0.59 – 0.73, N = 151 estimates) accounting for 44.3% of the variance in an unstructured
random effects model. Of special relevance here, effect size did not change with time since the accident of the study, thus
providing no systematic evidence for evolved adaptation to radiation. The effects of radiation on genetic damage variedamong taxa, with plants showing larger effects than animals. Humans were shown to have intermediate sensitivity toradiation as measured by mutations, when compared with other taxa (Figure I).

−1.0

0.0

1.0

2.0

3.0

Eﬀect size (Zr)

Figure I. Cumulative Distribution of Effect Sizes Weighted by Sample Size of Mutation Rates at Chernobyl
Ranked from the Weakest Negative Effects to the Strongest Positive Effects. Each bar and its 95% conﬁdence
interval (CI) represents one effect size. Effects sizes not overlapping with the vertical line at zero differ signiﬁcantly fromzero. The mean effect size of 1.09 was one of the largest in any biological meta-analyses. Adapted from [61].

has been often suggested that terrestrial life did not arise on Earth until atmospheric oxygen
levels had risen sufﬁciently to block the damaging effects of UV radiation [23,24], which implies alimit or constraint on the ability of populations to adapt to mutagenic environments.
Without the ability to repair the damage caused directly and indirectly by ionizing radiation to not
only genetic materials, but also proteins, including cell surface proteins, it seems likely that life
would not exist on this planet, at least in regions where radiation and other mutagens are found.
DNA repair has evolved in response to many physiological stressors that cause genetic damage[25,26], but mechanisms that eliminate proteins that have been damaged have resulted in theevolution of other mechanisms. Such repair mechanisms not only affecting damaged DNA, butalso causing elimination of damaged proteins, can pre-adapt some species to higher ionizing
radiation levels. Defective DNA repair abilities are often associated with disease, including cancer[27–29].
Given the likelihood of sustained directional selection for improved DNA repair ability and the
reduction of radiation-induced cellular damage since the beginning of life on Earth, evolutionary
theory would suggest that little adaptive genetic variation in such repair mechanisms would
presently exist in most populations. This is because, for simple Mendelian traits, beneﬁcial
mutations are rapidly ﬁxed, deleterious mutations generally are eliminated, and only neutral
mutations persist in most population unless eliminated via population bottlenecks or foundereffects [30]. Fundamentally, this relatively simple axiom of population genetics is the reason thatradiation hormesis is unlikely to exist, at least with respect to genetic damage.

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Trends in Ecology & Evolution, April 2016, Vol. 31, No. 4285

Seeds sown in two different plots

Common gardenCommon garden

Proteome

Proteome

Morphology and development

DNA damage

Linum usitatissimum

Chorthippus albomarginatus

Clethrionomys glareolus

Voles and vole-moles

Birds

Resistance to radiation

Field samples

Field samples?

?

Eight sites

Six sites

Six sites

Two sites

Two sites

Two sitesThree sites

Three sites

Three sites

Three sites

Three sites

Three sites

Four sites

Four sites

Sample
Size

No

?

No

No

No

No

No

No

Yes

Yes

No

No

No

No

Yes

Yes

OptimalRadiation
Level

No

No

No

No

No

No

No

No

No

No

No

No

No

No

No

No

Hormesis

No

No

Yes?

No

No

No

No

No

Yes

Yes?

No

No

No

Yes?

Yes?

Yes

Yes

Evidence for
Adaptation

Smaller seeds and reduced
germination could bepathological response; 35 of
720 (4.9%) proteins differed

Smaller seeds and reduced
germination could bepathological response

Smaller size of seeds could bepathological response; 64 of
698 (9.2%) proteins differed

Lower recombination rates inplants from contaminatedareas could be caused bymechanisms other thanadaptation

High-contamination plants
more resistant to twomutagens

Comments

[65]

[64]

[15]

S. Jenkinson
et al.,
unpublisheddata, 2016

[54]

[63]

[14]

[49]

[48]

[48]

[62]

[13]

[13]

[12]

[12]

[16]

[16]

Refs

Optimal radiation level indicates whether the organism performed better at an intermediate level of radiation than at lower or at higher radiation levels; hormesis indicates whether the organism performed better a low
levels of radiation compared with uncontaminated controls); evidence for adaptation shows whether organisms had superior ﬁtness when exposed to radiation.

aSeeds sown in two different plots

Proteome

Glycine max

Field samples

Field samples
Seeds sown in two different plots

Germination under stress

Oenothera biennis

GSH

Field samples

Pinus sylvestris

DNA repair

Transplant experiment

Methylation

Betula verrucosa

Transplant experiment

Recombination rates

Field samples

Transplant experimentSensitivity to mutagens

Arabidopsis thaliana

Field samples

Common garden

Resistance to radiation

Staphylococcus aureus

Number of aberrant cells inroot meristems

Common garden

Resistance to radiation

Bacillus pumilus

Methylation

Experimental Design

Response Variable

Species

Table 1. Studies Investigating Adaptation to Radiation from Chernobyla

Current explorations of mutation–selection balance theory suggest that, for natural populationsof ﬁnite sizes of less than a few thousand individuals, the addition of a small number of deleterious
mutations can tilt a population towards local extinction [31]. This is because many populations
exist in a balanced state that reﬂects ongoing adaptation to local environmental conditions andthe ﬁtness costs of constant immigration of individuals (maladaptive genotypes) that are not
optimally adapted to local conditions. If the environment changes quicker than the population
can adapt, it will go extinct. Likewise, genetic load due to the addition of deleterious mutations
via radiation effects can tip a local population towards extinction. Population size, inbreeding
effects, immigration rates, and breeding systems are likely to inﬂuence this process, but theultimate outcome for ﬁnite populations with limited immigration is likely to be extinction [30].

Selection and the Microevolution of Superior Phenotypes
Although several studies of plants and animals at Chernobyl have shown effects of intense
selection, resulting in the elimination of inferior phenotypes (i.e., purifying selection, which
eliminates alleles with deleterious effects) [32–45], we are unaware of even a single study
showing directional response for improved performance within populations that have been
subject to intense selection at Chernobyl or elsewhere (Table 1). This is perhaps surprising giventhat most traits not only show some degree of heritable genetic variation [46], but will also
respond when selection is applied (e.g., artiﬁcial selection for desirable traits can lead topopulation responses greater than several standard deviations in just a few generations[47]). It is perhaps telling that response to selection for increased radiation resistance appears
to be rare, perhaps reﬂecting a long history of selection that has eroded standing genetic
variation for this trait. Boubriak et al. [48] showed enhanced DNA repair in a single sample ofpollen from silver birch Betula verrucosa, although random factors can account for such aneffect. In part, this absence of studies stems from the general prediction and observation that
most, if not all, novel mutations are either neutral or slightly deleterious with respect to ﬁtness; thespontaneous generation of a beneﬁcial mutation is believed to be a rare event that, when it
occurs, proceeds to ﬁxation at a rapid pace. Geraskin et al. [49] showed in a 6-year study that
there was no change in the number of aberrant cells in root meristems of seeds exposed to anovel acute dose of radiation. This lack of temporal change in the number of aberrant cells
suggests, for this system, that there is an absence of adaptation to ionizing radiation.
Are there any studies showing adaptation to radiation (Table 1)? Ruiz-González et al. [16]showed for two common strains of bacteria from feathers of barn swallows Hirundo rusticafrom three study areas near Chernobyl and from Denmark (an uncontaminated control area)that bacteria originating from areas with intermediate radiation exposure performed better interms of resistance to an external radiation source in a common garden environment than did
bacteria from the control areas or the most irradiated areas. These bacteria on the plumage ofswallows are exposed to high radiation levels from the radionuclides in the soil used for theconstruction of nests. The common garden experiments suggested that bacteria performed
the best at an intermediate radiation level. It is perhaps surprising that there was no evidence ofadaptation to high radiation levels, given the higher intensity of selection that exists in suchenvironments. Explanations for this include the possibility that mechanisms associated withadaptation to intermediate radiation levels are different from those required to survive in highly
radioactive environments and that there is no genetically based variation in resistance to highmortality. Likewise, adaptation to low levels of radiation is unlikely because selection forresistance is likely to be lower [47]. Another explanation might be that costs of resistance(e.g., reduced replication rates) exceed the beneﬁts of increased survival, with the net effect thatthe contribution of these variants to future generations will be negligible. In addition, gene ﬂow
among populations inhabiting heterogeneous environments can stymy evolutionary responses[50] and has been found to limit population responses to selection in the face of climate change(e.g., [51]).

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Radiation hormesis posits that individuals perform better when conditioned by exposure to a low
dose of radiation, implying that there is a nonlinear relation between ﬁtness and radiation [9–11].
We are unaware of any studies showing experimental evidence of radiation hormesis effects
under ﬁeld conditions in whole-organism settings. The common garden experiment on bacteria,
which was crossed with an irradiation treatment, as discussed above [16], is also interestingfrom a hormesis perspective because the bacteria did not show superior performance when at
low levels of radiation, suggesting a cost to adaptive mechanisms in the absence of radiation.
Hence, we conclude that there are no explicit tests demonstrating radiation hormesis effects forwhole organisms under ﬁeld conditions.

Experimental Designs
17 studies had samples from a single contaminated site and a single control site, or a maximumof three sites differing in level of radioactivity. The use of samples from individuals from each suchsite is effectively pseudoreplication [52]; that is, the use of multiple observations from a single site
as if they are statistically independent, despite such observations being dependent because theyshare a common environment. Thus, no robust conclusions can be drawn from such data.
However, even multiple studies each based on two sites can be used to draw general conclusions in meta-analyses, in which effect size estimates are weighted by sample size to achieve
an overall effect size estimate across studies [33]. Such a meta-analysis is equal to coin ﬂipping,with the null expectation being that an equal number of studies go in each of the two directions[33].
There are several standard designs that can be used to make rigorous tests of adaptation toradiation. The prime design used to make inferences about the effects of environment of origin
and the environment of rearing is reciprocal transplants between contaminated and uncontaminated sites [53]. In this experimental design, individuals of two (or more) common origins (onecontaminated and one noncontaminated) are both reared not only in their home environment,
but also in the ‘other’ environment, allowing for both populations to be reared under both levelsof contamination. This allows not only for the comparison of the phenotype of individuals reared‘at home’ or away from their native environment, but also for a rigorous test of the effect of aninteraction between environments of origin and rearing. Surprisingly, we are unaware of any suchapproaches in the study of effects of radiation.
Another standard design that is less rigorous is the common garden experiment, whereindividuals from multiple environments varying in their level of exposure to radiation inprevious generations are reared together in a benign environment. If the effect of radiation
is maintained in the common garden in the current, but also in the subsequent twogenerations, we can infer that the differences have a genetic basis and are unlikely to be
due to epigenetic or maternal effects. This approach has been used in grasshoppers [54],although the evidence of phenotypic differences being related to radiation was negligible.
Ruiz-González et al. [16] used common garden experiments on two strains of bacteria of thespecies Bacillus pumilus and Staphylococcus aureus to test for increased performance
under elevated levels of radiation. Common garden experiments have also been done byrearing plants from seeds collected at different radiation levels at Chernobyl in an uncontaminated greenhouse.
Yet another design is the rearing or maintenance of standard organisms in environments differingin level of radiation. We are only aware of one study using the blue mouse Mus domesticus assay
to quantify somatic mutations in the Red Forest [55]. In such experiments, it is crucial that therearing conditions do not interfere with the outcome by the provisioning of high levels ofantioxidants in the diet, which can reduce or eliminate DNA damage.

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287

These designs are useful for demonstrating likely adaptive responses to past selective environments (i.e., explaining the past), but they do not provide information in and of themselves
concerning the mechanisms underlying any observed phenotypic variation; neither do they
speak to the potential for future evolutionary responses. The ability to predict response to
selection requires knowledge of the heritable basis of phenotypic variation with respect toresistance to radiation, which to our knowledge has never been addressed.

Concluding Remarks
Where to go from here? There is plenty of evidence for rapid evolutionary change in the face of achanging environment (e.g., [56,57]). Hence, there is every reason to expect that microevolutionary change can be demonstrated by studies at Chernobyl and Fukushima. We conclude that
there is a need for investment in long-term ecological studies conducted within a genetic
framework if we are to predict future responses to radiation exposure. Surprisingly, there
are no whole-genome estimates of mutation rates caused by chronic radiation exposure despite
30 years having passed since the accident in Chernobyl. Likewise, there are no estimates of how
chronic exposure to radiation lead to evolutionary changes in mutation rates (see Outstanding
Questions).
Which organisms to study? We suggest that a variety of organisms, such as sexual versus
asexual organisms, will be most informative. Such studies could beneﬁt from analyses of themechanisms of adaptation (i.e., DNA repair) and the costs of adaptation (i.e., trade-offs).
We have emphasized that not all designs are equally powerful and that some are nothing butclassical examples of pseudoreplication. Reciprocal transplant experiments are the way forward
because they allow for quantiﬁcation of the extent of adaptation, the mechanisms involved, andthe costs of adaptation.
Although hormesis is often purported to have a role in adaptation to radiation, we are unaware ofeven a single study demonstrating hormetic effects of ionizing radiation under ﬁeld conditions.
Again, this boils down to the question of how to make a rigorous test, with reciprocal transplant
experiments being the way forward.
Acknowledgments
We are grateful for support from the CNRS (France), the Samuel Freeman Charitable Trust, The American Council of
Learned Societies, and the College of Arts and Sciences at the University of South Carolina.

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Outstanding Questions
Whole-genome estimates of mutation
rates caused by chronic radiation.
Estimates of how chronic exposure toradiation lead to evolutionary changes
in mutation rates.
Reciprocal transplant experiments
between irradiated and uncontaminated study plots to quantify environmental and genetic effects foradaptation to radiation.
Accumulation of mutations within individuals over time in contaminated andcontrol areas.
Assessment of ecological factors
responsible for differences in mutation
accumulation and adaptation.

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