03. 2014年6月27日 20:06:08
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リンクがおかしいが元論文は、これか SurveyとしてはPaperのSelectionが、恣意的になされているようだが どんな研究でも危険率の設定で、必ずNegativeとPositiveな結果が出てくるし 分子レベルでの影響は↑に書いたように、確実に有意な影響が出るから、 そこを、どう判定しているか、その辺の議論と根拠が怪しいね
http://onlinelibrary.wiley.com/doi/10.1111/j.1469-185X.2012.00249.x/full
Abstract
Natural levels of radioactivity on the Earth vary by more than a thousand-fold; this spatial heterogeneity may suffice to create heterogeneous effects on physiology, mutation and selection. We review the literature on the relationship between variation in natural levels of radioactivity and evolution. First, we consider the effects of natural levels of radiation on mutations, DNA repair and genetics. A total of 46 studies with 373 effect size estimates revealed a small, but highly significant mean effect that was independent of adjustment for publication bias. Second, we found different mean effect sizes when studies were based on broad categories like physiology, immunology and disease frequency; mean weighted effect sizes were larger for studies of plants than animals, and larger in studies conducted in areas with higher levels of radiation. Third, these negative effects of radiation on mutations, immunology and life history are inconsistent with a general role of hormetic positive effects of radiation on living organisms. Fourth, we reviewed studies of radiation resistance among taxa. These studies suggest that current levels of natural radioactivity may affect mutational input and thereby the genetic constitution and composition of natural populations. Susceptibility to radiation varied among taxa, and several studies provided evidence of differences in susceptibility among populations or strains. Crucially, however, these studies are few and scattered, suggesting that a concerted effort to address this lack of research should be made.
I. INTRODUCTION
Radiation can be divided into non-ionizing radiation (radio waves, visible light and heat) and ionizing radiation that has sufficient energy to ionize an atom. Ionizing radiation consists of particles that cannot penetrate paper, particles that can penetrate paper, but not an aluminium sheet, and rays that can penetrate paper, aluminium and thin layers of lead. Both ionizing and non-ionizing radiation can be damaging for organisms, although ionizing radiation is more damaging because the ions that are generated may directly damage DNA and other molecules. Levels of background ionizing radiation (hereafter radiation) have always varied spatially and temporally on Earth. Levels of background radiation were very high during the Pre-Cambrian period peaking around two billion years ago at a dose rate of 7 mGy per year, but have decreased by a factor of 10 since life first originated (Karam & Leslie, 2005). During the subsequent 2 billion years, radiation levels fluctuated considerably due to large solar flares, nearby supernovae and gamma ray bursts. Large meteor impacts in Mexico, India, Russia and other sites also likely caused the release of vast amounts of radioactive material on Earth (e.g. Alvarez et al., 1980). Such fluctuations may have contributed to current levels of resistance to radiation damage in free-living organisms. Today, typical background radiation dose rates vary around a minimum of only 0.01–0.10 with the natural level in Chernobyl before the nuclear accident being 0.01–0.02. By contrast, there are geographic regions where naturally occurring radiation can reach very high levels (3 orders of magnitude above global mean levels). There are equally many sites with high levels of radiation in the oceans, with thermal vents and their associated unique biodiversity being a well-known example (e.g. Fiala-Médioni, Alaysee & Cahet, 1986; Cherry et al., 1992; Jollivet et al., 1995a, b, 2003). Maximum terrestrial levels of radioactivity reach as high as 29.7 h in Ramsar, Iran, 22 h in Morro do Ferro, Minas Gerais, Brazil, 12 h in Mombasa, Kenya, 10 /h in Lodeve, France, 4.0 Sv/h in Kerala, India, 4.0 Sv/h in Tamil Nadu, India, and 0.7 /h in Yangjiang, China (Ghiassi-Nejad et al., 2002). Such radiation is related to the presence of radionuclides in the rock or in the form of gases like radon that can be trapped inside buildings or caves and increase human exposure to mutagens that subsequently increase rates of cancer (e.g. Lubin & Boice, 1997; Hendry et al., 2009). These natural levels of radiation are still 20-fold less than the maximum levels present today at Chernobyl. Mutations are changes in genomic sequences of DNA that may occur as a consequence of breakage of a single or double strand of DNA. DNA repair can restore sequences of DNA, most readily single-strand, but also double-strand DNA (Lehman, 2006; von Sonntag, 2010). Somatic mutations are sometimes the source of genetic diseases including cancer, while germ-line mutations can be transferred to offspring. Mutations are an important source of novel genetic variation (Hartl & Clark, 1997). That radiation is a powerful mutagen was shown by classical laboratory experiments (Nadson & Philippov, 1925; Muller, 1954; UNSCEAR, 1988; National Academy of Sciences – Natural Resources Council, 1990), but it is less well known that natural variation in levels of background radiation is also a significant cause of mutation (e.g. Forster et al., 2002); exposure to natural radon in homes is the second leading cause of lung cancer in the US (e.g. Lubin & Boice, 1997; WHO, 2009). However, we currently do not know the relative importance of radiation and, for example, dietary mutagens as causes of mutations, nor do we understand the average effect of naturally occurring background radiation on mutations. What are the consequences of natural variation in background radiation for evolution? Given the current 1000-fold difference in natural levels of background radiation such effects should be measurable in both past and current rates of mutations, but we are unaware of any studies investigating such effects. A partial answer may come from a recent study of the relationship between local population density and radiation at Chernobyl arising from the catastrophe on 26 April 1986. Different species of birds in the Chernobyl area vary enormously in their tolerance of radiation; some species have similar local densities at high and low levels of radiation, while other species have dramatically reduced population densities at sites with high radiation levels. Møller et al. (2010) showed that historical mitochondrial mutation rates in birds, as reflected by DNA substitution rates, were positively correlated with the impact of radiation from Chernobyl on local population density, independent of all known confounding variables correlated with mitochondrial DNA (mtDNA) substitution rates. Thus, species that were ecologically strongly impacted by radiation around Chernobyl, as shown by reduced densities at high levels of radiation, were also those most strongly impacted by mutagens in the past as reflected by high substitution rates. Although other factors (e.g. variation in historical population sizes, mutational biases related to DNA composition and interactions, and selection) also likely affected historical mtDNA substitution rates (e.g. Gaut et al., 2011), we can conclude that current sensitivity to radiation at least in part reflects past sensitivity to mutagens in general. Very few mutations are beneficial; most are slightly deleterious or neutral (e.g. Lynch et al., 1999; Eyre-Walker & Keightley, 2007). If mutation rates are elevated in areas with high natural levels of background radiation, we should be able to demonstrate fitness costs of radiation. For example, it is well known that mutations are the source of many cancers and other diseases (e.g. Valko et al., 2004). It is also well known that cancer caused by radon shows enormous spatial variability so that foci of such cancers are concentrated in areas with specific rock substrata (e.g. Lubin & Boice, 1997). Are there effects of such natural variation in radiation on the incidence of diseases such as cancer, and hence intensity of selection to repair mutations more efficiently? If radiation at ‘natural’ levels can be shown to have negative fitness consequences for plants and animals, even though such natural levels may be modest, there is a reason to expect that higher doses due to nuclear accidents will have even larger negative fitness consequences. The flipside of negative fitness consequences is evolutionary adaptation to radiation. If organisms are exposed to the negative effects of radiation for long periods of time, we could expect that some individuals may become radio-tolerant, showing normal or even enhanced survival and reproduction in the face of radiation. If such variation in the ability to cope with radiation had a genetic basis, resistance to radiation would be selected, even if such resistance was associated with a physiological cost. The end point of evolutionary adaptation to radiation is exploitation of radiation to the advantage of the individual. For example, several micro-fungi and bacteria associated with thermal vents and deserts are able to live under extremely high radiation levels (e.g. Brooks & Murray, 1981; Suzuki et al., 1988; Jolivet et al., 2003, 2004; de Groot et al., 2005; Chanal et al., 2006; Shravage et al., 2007; Charmasson et al., 2009; Daly, 2009). Several micro-fungi from irradiated areas are directly attracted by radionuclides (positive radiotropism), being able to grow upon ‘hot particles’ and even degrade them (Zhdanova et al., 2004). Furthermore, in some cases ionizing radiation has a positive stimulatory effect on spore germination (Tugay et al., 2006). Finally, exposure to ionizing radiation increases the growth of some melanized fungi while simultaneously transferring electrons to melanin. This has led to speculation that these redox properties might even be used to transduce energy for cell metabolism, thereby enhancing growth (Dadachova et al., 2007; Dadachova & Casadevall, 2008). A slightly different aspect of adaptation to radiation and acquisition of fitness benefits from radiation exposure is hormesis; the suggestion that organisms may benefit from an hypothesised stimulatory effect of low levels of radiation compared to the absence of radiation (e.g. Planel et al., 1987; Wolff, 1989). There is an extensive literature on this subject in humans and other organisms [see reviews in Kondo (1993) and Luckey (1991)]. Mossman (2001) emphasized that the evidence is open to alternative interpretations: data purported to provide evidence for radiation hormetic effects in humans are based on epidemiological findings used to test different hypotheses; hormetic effects are weak at best and inconsistent; there is no consensus on how these presumed benefits are defined or quantified; and it remains unclear how hormesis can be classified between the Scylla of beneficial health effects and the Charybdis of requirements for protection of health. Here we suggest that the documented consequences of naturally increased levels of background radiation have important implications for hormesis. In particular, we would expect that radiation hormetic effects should be found in areas with higher levels of natural background radiation because of adaptation to such enhanced levels of radiation, and we predict that on average radiation should have positive effects on the wellbeing of humans and other organisms if hormesis operates at naturally occurring low-dose radiation. The objectives of this review of the effects of natural variation in radiation levels on free-living organisms were fourfold. (i) To review the effects of natural levels of radiation on mutation rates, DNA repair, and other genetic mechanisms. (ii) To review the evidence for the effects of natural levels of radiation on physiology, immunology and disease frequency. If there is adaptation to local radiation levels, then the relationship between radiation levels and the measured effect might be weaker than expected based solely on the direct effect of radiation on mutation rates (i.e. there is a confounding variable of the extent to which mutations are repaired). (iii) To review the evidence for radiation resistance to assess its prevalence in natural populations. (iv) To review the extent to which natural variation in background radiation has positive hormetic effects on health, fecundity and longevity. We emphasize that we do not review literature on the effects of radiation from nuclear accidents, nuclear weapons tests, medical treatments, or similar human-induced exposures, although such studies may prove useful for testing whether radio-resistant organisms predominate in such contaminated sites and whether resistance can change in response to altered background radiation levels. The information that is derived from this quantitative meta-analysis will help us to understand the role of radiation in the balance between mutation, selection and evolution, a topic of general interest in the field of evolutionary genetics. Information on radio-tolerance may help to focus future research in an attempt to understand the role of radiation in contemporary ecological and evolutionary processes. Finally, this review attempts to provide baseline information concerning the potential consequences of nuclear accidents like those at Chernobyl and Fukushima.
II. METHODS
(1) Literature search
We conducted an extensive search for all scientific papers on natural levels of radiation, radioactivity, radio-tolerance and radio-resistance, using the Web of Science and Google Scholar and the key words ‘radiation’, ‘radioactivity’, ‘radio-tolerance’, ‘radio-resistance’ and ‘high background radiation’ combined with ‘natural’. This was followed by subsequent searches for literature concerning natural radioactivity and ‘mutation*’, ‘physiology’, ‘immunology’ and ‘disease’. We also attempted to find all papers that cited Grüneberg et al. (1966), Gopal-Ayengar et al. (1970), Ahuja et al. (1973), Barcinski et al. (1975), Kochupillai et al. (1976) and Pillai, Thangavelu & Ramalingaswami (1976), which are considered seminal papers in this field. We searched all reference lists in the resulting list of publications for further papers that could include relevant information. The inclusion criteria for all publications were that: (i) they compared at least one control population with a low level of background radiation and one population with high background radiation; (ii) they had test statistics that could be converted into effect sizes; and (iii) they reported background radiation levels for both control and irradiated populations. We examined more than 5000 papers to arrive at the 46 publications included in our meta-analysis. These publications had 373 effect sizes, or 8.1 effect sizes per publication. These were reduced to 66 effect sizes because some of the 46 publications reported effects on more than1 species. We excluded the extensive literature on radon because this literature has already been reviewed elsewhere (e.g. Lubin & Boice, 1997; Hendry et al., 2009), and its volume would swamp the fewer publications reviewed herein. We located 56 publications on radio-tolerant and radio-resistant species within the initial 5000 papers. The cut-off date for inclusion of studies was 31 December 2011.
Because many of these papers were difficult to acquire through ordinary libraries, we have made available a directory containing copies of the papers used for this review of natural sources of radiation (http://cricket.biol.sc.edu/papers/natural/). (2) Extracting data
We extracted test statistics (t, F, c2) for all studies together with information on the number of populations under study (this was typically one high background radiation area and one control area) and the number of individuals studied. If no statistics were reported, we extracted means (S.E.M.) and conducted standard parametric tests for comparison of means, or we extracted all data and conducted regression analyses. If only a maximum probability value was reported, we conservatively estimated the Pearson correlation coefficient required for the given sample size to achieve the reported probability. If several effects were reported, we used the effect that controlled for confounding variables such as age or smoking in order to be conservative. In five studies included in the mean effect size calculations see Table 2 we conservatively used the number of populations rather than the number of subjects because the latter was not reported; in cases of cancer deaths (Körblein & Hoffmann, 2006) use of the size of the underlying total population would seriously distort our study findings towards the effect size in those studies. Therefore, for these five studies we used the number of populations to be conservative. Effect sizes estimated in the present review therefore are conservative. In total we obtained 373 effect-size estimates (Table 1). Table 1. Effect sizes for studies of effects of natural levels of radiation on biological response variables
Species Kingdom Effect Category References Confounding variables controlled Test statistic Direction of effect Value of test statistic r N No. populations Radiation level (mSv/year)
Confounding variables controlled: 0 – no, 1- yes; direction of effect: −1 implies decrease with increasing radiation level, 1 implies increase with increasing radiation level; r, Pearson r; N, sample size. Note that radiation levels are estimates based on maximum dose rates.
Allium cepa Plant DNA damage assessed by comet assay Mutation Saghirzadeh et al. (2008) 1 r 1 0.936 0.936 13 13 87.60
Calotropis gigantea Plant Cytological abnormalities Mutation Gopal-Ayengar et al. (1970) 0 r 1 0.255 0.255 7 7 82.96
Crotalaria verrucosa Plant Cytological abnormalities Mutation Gopal-Ayengar et al. (1970) 0 r 1 0.894 0.894 5 5 82.96
Crotalaria verrucosa Plant Pollen sterility Mutation Gopal-Ayengar et al. (1970) 0 r 1 0.488 0.488 3 3 82.96
Croton bonplandianum Plant Cytological abnormalities Mutation Gopal-Ayengar et al. (1970) 0 r 1 0.124 0.124 9 9 82.96
Homo sapiens Animal Aneuploid cells Mutation Barcinski et al. (1975) 1 t −1 0.029 −0.002 349 2 6.40
Homo sapiens Animal Chromatid aberrations Mutation Barcinski et al. (1975) 1 t −1 1.580 −0.085 349 2 6.40
Homo sapiens Animal Deletions Mutation Barcinski et al. (1975) 1 t 1 2.550 0.136 349 2 6.40
Homo sapiens Animal Dicentrics Mutation Barcinski et al. (1975) 1 t 1 2.380 0.127 349 2 6.40
Homo sapiens Animal Rings Mutation Barcinski et al. (1975) 1 t 1 2.490 0.132 349 2 6.40
Homo sapiens Animal Chromatid aberrations Mutation Barcinski et al. (1975) 1 t 1 1.580 0.085 349 2 6.40
Homo sapiens Animal Total number of breaks Mutation Barcinski et al. (1975) 1 t 1 4.910 0.255 349 2 6.40
Homo sapiens Animal Variance smaller for three out of six dermatoglyphic traits in contaminated area Morphology Ahuja et al. (1973) 0 F −1 1.450 −0.106 130 2 32.98
Homo sapiens Animal Variance smaller for three out of six dermatoglyphic traits in contaminated area Morphology Ahuja et al. (1973) 0 F 1 1.220 0.097 130 2 32.98
Homo sapiens Animal Variance smaller for three out of six dermatoglyphic traits in contaminated area Morphology Ahuja et al. (1973) 0 F −1 1.340 −0.102 130 2 32.98
Homo sapiens Animal Variance smaller for three out of six dermatoglyphic traits in contaminated area Morphology Ahuja et al. (1973) 0 F 1 1.620 0.112 130 2 32.98
Homo sapiens Animal Variance smaller for three out of six dermatoglyphic traits in contaminated area Morphology Ahuja et al. (1973) 0 F 1 2.050 0.126 130 2 32.98
Homo sapiens Animal Variance smaller for three out of six dermatoglyphic traits in contaminated area Morphology Ahuja et al. (1973) 0 F −1 2.190 −0.130 130 2 32.98
Homo sapiens Animal Antioxidant levels reduced Physiology Attar et al. (2007) 1 t 1 27.990 0.943 100 4 260.00
Homo sapiens Animal Neutrophil activity Immunology Attar et al. (2007) 1 t 1 15.200 0.838 100 4 260.00
Homo sapiens Animal Phagocytosis Immunology Attar et al. (2007) 1 t 1 20.340 0.899 100 4 260.00
Homo sapiens Animal Locomotion of peripheral neutrophils Immunology Attar et al. (2007) 1 t 1 32.650 0.957 100 4 260.00
Homo sapiens Animal Interleukine-2 Immunology Attar et al. (2007) 1 t 1 14.150 0.819 100 4 260.00
Homo sapiens Animal Interleukine-4 Immunology Attar et al. (2007) 1 t 1 24.190 0.925 100 4 260.00
Homo sapiens Animal Interleukine-10 Immunology Attar et al. (2007) 1 t 1 25.710 0.933 100 4 260.00
Homo sapiens Animal Interferon-gamma Immunology Attar et al. (2007) 1 t −1 11.110 −0.747 100 4 260.00
Homo sapiens Animal Proliferation Immunology Attar et al. (2007) 1 t −1 2.670 −0.260 100 4 260.00
Homo sapiens Animal Whorls, loops and arches Morphology Bhasin et al. (1980) 1 Chi-square 1 3.315 0.226 65 2 17.52
Homo sapiens Animal Whorls, loops and arches Morphology Bhasin et al. (1980) 1 Chi-square 1 4.304 0.257 65 2 17.52
Homo sapiens Animal Whorls, loops and arches Morphology Bhasin et al. (1980) 1 Chi-square 1 12.818 0.573 39 2 17.52
Homo sapiens Animal Whorls, loops and arches Morphology Bhasin et al. (1980) 1 Chi-square 1 0.480 0.099 49 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.576 0.092 69 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F −1 1.526 −0.149 69 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F −1 1.017 −0.122 69 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.681 0.100 69 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 1.748 0.159 69 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F −1 1.051 −0.124 69 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.816 0.110 69 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F −1 1.530 −0.149 69 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F −1 1.069 −0.125 69 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F −1 1.023 −0.123 69 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F −1 1.100 −0.131 65 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F −1 1.085 -0.130 65 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.993 0.125 65 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F −1 1.317 −0.143 65 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F −1 2.137 −0.181 65 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.724 0.103 69 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.714 0.103 69 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.461 0.083 69 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.576 0.092 69 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.714 0.103 69 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.643 0.131 39 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.484 0.114 39 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.385 0.101 39 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F −1 1.303 −0.184 39 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.415 0.105 39 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.587 0.125 39 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.962 0.159 39 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.646 0.131 39 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.368 0.099 39 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F −1 1.188 −0.157 49 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F −1 1.043 −0.147 49 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.642 0.116 49 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.565 0.109 49 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.516 0.104 49 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.664 0.118 49 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.548 0.107 49 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.587 0.111 49 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.752 0.125 49 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.575 0.110 49 2 17.52
Homo sapiens Animal Finger ridge count Morphology Bhasin et al. (1980) 1 F 1 0.924 0.139 49 2 17.52
Homo sapiens Animal Main line formulae Morphology Bhasin et al. (1980) 1 Chi-square 1 3.202 0.222 65 2 17.52
Homo sapiens Animal Main line formulae Morphology Bhasin et al. (1980) 1 Chi-square 1 0.241 0.061 65 2 17.52
Homo sapiens Animal Main line formulae Morphology Bhasin et al. (1980) 1 Chi-square 1 5.938 0.390 39 2 17.52
Homo sapiens Animal Main line formulae Morphology Bhasin et al. (1980) 1 Chi-square 1 2.199 0.212 49 2 17.52
Homo sapiens Animal Line D distribution Morphology Bhasin et al. (1980) 1 Chi-square −1 0.966 −0.122 65 2 17.52
Homo sapiens Animal Line D distribution Morphology Bhasin et al. (1980) 1 Chi-square −1 0.051 −0.028 65 2 17.52
Homo sapiens Animal Line D distribution Morphology Bhasin et al. (1980) 1 Chi-square −1 0.702 −0.134 39 2 17.52
Homo sapiens Animal Line D distribution Morphology Bhasin et al. (1980) 1 Chi-square 1 6.365 0.360 49 2 17.52
Homo sapiens Animal Hypothenar Morphology Bhasin et al. (1980) 1 Chi-square −1 0.024 −0.019 65 2 17.52
Homo sapiens Animal Hypothenar Morphology Bhasin et al. (1980) 1 Chi-square −1 0.118 −0.043 65 2 17.52
Homo sapiens Animal Hypothenar Morphology Bhasin et al. (1980) 1 Chi-square −1 2.669 −0.262 39 2 17.52
Homo sapiens Animal Hypothenar Morphology Bhasin et al. (1980) 1 Chi-square 1 5.929 0.348 49 2 17.52
Homo sapiens Animal Thenar I Morphology Bhasin et al. (1980) 1 Chi-square −1 1.615 −0.158 65 2 17.52
Homo sapiens Animal Thenar I Morphology Bhasin et al. (1980) 1 Chi-square −1 0.082 −0.036 65 2 17.52
Homo sapiens Animal Thenar I Morphology Bhasin et al. (1980) 1 Chi-square −1 0.045 −0.034 39 2 17.52
Homo sapiens Animal Thenar I Morphology Bhasin et al. (1980) 1 Chi-square −1 1.969 −0.200 49 2 17.52
Homo sapiens Animal Thenar II Morphology Bhasin et al. (1980) 1 Chi-square −1 0.172 −0.051 65 2 17.52
Homo sapiens Animal Thenar II Morphology Bhasin et al. (1980) 1 Chi-square −1 1.436 −0.149 65 2 17.52
Homo sapiens Animal Thenar II Morphology Bhasin et al. (1980) 1 Chi-square −1 0.363 −0.096 39 2 17.52
Homo sapiens Animal Thenar II Morphology Bhasin et al. (1980) 1 Chi-square −1 0.220 −0.067 49 2 17.52
Homo sapiens Animal Thenar III Morphology Bhasin et al. (1980) 1 Chi-square −1 0.150 −0.048 65 2 17.52
Homo sapiens Animal Thenar III Morphology Bhasin et al. (1980) 1 Chi-square −1 0.603 −0.096 65 2 17.52
Homo sapiens Animal Thenar III Morphology Bhasin et al. (1980) 1 Chi-square −1 0.563 −0.120 39 2 17.52
Homo sapiens Animal Thenar III Morphology Bhasin et al. (1980) 1 Chi-square −1 0.163 −0.058 49 2 17.52
Homo sapiens Animal Thenar IV Morphology Bhasin et al. (1980) 1 Chi-square −1 0.090 −0.037 65 2 17.52
Homo sapiens Animal Thenar IV Morphology Bhasin et al. (1980) 1 Chi-square −1 0.688 −0.103 65 2 17.52
Homo sapiens Animal Thenar IV Morphology Bhasin et al. (1980) 1 Chi-square −1 1.108 −0.169 39 2 17.52
Homo sapiens Animal Thenar IV Morphology Bhasin et al. (1980) 1 Chi-square 1 4.443 0.301 49 2 17.52
Homo sapiens Animal Interdigital ridge count a-b Morphology Bhasin et al. (1980) 1 F 1 0.846 0.115 65 2 17.52
Homo sapiens Animal Interdigital ridge count b-c Morphology Bhasin et al. (1980) 1 F −1 2.120 −0.180 65 2 17.52
Homo sapiens Animal Interdigital ridge count c-d Morphology Bhasin et al. (1980) 1 F 1 0.639 0.100 65 2 17.52
Homo sapiens Animal Interdigital ridge count a-d Morphology Bhasin et al. (1980) 1 F 1 0.828 0.114 65 2 17.52
Homo sapiens Animal Interdigital ridge count d-t Morphology Bhasin et al. (1980) 1 F −1 1.189 −0.136 65 2 17.52
Homo sapiens Animal Interdigital ridge count angle atd Morphology Bhasin et al. (1980) 1 F 1 3.398 0.226 65 2 17.52
Homo sapiens Animal Interdigital ridge count distance c-t Morphology Bhasin et al. (1980) 1 F 1 5.035 0.272 65 2 17.52
Homo sapiens Animal Interdigital ridge count a-b Morphology Bhasin et al. (1980) 1 F −1 1.453 −0.150 65 2 17.52
Homo sapiens Animal Interdigital ridge count b-c Morphology Bhasin et al. (1980) 1 F −1 2.053 −0.178 65 2 17.52
Homo sapiens Animal Interdigital ridge count c-d Morphology Bhasin et al. (1980) 1 F −1 1.529 −0.154 65 2 17.52
Homo sapiens Animal Interdigital ridge count a-d Morphology Bhasin et al. (1980) 1 F 1 1.010 0.126 65 2 17.52
Homo sapiens Animal Interdigital ridge count d-t Morphology Bhasin et al. (1980) 1 F −1 1.335 −0.144 65 2 17.52
Homo sapiens Animal Interdigital ridge count angle atd Morphology Bhasin et al. (1980) 1 F 1 3.172 0.219 65 2 17.52
Homo sapiens Animal Interdigital ridge count distance c-t Morphology Bhasin et al. (1980) 1 F 1 3.667 0.235 65 2 17.52
Homo sapiens Animal Interdigital ridge count a-b Morphology Bhasin et al. (1980) 1 F 1 0.874 0.117 65 2 17.52
Homo sapiens Animal Interdigital ridge count b-c Morphology Bhasin et al. (1980) 1 F −1 1.613 −0.158 65 2 17.52
Homo sapiens Animal Interdigital ridge count c-d Morphology Bhasin et al. (1980) 1 F −1 0.965 −0.123 65 2 17.52
Homo sapiens Animal Interdigital ridge count a-d Morphology Bhasin et al. (1980) 1 F 1 0.511 0.090 65 2 17.52
Homo sapiens Animal Interdigital ridge count d-t Morphology Bhasin et al. (1980) 1 F 1 0.396 0.079 65 2 17.52
Homo sapiens Animal Interdigital ridge count angle atd Morphology Bhasin et al. (1980) 1 F −1 0.497 −0.088 65 2 17.52
Homo sapiens Animal Interdigital ridge count distance c-t Morphology Bhasin et al. (1980) 1 F −1 0.371 −0.077 65 2 17.52
Homo sapiens Animal Interdigital ridge count a-b Morphology Bhasin et al. (1980) 1 F −1 2.186 −0.183 65 2 17.52
Homo sapiens Animal Interdigital ridge count b-c Morphology Bhasin et al. (1980) 1 F −1 0.973 −0.123 65 2 17.52
Homo sapiens Animal Interdigital ridge count c-d Morphology Bhasin et al. (1980) 1 F 1 0.699 0.105 65 2 17.52
Homo sapiens Animal Interdigital ridge count a-d Morphology Bhasin et al. (1980) 1 F 1 0.308 0.070 65 2 17.52
Homo sapiens Animal Interdigital ridge count d-t Morphology Bhasin et al. (1980) 1 F −1 1.043 −0.128 65 2 17.52
Homo sapiens Animal Interdigital ridge count angle atd Morphology Bhasin et al. (1980) 1 F −1 0.653 −0.101 65 2 17.52
Homo sapiens Animal Interdigital ridge count distance c-t Morphology Bhasin et al. (1980) 1 F 1 0.736 0.107 65 2 17.52
Homo sapiens Animal Interdigital ridge count a-b Morphology Bhasin et al. (1980) 1 F −1 1.201 −0.177 39 2 17.52
Homo sapiens Animal Interdigital ridge count b-c Morphology Bhasin et al. (1980) 1 F −1 1.327 −0.186 39 2 17.52
Homo sapiens Animal Interdigital ridge count c-d Morphology Bhasin et al. (1980) 1 F 1 0.651 0.131 39 2 17.52
Homo sapiens Animal Interdigital ridge count a-d Morphology Bhasin et al. (1980) 1 F −1 1.027 −0.164 39 2 17.52
Homo sapiens Animal Interdigital ridge count d-t Morphology Bhasin et al. (1980) 1 F 1 0.132 0.060 39 2 17.52
Homo sapiens Animal Interdigital ridge count angle atd Morphology Bhasin et al. (1980) 1 F 1 1.305 0.185 39 2 17.52
Homo sapiens Animal Interdigital ridge count distance c-t Morphology Bhasin et al. (1980) 1 F −1 0.353 −0.097 39 2 17.52
Homo sapiens Animal Interdigital ridge count a-b Morphology Bhasin et al. (1980) 1 F 1 0.361 0.098 39 2 17.52
Homo sapiens Animal Interdigital ridge count b-c Morphology Bhasin et al. (1980) 1 F −1 1.378 −0.189 39 2 17.52
Homo sapiens Animal Interdigital ridge count c-d Morphology Bhasin et al. (1980) 1 F −1 1.311 −0.185 39 2 17.52
Homo sapiens Animal Interdigital ridge count a-d Morphology Bhasin et al. (1980) 1 F −1 1.073 −0.168 39 2 17.52
Homo sapiens Animal Interdigital ridge count d-t Morphology Bhasin et al. (1980) 1 F 1 0.300 0.090 39 2 17.52
Homo sapiens Animal Interdigital ridge count angle atd Morphology Bhasin et al. (1980) 1 F 1 0.437 0.108 39 2 17.52
Homo sapiens Animal Interdigital ridge count distance c-t Morphology Bhasin et al. (1980) 1 F 1 0.812 0.147 39 2 17.52
Homo sapiens Animal Interdigital ridge count a-b Morphology Bhasin et al. (1980) 1 F −1 0.983 −0.143 49 2 17.52
Homo sapiens Animal Interdigital ridge count b-c Morphology Bhasin et al. (1980) 1 F −1 1.741 −0.189 49 2 17.52
Homo sapiens Animal Interdigital ridge count c-d Morphology Bhasin et al. (1980) 1 F 1 0.832 0.132 49 2 17.52
Homo sapiens Animal Interdigital ridge count a-d Morphology Bhasin et al. (1980) 1 F 1 0.735 0.124 49 2 17.52
Homo sapiens Animal Interdigital ridge count d-t Morphology Bhasin et al. (1980) 1 F 1 0.310 0.081 49 2 17.52
Homo sapiens Animal Interdigital ridge count angle atd Morphology Bhasin et al. (1980) 1 F −1 0.606 −0.113 49 2 17.52
Homo sapiens Animal Interdigital ridge count distance c-t Morphology Bhasin et al. (1980) 1 F −1 0.566 −0.109 49 2 17.52
Homo sapiens Animal Interdigital ridge count a-b Morphology Bhasin et al. (1980) 1 F −1 2.179 −0.210 49 2 17.52
Homo sapiens Animal Interdigital ridge count b-c Morphology Bhasin et al. (1980) 1 F −1 2.462 −0.223 49 2 17.52
Homo sapiens Animal Interdigital ridge count c-d Morphology Bhasin et al. (1980) 1 F 1 0.747 0.125 49 2 17.52
Homo sapiens Animal Interdigital ridge count a-d Morphology Bhasin et al. (1980) 1 F −1 1.525 −0.177 49 2 17.52
Homo sapiens Animal Interdigital ridge count d-t Morphology Bhasin et al. (1980) 1 F 1 0.601 0.112 49 2 17.52
Homo sapiens Animal Interdigital ridge count angle atd Morphology Bhasin et al. (1980) 1 F −1 0.682 −0.120 49 2 17.52
Homo sapiens Animal Interdigital ridge count distance c-t Morphology Bhasin et al. (1980) 1 F −1 0.736 −0.124 49 2 17.52
Homo sapiens Animal SRBC right S1 Morphology Bhasin et al. (1982) 1 Chi-square −1 2.340 −0.190 130 2 15.00
Homo sapiens Animal SRBC right S2 Morphology Bhasin et al. (1982) 1 Chi-square 1 1.231 0.134 130 2 15.00
Homo sapiens Animal SRBC right S3 Morphology Bhasin et al. (1982) 1 Chi-square −1 0.062 −0.031 130 2 15.00
Homo sapiens Animal SRBC right S4 Morphology Bhasin et al. (1982) 1 Chi-square 1 2.489 0.196 130 2 15.00
Homo sapiens Animal SRBC right S5 Morphology Bhasin et al. (1982) 1 Chi-square −1 0.303 −0.068 130 2 15.00
Homo sapiens Animal SRBC left S1 Morphology Bhasin et al. (1982) 1 Chi-square −1 0.207 −0.056 130 2 15.00
Homo sapiens Animal SRBC left S2 Morphology Bhasin et al. (1982) 1 Chi-square −1 0.381 −0.077 130 2 15.00
Homo sapiens Animal SRBC Left S3 Morphology Bhasin et al. (1982) 1 Chi-square −1 0.088 −0.037 130 2 15.00
Homo sapiens Animal SRBC left S4 Morphology Bhasin et al. (1982) 1 Chi-square 1 1.868 0.170 130 2 15.00
Homo sapiens Animal SRBC Left S5 Morphology Bhasin et al. (1982) 1 Chi-square 1 0.000 0.000 130 2 15.00
Homo sapiens Animal DRBC right S1 Morphology Bhasin et al. (1982) 1 Chi-square −1 0.383 −0.108 130 2 15.00
Homo sapiens Animal DRBC right S2 Morphology Bhasin et al. (1982) 1 Chi-square 1 0.000 0.000 130 2 15.00
Homo sapiens Animal DRBC right S3 Morphology Bhasin et al. (1982) 1 Chi-square −1 0.992 −0.152 130 2 15.00
Homo sapiens Animal DRBC right S4 Morphology Bhasin et al. (1982) 1 Chi-square −1 0.273 −0.065 130 2 15.00
Homo sapiens Animal DRBC right S5 Morphology Bhasin et al. (1982) 1 Chi-square 1 0.000 0.000 130 2 15.00
Homo sapiens Animal DRBC left S1 Morphology Bhasin et al. (1982) 1 Chi-square 1 0.000 0.000 130 2 15.00
Homo sapiens Animal DRBC left S2 Morphology Bhasin et al. (1982) 1 Chi-square 1 0.000 0.000 130 2 15.00
Homo sapiens Animal DRBC left S3 Morphology Bhasin et al. (1982) 1 Chi-square −1 0.656 −0.050 130 2 15.00
Homo sapiens Animal DRBC left S4 Morphology Bhasin et al. (1982) 1 Chi-square −1 0.004 −0.008 130 2 15.00
Homo sapiens Animal DRBC left S5 Morphology Bhasin et al. (1982) 1 Chi-square 1 0.000 0.000 130 2 15.00
Homo sapiens Animal DRBC right S6 Morphology Bhasin et al. (1982) 1 Chi-square 1 0.000 0.000 130 2 15.00
Homo sapiens Animal DRBC left S6 Morphology Bhasin et al. (1982) 1 Chi-square 1 0.000 0.000 130 2 15.00
Homo sapiens Animal TRBC right Morphology Bhasin et al. (1982) 1 Chi-square −1 0.010 −0.012 130 2 15.00
Homo sapiens Animal TRBC left Morphology Bhasin et al. (1982) 1 Chi-square −1 0.010 −0.012 130 2 15.00
Homo sapiens Animal Cancer rate Disease Binu et al. (2005) 1 r 1 0.100 0.100 205 2 82.96
Homo sapiens Animal Lymphocyte chromosomal aberrations dicentrics and rings Mutation Chen & Wei (1991) 1 t 1 1.867 0.128 210 2 3.30
Homo sapiens Animal Lymphocyte chromosomal aberrations dicentrics and rings Mutation Chen & Wei (1991) 1 t 1 3.294 0.216 224 2 3.30
Homo sapiens Animal Lymphocyte chromosomal aberrations translocations and inversions Mutation Chen & Wei (1991) 1 t 1 2.000 0.137 210 2 3.30
Homo sapiens Animal Lymphocyte chromosomal aberrations translocations and inversions Mutation Chen & Wei (1991) 1 t 1 2.667 0.176 224 2 3.30
Homo sapiens Animal Lymphocyte chromosomal aberrations dicentrics and rings Mutation Chen & Wei (1991) 1 t 1 0.105 0.007 221 2 3.30
Homo sapiens Animal Lymphocyte chromosomal aberrations dicentrics and rings Mutation Chen & Wei (1991) 1 t 1 2.933 0.227 161 2 3.30
Homo sapiens Animal Lymphocyte chromosomal aberrations translocations and inversions Mutation Chen & Wei (1991) 1 t 1 4.210 0.279 212 2 3.30
Homo sapiens Animal Lymphocyte chromosomal aberrations translocations and inversions Mutation Chen & Wei (1991) 1 t 1 3.250 0.219 212 2 3.30
Homo sapiens Animal Cancer mortality Disease Chen & Wei (1991) 1 r −1 .― 0.000 1035410 2 3.30
Homo sapiens Animal Cancer mortality Disease Chen & Wei (1991) 1 r −1 .― 0.001 968429 2 3.30
Homo sapiens Animal Mitotic cell divisions Mutation Chen & Wei (1991) 1 t 1 2.090 0.135 239 2 3.30
Homo sapiens Animal Mitotic cell divisions Mutation Chen & Wei (1991) 1 t 1 4.920 0.359 166 2 3.30
Homo sapiens Animal Mitotic cell divisions Mutation Chen & Wei (1991) 1 t 1 1.600 0.140 130 2 3.30
Homo sapiens Animal Unscheduled DNA synthesis Mutation Chen & Wei (1991) 1 t 1 0.910 0.133 48 2 3.30
Homo sapiens Animal Unscheduled DNA synthesis Mutation Chen & Wei (1991) 1 t 1 1.568 0.324 23 2 3.30
Homo sapiens Animal Unscheduled DNA synthesis Mutation Chen & Wei (1991) 1 t 1 1.242 0.203 38 2 3.30
Homo sapiens Animal Unscheduled DNA synthesis Mutation Chen & Wei (1991) 1 t 1 1.960 0.359 28 2 3.30
Homo sapiens Animal Chromosomal aberrations dicentrics Mutation Cheriyan et al. (1999) 1 t −1 0.056 −0.001 10230 2 35.00
Homo sapiens Animal Chromosomal aberrations translocations Mutation Cheriyan et al. (1999) 1 t 1 1.250 0.012 10230 2 35.00
Homo sapiens Animal Chromosomal aberrations inversions Mutation Cheriyan et al. (1999) 1 t −1 1.000 −0.010 10230 2 35.00
Homo sapiens Animal Chromosomal aberrations centric fragments Mutation Cheriyan et al. (1999) 1 t 1 2.800 0.028 10230 2 35.00
Homo sapiens Animal Chromosomal aberrations acentric fragments Mutation Cheriyan et al. (1999) 1 t −1 4.060 −0.040 10230 2 35.00
Homo sapiens Animal Chromosomal aberrations minutes Mutation Cheriyan et al. (1999) 1 t 1 0.000 0.000 10230 2 35.00
Homo sapiens Animal Chromosomal aberrations multiple aberrations Mutation Cheriyan et al. (1999) 1 t 1 2.200 0.022 10230 2 35.00
Homo sapiens Animal Chromosomal aberrations chromosome breaks Mutation Cheriyan et al. (1999) 1 t −1 4.900 −0.048 10230 2 35.00
Homo sapiens Animal Chromosomal aberrations chromosome gaps Mutation Cheriyan et al. (1999) 1 t −1 3.430 −0.034 10230 2 35.00
Homo sapiens Animal Chromosomal aberrations chromatid breaks Mutation Cheriyan et al. (1999) 1 t −1 2.000 −0.020 10230 2 35.00
Homo sapiens Animal Chromosomal aberrations chromatid gaps Mutation Cheriyan et al. (1999) 1 t −1 3.230 −0.032 10230 2 35.00
Homo sapiens Animal Chromosomal aberrations polyploids Mutation Cheriyan et al. (1999) 1 t 1 2.150 0.021 10230 2 35.00
Homo sapiens Animal Chromosomal aberrations endoreplications Mutation Cheriyan et al. (1999) 1 t −1 0.820 −0.008 10230 2 35.00
Homo sapiens Animal Chromosomal aberrations autosomal trisomies Mutation Cheriyan et al. (1999) 1 t −1 1.140 −0.009 16169 2 35.00
Homo sapiens Animal Chromosomal aberrations 48 XXY + 21 Mutation Cheriyan et al. (1999) 1 t 1 1.290 0.010 16169 2 35.00
Homo sapiens Animal Chromosomal aberrations 48 XXY + 21 + centric fragments Mutation Cheriyan et al. (1999) 1 t −1 0.180 −0.001 16169 2 35.00
Homo sapiens Animal Chromosomal aberrations sex chromosomal Mutation Cheriyan et al. (1999) 1 t 1 1.310 0.010 16169 2 35.00
Homo sapiens Animal Chromosomal aberrations deletions Mutation Cheriyan et al. (1999) 1 t −1 2.760 −0.022 16169 2 35.00
Homo sapiens Animal Chromosomal aberrations inversions Mutation Cheriyan et al. (1999) 1 t 1 1.210 0.010 16169 2 35.00
Homo sapiens Animal Chromosomal aberrations Robertsonian translocations Mutation Cheriyan et al. (1999) 1 t 1 1.210 0.010 16169 2 35.00
Homo sapiens Animal Chromosomal aberrations other translocations Mutation Cheriyan et al. (1999) 1 t −1 0.140 −0.001 16169 2 35.00
Homo sapiens Animal Frequency of micronuclei Mutation Das & Karuppasamy (2009) 1 t −1 0.003 −0.004 271 2 4.00
Homo sapiens Animal Telomere length Physiology Das et al. (2009) 1 t −1 0.880 −0.050 310 2 4.00
Homo sapiens Animal Mitochondrial DNA mutations Mutation Forster et al. (2002) 1 Chi-square 1 8.983 0.097 795 2 11.00
Homo sapiens Animal Surface proteins CD4+/CD69+ on T helper cells unstimulated Immunology Ghiassi-Nejad et al. (2004) 1 t −1 1.020 −0.115 80 2 13.00
Homo sapiens Animal Surface proteins CD8+/CD69+ on T helper cells unstimulated Immunology Ghiassi 1 t 1 0.000 0.000 80 2 13.00
Homo sapiens Animal Surface proteins CD4+/CD69+ on T helper cells stimulated Immunology Ghiassi 1 t 1 2.200 0.242 80 2 13.00
Homo sapiens Animal Surface proteins CD8+/CD69+ on T helper cells stimulated Immunology Ghiassi 1 t 1 0.520 0.059 80 2 13.00
Homo sapiens Animal Percentage stable cell aberrations Mutation Ghiassi 1 t 1 2.690 0.291 80 2 13.00
Homo sapiens Animal Percentage unstable cell aberrations Mutation Ghiassi 1 t 1 1.762 0.196 80 2 13.00
Homo sapiens Animal Chromosomal aberrations Mutation Hayata et al. (2000) 1 r −1 0.100 0.100 17 2 3.12
Homo sapiens Animal Chromosomal aberrations dicentric and ring chromosomes Mutation Hayata et al. (2004) 1 r 1 0.410 0.410 39 2 3.11
Homo sapiens Animal Chromosomal aberrations Mutation Hayata et al. (2004) 1 t 1 5.182 0.544 66 2 3.11
Homo sapiens Animal Congenital malformations Morphology Jaikrishan et al. (1999) 1 Chi-square 1 0.349 0.004 36805 2 2.84
Homo sapiens Animal Stillbirths Mutation Jaikrishan et al. (1999) 1 Chi-square 1 1.040 0.008 36805 2 2.84
Homo sapiens Animal Male cancer rate Disease Jayalekshmi et al. (2005) 1 r 1 0.022 0.022 179810 12 1.72
Homo sapiens Animal Female cancer rate Disease Jayalekshmi et al. (2005) 1 r −1 0.169 0.169 179810 12 1.72
Homo sapiens Animal Chromosomal aberrations with fragments Mutation Jiang et al. (2000) 1 F 1 5.823 0.365 40 2 149.00
Homo sapiens Animal Chromosomal aberrations without fragments Mutation Jiang et al. (2000) 1 F 1 3.669 0.297 40 2 149.00
Homo sapiens Animal Down's syndrome Disease Kochupillai et al. (1976) 0 Chi-square 1 4.480 0.870 12 2 22.50
Homo sapiens Animal Chromatid aberrations Mutation Kochupillai et al. (1976) 0 Chi-square 1 2.058 0.220 85 2 22.50
Homo sapiens Animal Chromosome aberrations Mutation Kochupillai et al. (1976) 0 Chi-square 1 10.527 0.498 85 2 22.50
Homo sapiens Animal Severe mental retardation Disease Kochupillai et al. (1976) 0 Chi-square 1 4.880 0.613 13 2 22.50
Homo sapiens Animal Cancer mortality Disease Körblein & Hoffmann (2006) 1 t 1 3.289 0.321 96 96 0.67
Homo sapiens Animal Child mortality Disease Körblein & Hoffmann (2006) 1 t 1 3.223 0.315 96 96 0.67
Homo sapiens Animal Initial DNA damage Mutation Masoomi et al. (2006) 1 F 1 27.627 0.529 73 3 10.20
Homo sapiens Animal Induced DNA damage Mutation Masoomi et al. (2006) 1 F 1 128.407 0.802 73 3 10.20
Homo sapiens Animal Vitamin C in plasma Physiology Masoomi et al. (2006) 1 t 1 1.200 0.020 73 3 10.20
Homo sapiens Animal Vitamin C in urine Physiology Masoomi et al. (2006) 1 t −1 1.840 0.046 73 3 10.20
Homo sapiens Animal Number of micronuclei before irradiation Mutation Mohammadi et al. (2006) 0 t −1 0.832 −0.164 27 2 13.00
Homo sapiens Animal No. micronuclei after irradiation Mutation Mohammadi et al. (2006) 0 t −1 2.905 −0.502 27 2 13.00
Homo sapiens Animal Cell apoptosis before irradiation Mutation Mohammadi et al. (2006) 0 t −1 0.668 −0.132 27 2 13.00
Homo sapiens Animal Cell apoptosis after irradiation Mutation Mohammadi et al. (2006) 0 t 1 4.261 0.649 27 2 13.00
Homo sapiens Animal DNA damage before irradiation Mutation Mohammadi et al. (2006) 0 t 1 10.074 0.896 27 2 13.00
Homo sapiens Animal DNA damage after irradiation Mutation Mohammadi et al. (2006) 0 t 1 8.856 0.871 27 2 13.00
Homo sapiens Animal Residual DNA damage after irradiation Mutation Mohammadi et al. (2006) 0 t 1 8.442 0.860 27 2 13.00
Homo sapiens Animal Residual DNA damage after irradiation Mutation Mohammadi et al. (2006) 0 t 1 5.491 0.739 27 2 13.00
Homo sapiens Animal DNA repaired Mutation Mohammadi et al. (2006) 0 t 1 4.467 0.666 27 2 13.00
Homo sapiens Animal Cancer rate Disease Monfared et al. (2010) 0 r −1 0.430 −0.430 184 184 0.53
Homo sapiens Animal Chromosome aberrations per cell Mutation Mortazavi & Karam (2005) 0 t 1 1.725 0.288 35 2 13.00
Homo sapiens Animal Chromosome aberrations per cell after exposure to 1.5 Gy Mutation Mortazavi & Karam (2005) 0 t 1 5.273 0.676 35 2 13.00
Homo sapiens Animal Chromosome aberrations per cell Mutation Mortazavi et al. (2005) 0 t 1 16.667 0.931 45 2 1.36
Homo sapiens Animal Chromosome aberrations per cell after exposure to 2 Gy gamma rays Mutation Mortazavi et al. (2005) 0 t −1 15.241 −0.919 45 2 1.36
Homo sapiens Animal Chromosome aberrations per cell Mutation Mortazavi et al. (2005) 0 t −1 0.625 −0.194 12 2 1.36
Homo sapiens Animal Chromosome aberrations per cell after exposure to 1.5 Gy Mutation Mortazavi et al. (2005) 0 t −1 9.213 −0.946 12 2 1.36
Homo sapiens Animal Cancer rates Disease Nair et al. (1999) 0 r −1 0.068 0.068 195962 2 2.03
Homo sapiens Animal Cancer rates women Disease Nair et al. (1999) 0 r −1 0.057 0.057 198848 2 2.03
Homo sapiens Animal Chromosomal and Down syndrome Mutation Padmanabhan et al. (2004) 1 Chi-square 1 4.310 0.008 62914 2 5.63
Homo sapiens Animal Autosomal dominant anomalies Mutation Padmanabhan et al. (2004) 1 Chi-square 1 6.270 0.010 62914 2 5.63
Homo sapiens Animal De novo cases of autosomal dominant anomalies Mutation Padmanabhan et al. (2004) 1 Chi-square 1 0.940 0.004 62914 2 5.63
Homo sapiens Animal Autosomal and X-linked recessives Mutation Padmanabhan et al. (2004) 1 Chi-square 1 9.096 0.012 62914 2 5.63
Homo sapiens Animal Congenital anomalies Morphology Padmanabhan et al. (2004) 1 Chi-square 1 0.600 0.003 62914 2 5.63
Homo sapiens Animal Multifactorial anomalies Morphology Padmanabhan et al. (2004) 1 Chi-square 1 7.010 0.011 62914 2 5.63
Homo sapiens Animal All thyroid swellings Disease Pillai et al. (1976) 0 Chi-square 1 0.128 0.023 250 2 15.00
Homo sapiens Animal All nodular swellings Disease Pillai et al. (1976) 0 Chi-square −1 2.777 0.023 250 2 15.00
Homo sapiens Animal Uninodular swellings Disease Pillai et al. (1976) 0 Chi-square 1 0.128 0.001 250 2 15.00
Homo sapiens Animal Number of copies of the sex determining SRY gene Mutation Premi et al. (2009) 1 r 1 0.579 0.579 21 2 2.03
Homo sapiens Animal Gene expression of sex determining SRY gene Mutation Premi et al. (2009) 1 r 1 0.526 0.526 21 2 9.00
Homo sapiens Animal Number of micro-deletions Mutation Premi et al. (2009) 1 Chi-square 1 1052.971 0.945 1180 3 2.03
Homo sapiens Animal DBY1 and DBY2 genes on the Y chromosome Mutation Premi et al. (2009) 1 Chi-square 1 227.780 0.439 1180 3 2.03
Homo sapiens Animal Microdeletions Mutation Premi et al. (2009) 1 Chi-square 1 583.790 0.703 1180 3 2.03
Homo sapiens Animal Extra amplicons for parts of their genomes Mutation Premi et al. (2009) 1 Chi-square 1 1144.208 0.985 1180 3 2.03
Homo sapiens Animal Gene duplication of Y chromosome Mutation Premi et al. (2009) 1 Chi-square 1 643.246 0.738 1180 3 2.03
Homo sapiens Animal Loss of Y chromosome Mutation Premi et al. (2009) 1 Chi-square 1 15.550 0.115 1180 3 2.03
Homo sapiens Animal Sex ratio Sex ratio Saadat (2003) 1 Chi-square 1 0.950 0.007 21857 2 13.00
Homo sapiens Animal Sex ratio Sex ratio Saadat (2003) 0 Chi-square −1 0.130 0.001 261509 2 13.00
Homo sapiens Animal Down's syndrome Disease Sundaram (1977) 1 Chi-square 1 2.800 0.483 12 2 22.50
Homo sapiens Animal Down's syndrome Disease Tao & Wei (1986) 1 Chi-square 1 2.821 0.010 26512 2 3.36
Homo sapiens Animal T-lymphocyte count Immunology Tao & Wei (1986) 1 t 1 0.129 0.000 168 2 3.36
Homo sapiens Animal Cell proliferation Immunology Tao & Wei (1986) 1 t 1 1.661 0.016 168 2 3.36
Homo sapiens Animal Morphological transformation rate of lymphocytes Immunology Tao & Wei (1986) 1 t 1 3.835 0.024 592 2 3.36
Homo sapiens Animal 31 hereditary diseases Disease Tao & Wei (1986) 1 Chi-square 1 0.002 0.000 26512 2 3.36
Homo sapiens Animal B-lymphocyte count Immunology Tao & Wei (1986) 1 t 1 2.150 0.012 166 2 3.36
Homo sapiens Animal Cancer rates Disease Tao et al. (2000) 1 t −1 0.145 0.000 393 2 6.40
Homo sapiens Animal Down's syndrome Disease Thampi et al. (2005) 1 Chi-square 1 6.085 0.098 632 2 82.96
Homo sapiens Animal Malformations Mutation Thampi et al. (2005) 1 Chi-square −1 2.080 −0.033 1869 2 82.96
Homo sapiens Animal Stillbirths Mutation Thampi et al. (2005) 1 Chi-square −1 0.000 −0.003 470 2 82.96
Homo sapiens Animal Karyotype anomalies Mutation Thampi et al. (2005) 1 t −1 0.282 −0.002 23844 2 82.96
Homo sapiens Animal Age-adjusted liver cancer incidence linear model for men Disease Ujeno (1983) 1 r 1 0.659 0.659 13 13 1.05
Homo sapiens Animal Standardized mortality ratio of leukemia for men Disease Ujeno (1983) 1 r −1 0.211 −0.211 46 46 1.05
Homo sapiens Animal Stomach cancer mortality in male population aged more than 40 years Disease Ujeno (1983) 1 r 1 0.802 0.802 649 649 1.05
Homo sapiens Animal Age-adjusted liver cancer incidence exponential model for men Disease Ujeno (1983) 1 r 1 0.694 0.694 13 13 1.05
Homo sapiens Animal Standardized mortality ratio of leukemia for women Disease Ujeno (1983) 1 r 1 0.110 0.110 46 46 1.05
Homo sapiens Animal Cancer as a cause of death Disease Veiga & Koifman (2005) 0 t 1 0.000 0.000 479 2 2.40
Homo sapiens Animal Oesophagus cancer as a cause of death Disease Veiga & Koifman (2005) 0 t −1 2.119 −0.480 17 2 2.40
Homo sapiens Animal Stomach cancer as a cause of death Disease Veiga & Koifman (2005) 0 t −1 1.524 −0.234 42 2 2.40
Homo sapiens Animal Larynx cancer as a cause of death Disease Veiga & Koifman (2005) 0 t −1 0.091 −0.034 9 2 2.40
Homo sapiens Animal Lung cancer as a cause of death Disease Veiga & Koifman (2005) 0 t −1 1.372 −0.226 37 2 2.40
Homo sapiens Animal Female breast cancer as a cause of death Disease Veiga & Koifman (2005) 0 t −1 1.156 −0.245 23 2 2.40
Homo sapiens Animal Prostrate cancer as a cause of death Disease Veiga & Koifman (2005) 0 t 1 1.206 0.205 35 2 2.40
Homo sapiens Animal Leukaemia as a cause of death Disease Veiga & Koifman (2005) 0 t 1 0.000 0.000 19 2 2.40
Homo sapiens Animal Cancer as a cause of death Disease Veiga & Koifman (2005) 0 t 1 10.045 0.287 1122 2 3.40
Homo sapiens Animal Oesophagus cancer as a cause of death Disease Veiga & Koifman (2005) 0 t 1 2.541 −0.421 32 2 3.40
Homo sapiens Animal Stomach cancer as a cause of death Disease Veiga & Koifman (2005) 0 t −1 3.121 0.263 133 2 3.40
Homo sapiens Animal Larynx cancer as a cause of death Disease Veiga & Koifman (2005) 0 t 1 0.761 0.172 21 2 3.40
Homo sapiens Animal Lung cancer as a cause of death Disease Veiga & Koifman (2005) 0 t 1 2.660 0.245 113 2 3.40
Homo sapiens Animal Female breast cancer as a cause of death Disease Veiga & Koifman (2005) 0 t 1 3.155 0.340 78 2 3.40
Homo sapiens Animal Prostrate cancer as a cause of death Disease Veiga & Koifman (2005) 0 t 1 1.089 0.145 57 2 3.40
Homo sapiens Animal Leukaemia as a cause of death Disease Veiga & Koifman (2005) 0 t 1 2.117 0.295 49 2 3.40
Homo sapiens Animal Cancer as a cause of death Disease Veiga & Koifman (2005) 0 t 1 1.764 0.081 468 2 6.40
Homo sapiens Animal Oesophagus cancer as a cause of death Disease Veiga & Koifman (2005) 0 t 1 2.100 0.315 42 2 6.40
Homo sapiens Animal Stomach cancer as a cause of death Disease Veiga & Koifman (2005) 0 t 1 3.468 0.347 90 2 6.40
Homo sapiens Animal Larynx cancer as a cause of death Disease Veiga & Koifman (2005) 0 t 1 0.104 0.039 9 2 6.40
Homo sapiens Animal Lung cancer as a cause of death Disease Veiga & Koifman (2005) 0 t 1 2.814 0.309 77 2 6.40
Homo sapiens Animal Female breast cancer as a cause of death Disease Veiga & Koifman (2005) 0 t 1 0.762 0.148 28 2 6.40
Homo sapiens Animal Prostrate cancer as a cause of death Disease Veiga & Koifman (2005) 0 t 1 2.971 0.401 48 2 6.40
Homo sapiens Animal Leukaemia as a cause of death Disease Veiga & Koifman (2005) 0 t −1 0.035 −0.008 19 2 6.40
Homo sapiens Animal Other abnormalities Disease Wang et al. (1990) 1 t −1 2.053 −0.046 2006 2 3.30
Homo sapiens Animal All nodular disease Disease Wang et al. (1990) 1 t 1 1.325 0.030 2006 2 3.30
Homo sapiens Animal Thyroxine-free serum (T4) Disease Wang et al. (1990) 1 t −1 0.417 −0.018 550 2 3.30
Homo sapiens Animal Tiiodo-thryroxine-free serum (T3) Disease Wang et al. (1990) 1 t 1 0.400 0.017 550 2 3.30
Homo sapiens Animal Anti-mitochondrial antibody serum (AMA) Disease Wang et al. (1990) 1 t 1 0.600 0.026 550 2 3.30
Homo sapiens Animal Urinary iodine-creatinine Disease Wang et al. (1990) 1 t 1 6.842 0.380 279 2 3.30
Homo sapiens Animal Urinary iodine Disease Wang et al. (1990) 1 t −1 3.231 −0.191 279 2 3.30
Homo sapiens Animal Translocations Mutation Wang et al. (1990) 1 t 1 0.571 0.041 200 2 3.30
Homo sapiens Animal Inversions Mutation Wang et al. (1990) 1 t 1 0.800 0.057 200 2 3.30
Homo sapiens Animal Deletions Mutation Wang et al. (1990) 1 t 1 2.800 0.195 200 2 3.30
Homo sapiens Animal Unstable chromosomal aberrations Mutation Wang et al. (1990) 1 t 1 3.333 0.230 200 2 3.30
Homo sapiens Animal Prevalence of 31 hereditary diseases Disease Wei et al. (1990) 1 Chi-square 1 0.002 0.000 26572 2 3.37
Homo sapiens Animal Cancer mortality Disease Wei et al. (1990) 1 r −1 0.002 0.002 632280 2 3.37
Homo sapiens Animal Down's syndrome Disease Wei et al. (1990) 1 Chi-square 1 2.820 0.010 26572 2 3.37
Homo sapiens Animal Down's syndrome Disease Wei et al. (1990) 1 Chi-square 1 5.624 0.011 47095 2 3.37
Homo sapiens Animal Nodular disease Disease Wei et al. (1990) 1 Chi-square 1 0.017 0.003 2006 2 3.37
Homo sapiens Animal Chromosomal translocations Mutation Zhang et al. (2003) 1 F 1 0.004 0.010 40 2 2.75
Homo sapiens Animal Chromosomal translocations Mutation Zhang et al. (2004) 1 F 1 6.117 0.330 52 2 2.71
Homo sapiens Animal Cancer rates Disease Zou et al. (2005) 1 t 1 0.000 0.000 1202 2 6.37
Homo sapiens Animal Non-cancer mortality Disease Zou et al. (2005) 1 t 1 1.960 0.020 10038 2 6.37
Ipomoea pes-caprae Plant Cytological abnormalities Mutation Gopal-Ayengar et al. (1970) 0 r 1 0.751 0.751 6 6 82.96
Ipomoea pes-caprae Plant Pollen sterility Mutation Gopal-Ayengar et al. (1970) 0 r 1 0.414 0.414 6 6 82.96
Launaea pinnatifida Plant Cytological abnormalities Mutation Gopal-Ayengar et al. (1970) 0 r 1 0.983 0.983 5 5 82.96
Launaea pinnatifida Plant Pollen sterility Mutation Gopal-Ayengar et al. (1970) 0 r 1 0.751 0.751 5 5 82.96
Lochnera rosea Plant Cytological abnormalities Mutation Gopal-Ayengar et al. (1970) 0 r 1 0.934 0.934 11 11 49.06
Lochnera rosea Plant Cytological abnormalities Mutation Gopal-Ayengar et al. (1970) 0 r 1 0.749 0.749 11 11 49.06
Lochnera rosea Plant Cytological abnormalities Mutation Gopal-Ayengar et al. (1970) 0 r 1 0.896 0.896 11 11 82.96
Lochnera rosea Plant Pollen sterility Mutation Gopal-Ayengar et al. (1970) 0 r 1 0.538 0.538 11 11 82.96
Rattus rattus Animal Standardized variance in tooth measurements Morphology Grüneberg et al. (1966) 1 t −1 0.159 −0.005 855 16 8.53
Rattus rattus Animal Mean skeletal character value Morphology Grüneberg et al. (1966) 1 t 1 1.997 0.068 855 16 8.53
Rattus rattus Animal Variance in skeletal character values Morphology Grüneberg et al. (1966) 1 t −1 0.612 −0.021 855 16 8.53
Rattus rattus Animal Fossa olecrani perforata Morphology Grüneberg et al. (1966) 1 Chi-square −1 38.494 −0.212 855 16 8.53
Rattus rattus Animal Foramen hypoglossi double Morphology Grüneberg et al. (1966) 1 Chi-square −1 19.926 −0.153 855 16 8.53
Rattus rattus Animal Maxillary foramen double Morphology Grüneberg et al. (1966) 1 Chi-square 1 0.600 0.026 855 16 8.53
Rattus rattus Animal Metoptic roots abnormal Morphology Grüneberg et al. (1966) 1 Chi-square −1 74.558 −0.295 855 16 8.53
Rattus rattus Animal Pregancy rate Fecundity Grüneberg et al. (1966) 1 Chi-square 1 0.025 0.007 469 16 8.53
Rattus rattus Animal Dead embryos Mutation Grüneberg et al. (1966) 1 Chi-square −1 0.018 −0.007 399 16 8.53
Rattus rattus Animal Pre-implantation loss Mutation Grüneberg et al. (1966) 1 Chi-square −1 1.258 −0.064 307 16 8.53
Rattus rattus Animal Post-implantation loss Mutation Grüneberg et al. (1966) 1 Chi-square 1 0.001 0.002 372 16 8.53
Rattus rattus Animal Standardized variance in tooth measurements females Morphology Grüneberg et al. (1966) 1 t −1 0.718 −0.025 855 16 8.53
Rattus rattus Animal Metoptic roots abnormal Morphology Grüneberg et al. (1966) 1 t −1 0.721 −0.025 855 16 8.53
Tradescantia sp. Plant Stamen hair mutations Mutation de Azevedo Gomes et al. (2002) 1 t 1 4.004 0.853 20 2 7.89
Tradescantia sp. Plant Stamen hair mutations Mutation de Azevedo Gomes et al. (2002) 1 t 1 1.692 0.568 20 2 31.56
Tradescantia sp. Plant Stamen hair mutations Mutation de Azevedo Gomes et al. (2002) 1 t 1 2.661 0.736 20 2 52.60
Tradescantia sp. Plant Stamen hair mutations Mutation de Azevedo Gomes et al. (2002) 1 t 1 1.434 0.505 20 2 110.46
Tradescantia sp. Plant Stamen hair mutations Mutation de Azevedo Gomes et al. (2002) 1 t 1 3.277 0.801 20 2 215.66
Tradescantia sp. Plant Stamen hair mutations Mutation de Azevedo Gomes et al. (2002) 1 t 1 3.587 0.826 20 2 263.00
Tradescantia sp. Plant Stamen hair mutations Mutation de Azevedo Gomes et al. (2002) 1 t 1 0.772 0.300 20 2 526.00
Tradescantia sp. Plant Stamen hair mutations Mutation Nayar et al. (1970) 1 r 1 0.784 0.784 4 2 95.09
Tyto alba Animal Intensity of pheomelanin colour Physiology Galván & Alonso-Alvarez (2011) 0 t 1 2.250 0.030 376 18 1.40
Table 2. Mean effect sizes weighted by sample size, their confidence intervals, number of studies, heterogeneity (QT) among studies (global test) or among categories, degrees of freedom (d.f.) for the heterogeneity test and probability (P) for this heterogeneity test for different groupings of the data set listed in Table 1
Category Mean effect size Bootstrap 95% confidence interval No. studies QT d.f. P
All studies 0.093 0.039, 0.171 66 952.41 65 1000 Gy Kopylov et al. (1993)
Rubrobacter radiotolerans Resistance to γ-radiation source Resistance to 11000 Gy Suzuki et al. (1988) and Ferreira et al. (1999)
Rubrobacter xylanophilus Resistance to γ-radiation source Resistance to 5500 Gy Ferreira et al. (1999)
Desulfurococcus amyloliticus Resistance to γ-radiation source > 2500 Gy Kopylov et al. (1993)
Deinococcus radiodurans Resistance to γ-radiation source 10000 Gy Brooks & Murray (1981) and Ito et al. (1983)
Deinococcus deserti Resistance to γ-radiation source 15000 Gy De Groot et al. (2005)
Deinococcus radiopugnans Extremely efficient DNA repair 1500 rad Minton (1994)
Deinococcus proteolyticus Extremely efficient DNA repair 1500 rad Minton (1994)
Deinococcus radiophilus Extremely efficient DNA repair 1500 rad Minton (1994)
Deinococcus geothermalis Resistance to γ-radiation 7300 Gy Ferreira et al. (1997)
Deinococcus murrayi Resistance to γ-radiation 3700 Gy Ferreira et al. (1997)
Deinococcus Nine new species Resistance to 30000 Gy Rainey et al. (2005)
Deinobacter grandis ― ― Minton (1994)
Cryptococcus neoformans Resistance to γ-radiation source Resistance to 4000 Gy Dadachova et al. (2004)
Histoplasma capsulatum Resistance to γ-radiation source Resistance to 4000 Gy Dadachova et al. (2004)
Pyrococcus abyssi Resistance to γ-radiation source Maximum of 2500 Gy Gérard et al. (2001)
Pyrococcus furiosus Resistance to high γ-radiation source Chromosome fully restored following fragmentation caused by 2500 Gy DiRuggiero et al. (1997)
Geodermatophilus sp. Resistance to γ-radiation source Resistance to 30000 Gy Rainey et al. (2005)
Hymenobacter actinosclerus Resistance to γ-radiation source Resistance to 3500 Gy Collins et al. (2000)
Hymenobacter sp. Resistance to γ-radiation source Resistance to 30000 Gy Rainey et al. (2005)
Metazoa:
Caenorhabditis elegans Resistance to irradiation, but subsequently sterile Resistance to 5000 Gy Johnson & Hartman (1988)
Bdelloid rotifers Adineta vaga and Philodina roseola Resistance to irradiation, but subsequently sterile Survives 1120 Gy, which is much higher than in a desiccation-intolerant rotifer Gladyshev & Meselson (2008)
Milnesium tardigradum Resistance to γ-radiation source and heavy ions Resistance up to 6200 Gy in hydrated animals and 5200 Gy in anhydrobiotic animals. Survival dose-dependent, but sterility complete above 1000 Gy Horikawa et al. (2006)
Drosophila melanogaster Differences between two strains in maturation rates and mutation frequency linked to radiation ― Strømnæs (1955, 1959)
Drosophila melanogaster Differences in radio-resistance among three strains due to dominant effects ― Ogaki & Nakashima-Tanaka (1966)
Drosophila melanogaster Mortality analysis of iso-female lines showed significant strain and strain-by-dose effects. Additive differences from a 4 × 4 diallelic cross, but low dominance and inter-chromosomal interaction effects 90000 and 110000 rads γ-radiation Parsons et al. (1969)
Drosophila nebulosa Mortality and reproductive performance differed among iso-female lines, and diallelic crosses showed evidence of additive differences 90000 rad Kratz (1975)
Drosophila willistoni Egg eclosion and reproductive performance differed significantly among areas ranging from 0.05 to 3.5 mR/h 1000 rad Cordeiro et al. (1973)
Bombyx mori Differences among lines ― Tazima (1957)
Bombyx mori Differences among lines ― Murakami & Tazima (1966)
Mus musculus LD50 was affected by a recessive genetic factor ― Kohn & Kalman (1956)
Mus musculus Difference among strains in number of offspring and duration of the fertile period ― Ehling (1964)
Mus musculus Variance in sensitivity is additive with a heritability of 0.55 ― Grahn (1958)
We are only aware of a single negative result: Varanda, Takahashi & Soares (1985) were unable to show radio-resistance in Melittobia hawaiiensis exposed to high levels of gamma radiation for many generations. Many studies have shown that selection in the laboratory for radio-resistance is effective (e.g. Wallace, 1952). We do not discuss such studies further here. By far the largest majority of studies showing radio-tolerance or radio-resistance are concerned with bacteria (Table 3). Deinococcus deserti were able to survive levels of radiation up to 15000 Gy (de Groot et al., 2005). Daly (2009) showed that manganese-based protein complexes could provide protection to DNA repair machinery thus permitting survival at very high radiation levels. Fungi constitute the other major group showing extreme radio-tolerance, even growing within the sarcophagus at Chernobyl (Zhdanova et al., 2000). Experimental studies have shown hyphal growth directed towards radiation sources (Zhdanova et al., 2004). Some metazoan bdelloid rotifers (Gladyshev & Meselson, 2008) and tardigrades (Horikawa et al., 2006) show an ability to survive high radiation doses, although this is accompanied by sterility. Drosophila spp., silkworm Bombyx mori and mouse Mus musculus show differences in resistance to radiation, although tolerance levels are many orders of magnitude lower than in bacteria and fungi (Table 3).
IV. DISCUSSION
The objectives of this review were to examine the effects of radiation on DNA, health, and radiation resistance, and to investigate evidence for the presence of hormesis (positive effects of radiation). We found extensive evidence of small, but significant negative effects of natural variation in background radiation on immunology, mutation and disease across a range of different species of animals and plants. This significant effect was robust to indirect tests for effects of publication bias as provided by the trim and fill procedure (Duval & Tweedie, 2000a, b). The effects for plants were much stronger than for animals, and studies conducted at higher natural radiation levels showed stronger effect sizes. Numerous studies have shown evidence of radio-resistance, mainly in bacteria and fungi, but also in Metazoa including fruitflies and mice; the extent of this radio-resistance differs among taxa.
The studies reviewed herein generally had a design that compared one or more control populations with a ‘normal’ level of background radiation with one or more populations that had a ‘high’ level of background radiation. More than 75% of all effect sizes consisted of comparisons of one control and one high-radiation population. If effects were entirely due to chance alone, we should expect equally many ‘positive’ and ‘negative’ effect sizes, with an expected mean of zero, which was clearly not the case. An explicit test for effects of level of replication showed no significant confounding effects. Typically the level of radiation in the high-radiation population was an order of magnitude above the level in the control population. Because such population comparisons are correlational in nature, they may be confounded by uncontrolled third variables. As a case in point, one of the first studies of the effects of high background radiation in Kerala, India, by Kochupillai et al. (1976) was subsequently criticised for not having properly controlled the incidence of Down's syndrome for differences in age of mothers in the control population and the high-radiation-level population (Sundaram, 1977). However, subsequent studies of the incidence of Down's syndrome in Kerala corrected for such confounding effects, and studies in other areas also have confirmed the initial observation. Subsequent studies have carefully tested and controlled study design for the confounding effects of age, sex, ethnicity, religion, consanguinity, smoking, unemployment rate and other factors. In fact, most studies of humans in high-radiation areas are characterized by extreme ethnic homogeneity because populations have been living in the study area for many generations. A case in point is the study of effects of radiation in the Guangdong Province in Southern China, where the study populations consist of homogeneous Han Chinese that have lived in the region for many centuries (Wang et al., 1990). Many studies report effects before and after statistical control for confounding variables, and we consistently used such robust effect sizes in this review. When testing for a difference in mean effect size between more and less rigorous studies, we found no significant difference. The distribution of effect sizes in relation to sample size is usually assumed to be funnel-shaped with larger variance around the true mean effect size at smaller sample sizes (the so-called funnel plot) (Light & Pillemer, 1984; Begg, 1994). Asymmetric plots may be due to publication bias, heterogeneity in effect sizes or other factors (e.g. Egger et al., 1997; Thornhill, Møller & Gangestad, 1999). We found evidence of asymmetric funnel plots (Fig. 2), but also showed that elimination of such asymmetry by adoption of the ‘trim and fill’ procedure (Duval & Tweedie, 2000a, b) did not eliminate an overall significant mean effect size. Radiation causes mutations even at the modest levels of natural radiation. There is extensive evidence for naturally high levels of radiation being associated with increased rates of genetic damage, including mutations. This effect was the predominant finding in most studies, showing a small, but highly significant effect size (Tables 1 and 2). In other words, effects of natural radiation are reported at a much higher frequency than would be expected by chance alone. This implies that natural radiation effects like those reported here are frequent and significant. The magnitude of the overall effect was ‘only’ small, accounting for less than 1% of the variance. However, in an evolutionary context even a small effect may have large consequences when considered across the large number of generations of evolutionary time scales. It is important to notice that we found a mean difference in effect size of almost an order of magnitude between animals and plants, suggesting that the sessile habits of plants subject them to chronic radiation. However, the difference in effect size for mutations between animals and plants was not statistically significant, although the difference in mean effects was large, probably due to low statistical power. More studies are required to assess this effect. In addition, reduced levels of migration in plants compared to mammals should result in greater levels of local adaptation in plants. Indeed, recent studies of DNA repair and gene expression in plants in Chernobyl seem to be consistent with such an interpretation (Boubriak et al., 2008; Danchenko et al., 2009; Klubicová et al., 2010). Despite this expectation we still found stronger negative effects of radiation on plants than on animals. Therefore, we can conclude that there is current selection for local adaptation in plants to cope with elevated levels of background radiation. Forster et al. (2002) showed that human mutation rates in naturally radioactive areas were seven times higher than in control regions, at a background radiation level ten times higher than the worldwide average. This is a typical level of radiation in so-called high-level radiation areas across the world, and this level of radiation is typically what is reported in the studies reviewed here (Table 1). In addition, Forster et al. (2002) showed that mutations were strongly aggregated at specific locations on the chromosomes that have had an evolutionary history of high mutation rates. This observation provides evidence that these radiation-associated point mutations are associated with a radiation-induced increase in the cell's normal mutation mechanisms or a decrease in repair mechanisms at these particular sites (Dubrova et al., 1997). Chronic exposure to radiation is associated with significant costs in terms of health. Here we have shown evidence of significant negative effects on immunology, mutation and disease frequency in a large number of studies (Tables 1 and 2). The observed high frequency of negative effects is very unlikely to reflect random chance. The findings reviewed here include reduced levels of antioxidants, weakened immune responses and elevated frequencies of disease including cancer. Antioxidant levels are typically suppressed in irradiated individuals as commonly reported from radiation accidents (e.g. Yablokov, Nesterenko & Nesterenko, 2009). Attar, Kondolousy & Khansari (2007) showed a similar effect on a number of different measures of immunity in humans in Iran exposed to elevated background radiation levels. This implies that elevated incidence of disease in contaminated areas may be caused by effects of radiation on the immune system rather than being a consequence of increased mutation rates directly causing disease. Three epidemiological studies link cancer to elevated levels of background radiation, even after controlling for potentially confounding variables (Ujeno, 1983; Tao et al., 2000; Körblein & Hoffmann, 2006). These findings about disease incidence and natural variation in background radiation have implications for studies of the effects of radiation accidents such as Chernobyl, Fukushima Daiichi and Three Mile Island. Given that natural levels of radiation typically are much lower than those reported for areas subjected to radiation accidents we can predict that the significant effects reported here for natural radiation will be even stronger in areas that are accidentally contaminated with high levels of radiation. There is extensive evidence of radiation-resistance in bacteria and fungi, but also in higher organisms such as Caenorhabditis elegans, bdelloid rotifers, tardigrades, insects and mice (Table 3). Some of these results, such as the tardigrades, can be explained by an absence of replicating cells after birth. While bacteria and fungi can survive exposure to even 15000 Gy, sustainable levels for Metazoa are much lower. However, it remains interesting that there is significant variation in radio-resistance even in mammals. Our review showed clear evidence of interspecific differences in resistance to radiation. Resistance to ionizing radiation in Dinococcus radiodurans and bdelloid rotifers appears to be derived from their desiccation resistance (Mattimore & Battista, 1996; Gladyshev & Meselson, 2008). A recent study showed that bacterial biofilms resistant to desiccation and ultraviolet radiation are pre-adapted to cope with ionizing radiation from Chernobyl (Ragon et al., 2011), apparently because the same underlying mechanisms are responsible for resistance in both cases. In Deinococcus radiodurans there seems to have been an accumulation of genes involved in resistance to radiation that allowed it to cope successfully with different kinds of environmental stresses (or vice versa) compared to a closely related radio-susceptible bacterium (Omelchenko et al., 2005). Even large amounts of DNA damage in D. radiodurans can be repaired without leaving any obvious trace of mutations through homologous recombination, use of single-strand DNA for recombination, regulated DNA replication, and export of damaged nucleotides from the cell for mutation avoidance (Battista et al., 1999; Cox & Battista, 2005). The underlying mechanisms responsible for radiation resistance were originally thought to be efficient DNA repair; the current focus has switched towards mechanisms of repair of DNA damage caused by reactive oxygen species. Both desiccation and irradiation result in oxidative stress (França, Panek & Eleutherio, 2007). High levels of reactive oxidative species cause damage to DNA and proteins that require correction through repair (Minton, 1994, 1996; DiRuggiero et al., 1997; Battista et al., 1999). Daly et al. (2004) showed that Deinococcus radiodurans and other radio-resistant bacteria differ from non-radio-resistant species in their level of accumulation of intracellular manganese and low levels of iron; melanin may play a similar role in fungi (Dadachova et al., 2007 and trehalose in cyanobacteria (Shirkey et al., 2003). In experimental settings manganese seems to facilitate recovery from radiation injury. When manganese combines with ligands, the resulting products can act as powerful scavengers of free radicals arising as a consequence of ionizing radiation (Daly, 2009). Because such bacterial cells rely on homologous recombination for rejoining double-strand breakage of DNA, the presence of multiple copies of the genome in combination with antioxidant protection would allow cells to survive even with multiple double-strand breakages. It is interesting that it appears that protection mechanisms against reactive oxygen species rather than DNA repair as such is the basis for radio-resistance in bacteria such as Deinococcus radiodurans. Differences among bacterial taxa in their level of radio-resistance appear to be related to the importance of manganese in such antioxidant defence (Daly, 2009). Thus, it is probably not a coincidence that interspecific differences in the ability to survive the impact of radiation at Chernobyl are associated with ecological factors closely linked to antioxidant status (Møller & Mousseau, 2007). The antioxidant status of individuals (Bonisoli-Alquati et al., 2010), and the amount of pheomelanic plumage in birds (Galván, Mousseau & Møller, 2011) predicts the ability to sustain radiation, apparently due to the action of the powerful antioxidant glutathione. The effects of low-dose radiation reported here emphasise a significant role of oxidative stress at even very low levels of natural background radiation. We hypothesise that limited availability of antioxidants and the associated physiological problems in terms of reduced ability to repair damage to DNA and other molecules may account for such effects. Hormesis is defined as a beneficial effect of normal background radiation on life-history traits such as fecundity and longevity compared to levels achieved in the complete absence of radiation (reviews in Kondo, 1993; Luckey, 1991). If hormetic effects of radiation on fitness exist, we should expect that the optimal level of radiation should increase with background radiation level. If hormesis has evolved as a consequence of local adaptation to specific levels of radiation, we might even find that all populations should perform best at some local level of radiation; exceeding their performance in the absence of radiation. The latter scenario would suggest that fitness should be independent of level of natural background radiation. In either case, we should not expect to find increased mutation rates, impaired immune function, increased incidence of disease and increased mortality in areas with higher levels of normal background radiation. Our findings are clearly inconsistent with a general role for hormesis in adaptation to elevated levels of natural background radiation. We note that some effect sizes reported herein were negative, thereby deviating from this expectation. However, these effects were of a level that would be expected by chance, inconsistent with expectations for a hormesis hypothesis. In conclusion, reported rates of mutation caused by natural variation in radiation levels are almost exclusively restricted to studies of humans with only a few studies on other species available. Information on physiology, immunology and disease associated with radiation again are restricted almost exclusively to studies of humans. Note, however, that there is no evidence of radio-tolerance or radio-resistance in humans, and there are still no studies of disease and mutation rates in species in which radio-tolerance or radio-resistance has been documented. The present review provides evidence for interspecific variation in radio-tolerance and radio-resistance in a large number of taxa, suggesting that there has been selection for and evolution of such characteristics. The scarcity of studies on mutations and disease in organisms other than humans clearly should be addressed.
V. CONCLUSIONS
We reviewed the literature on responses to natural variation in background radiation. There was evidence of a significant, but small effect of natural variation in background radiation on mutation rates, DNA damage and DNA repair.
There were significant effects of natural variation in background radiation on immunology and disease including cancer.
The findings reported here are inconsistent with a general role of hormesis from low levels of natural background radiation.
There was strong evidence for the existence of radio-resistance in different taxa, with differences among taxa recorded in a variety of studies.
These findings concerning the relationship between natural variation in background radiation and various biological response variables have important implications for assessment of the biological effects of radiation accidents.
Future studies should address the underlying mechanisms accounting for interspecific differences in susceptibility to radiation.
VI. ACKNOWLEDGEMENTS
P. Lopez helped with references S. Randic, M. D. Jennions and two anonymous referees provided helpful suggestions for the meta-analysis.
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http://noimmediatedanger.net/contents/seminar1976/250
アーチャー博士の主張を証明したのが、37年後の2013年に発表された論文「バックグラウンド放射線の人間、動物、その他の有機体への影響」（Møller, A.P. & Mousseau, T.A. (2013) The effects of natural variation in background radioactivity on humans, animals and other organisms, Biological Reviews, 88: 226-254）である。サウスカロライナ大学のムソー教授とパリ11大学のメラー教授がバックグラウンド放射線の影響に関する5,000以上の論文を検証し、量的比較をするために46論文を選んで精査した。いずれの論文も被ばくした人々と、していない人々の対照群を比較した。植物や動物への影響も含まれるが、大半は人間への影響で、DNA損傷、ダウン症、出生児の性比などを検証した。どの項目でも統計処理を行った結果、免疫、生理機能、突然変異、疾病発症率などの点でマイナス影響があることが判明した。すべての項目でマイナス影響の発生は偶然の確率を超えていた。
http://www.newswise.com/articles/even-low-level-radioactivity-is-damaging
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