Content uploaded by Jaroslav Flegr
All content in this area was uploaded by Jaroslav Flegr
Content may be subject to copyright.
Toxoplasmosis-Associated Difference in Intelligence and
Personality in Men Depends on Their Rhesus Blood
Group but Not ABO Blood Group
*, Marek Preiss
1Department of Biology, Faculty of Science, Charles University in Prague, Prague, Czech Republic, 2Department of Biochemistry & Brain Pathophysiology, Prague
Psychiatric Center, Prague, Czech Republic, 3Central Medical Psychology Department, Military University Hospital Prague, Prague, Czech Republic
The parasite Toxoplasma gondii influences the behaviour of infected animals and probably also personality of
infected humans. Subjects with a Rhesus-positive blood group are protected against certain behavioural effects associated
with Toxoplasma infection, including the deterioration of reaction times and personality factor shift.
Here, we searched for differences in the toxoplasmosis-associated effects between RhD-
positive and RhD-negative subjects by testing 502 soldiers with two personality tests and two intelligence tests. The
infected subjects expressed lower levels of all potentially pathognomic factors measured with the N-70 questionnaire and in
neurasthenia measured with NEO-PI-R. The RhD-positive, Toxoplasma-infected subjects expressed lower while RhD-
negative, Toxoplasma-infected subjects expressed higher intelligence than their Toxoplasma-free peers. The observed
Toxoplasma-associated differences were always larger in RhD-negative than in RhD-positive subjects.
RhD phenotype plays an important role in the strength and direction of association between latent
toxoplasmosis and not only psychomotor performance, but also personality and intelligence.
Citation: Flegr J, Preiss M, Klose J (2013) Toxoplasmosis-Associated Difference in Intelligence and Personality in Men Depends on Their Rhesus Blood Group but
Not ABO Blood Group. PLoS ONE 8(4): e61272. doi:10.1371/journal.pone.0061272
Editor: Martin E. Rottenberg, Karolinska Institutet, Sweden
Received October 18, 2012; Accepted March 7, 2013; Published April 10, 2013
Copyright: ß2013 Flegr et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The authors’ work was supported by the Grand Agency of the Czech Republic (Grant No. P303/11/1398) and Charles University of Prague (GAUK 18810,
grant UNCE 204004). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: firstname.lastname@example.org
The trophically transmitted parasites often modify the behavior
of their intermediate host to increase its susceptibility to predation
[1,2]. By this they increase the probability of their transmission
from intermediate to definitive host. A popular model for studying
such manipulation activity of parasites in a mammal host is
Toxoplasma gondii, for review see [3,4]. In its life cycle, Toxoplasma
needs to be transmitted from the intermediate host, e.g. an
infected rodent, to the definitive host, i.e. any representative of the
Felinidae family, including the domestic cat. It is known that
infected rodents are hyperactive in the open field [5,6], exhibit
increased voluntary wheel running [7,8] and longer exploration
times in the hole board test , are deficient in motor performance
and coordination [8,10], and have longer reaction times ,
impaired working memory , and impaired ability to recognise
novel stimuli [8,13]. The most specific and also the most
spectacular toxoplasmosis-associated change reported in rodents
is the so-called Fatal attraction phenomenon, i.e. the conversion of
the rats’ and mice’s innate fear of cat odour into attraction to cat
odour (but not to the odour of other predators). This phenomenon
was observed in several laboratories [12,14–16] and was
dependent on activation of the brain regions that respond to
sexual stimuli in normal mice by the odour of a particular
predator, the cat in infected rodents . Current results suggest
that changed concentrations of testosterone  and dopamine
probably play an important role in the differences in the
personality and behavior between Toxoplasma-infected and Toxo-
plasma-free subjects. It was found that the Toxoplasma gondii genome
contains two genes for enzymes (tyrosine hydroxylases) implicated
in the synthesis of dopamine  and increased concentration of
this neurotransmitter was observed in the infected rodent brain
Any warm-blooded animal, including humans, can be infected
with Toxoplasma and the prevalence of this infection in different
countries varies between 5 and 80% depending on climate,
hygienic standards and kitchen habits . After a short phase of
acute toxoplasmosis, the infection proceeds to its latent stage when
tissue cysts with bradyzoites are formed and these survive for the
rest of the host’s life mainly in neural and muscular tissues. In
immunocompetent subjects, the latent phase of infection was
considered asymptomatic and harmless from the clinical point of
view, however, results of many recent studies suggested that this
form of the infection could have many serious clinical implications
[21–24]. However, practically all studies performed in the past 20
years have demonstrated behavioural changes including the Fatal
attraction phenomenon , observed earlier in laboratory
animals, also in humans, for recent reviews, see [3,26].
PLOS ONE | www.plosone.org 1 April 2013 | Volume 8 | Issue 4 | e61272
It is well known that the gene pool of the local human
population is strongly influenced by the selection pressure of
parasites. Recent studies have shown that the association between
latent toxoplasmosis and human reaction times, personality and
physiology depend on RhD phenotype of the infected subject [27–
31]. It has even been suggested that the spreading of the deletion
responsible for RhD negativity in the Caucasian population can be
caused by increased psychomotor performance of RhD-negative,
Toxoplasma-free subjects in Europe where the cats and therefore
also toxoplasmosis were rare before the advent of the domestic cat
. The association between toxoplasmosis and the personality of
RhD-negative and RhD-positive subjects was studied using
Cattell’s 16PF and Cloninger’s TCI questionnaires . In the
present study, we searched for the difference between RhD-
positive and RhD-negative subjects using the NEO-PI-R ques-
tionnaire that is based on the modern Big Five model of
personality. Moreover, we searched for similar RhD phenotype-
and toxoplasmosis-associated differences in verbal and nonverbal
intelligence and also in pathognomic traits measured with the N-
Materials and Methods
All participants provided their written informed consent. The
recruitment of study subjects and data handling were performed in
compliance with the Czech legislation in force and were approved
by the Institutional Review Board of the Faculty of Science,
Sample and Participant Selection
All psychological testing was performed at the Military
University Hospital Prague. The study population consisted of
502 male soldiers of Czech nationality (age: 18–52, mean 27.25,
S.D. 6.71, median 25.94) who attended the Military University
Hospital Prague to take entrance psychological examinations for
military missions in 2005 and consented to participate in the
research project. The subjects were examined with standardized
panel of psychological and performance tests, essayed for RhD
and ABO phenotype during the health examination and also
provided 5 ml of blood for a serology test. In the informed consent
form, the general aim of the project (a study of the influence of
environmental factors on human psychology and performance)
and the need for obtaining their consent to using the results of
their psychological and clinical examinations were explained. The
consent rate was about 65%.
The N-70 is a questionnaire constructed for the assessment of
seven areas of clusters - anxiety, depression, phobia, hysteria,
hypochondria, psychosomatic symptoms and psychastenia .
The purpose of this method is to detect individuals who may be
too sensitive for military operations . Subjects are asked to
answer 70 questions using a 3-point agreement scale. Scores in
each cluster range from 0–30. The total N-70 score is the number
of non-negative answers for all 70 questions.
The electronic version of NEO-PI-R (Costa & Mccrae, 1992)
translated to Czech and validated by Hr
ˇkova´ (2001)  was
Wiener Matrizen-Test of intelligence
The Wiener Matrizen-Test (WMT) , a nonverbal intelli-
gence test, is an adapted version of the Raven progressive matrices
which conforms to the Rasch model . The WMT assesses
general intelligence by measuring reasoning ability. The test
requires the completion of 24 matrices with increasing task
difficulty and was administered without an explicit time limit. The
intention and conceptualization of the WMT are largely based on
Raven’s Matrices [37–39]. The correlation between the WMT
and Standard Progressive Matrices is about r = 0.92 .
Construction and item selection, however, follow the standards
of Rasch scaling. For these reasons, and due to the fact that the
WMT showed comparable validity characteristics but had a
considerably higher administration economy, we prefer the WMT
to the Raven matrices in clinical practice. The split-half reliability
of the WMT is 0.83 . The 1993 Czech adopted version ,
distributed by Psychodiagnostika (Brno), was used in the present
study. Both the raw score and the IQ adjusted for age of the
participant were compared in statistical tests.
OTIS test of intelligence
The OTIS test is a test of verbal intelligence which was derived
from the original test . Seven types of items were taken from
the original test:
– term or object definition by choosing the most suitable
– term or object definition by choosing the most suitable
– the choice of an object based on common attributes
– the choice of the opposite
– the identifying of ‘‘foreign’’ (unrelated) terms
– logical or ethical solution of the situations
– the interpretation of the adage
The test contains 32 items (0–32). The maximum score is
therefore 32 points. Both the raw score and the IQ (adjusted for
the educational level, see ) were compared in statistical tests.
Immunological tests for toxoplasmosis
All serological tests were carried out in the National Reference
Diagnostic Laboratory for Toxoplasmosis, National Institute of
Public Health, Prague. Specific IgG and IgM antibody titres were
determined by ELISA (IgG: SEVAC, Prague, IgM: TestLine,
Brno), optimized for early detection of acute toxoplasmosis
(Pokorny´ et al., 1989) and by complement fixation tests (CFT)
(SEVAC, Prague) which are more sensitive and therefore more
suitable for the detection of old T. gondii infection (Warren &
Sabin, 1942). The titre of anti-Toxoplasma antibodies in sera was
measured in dilutions between 1:8 and 1:1024. The subjects with
negative results of IgM ELISA (positivity index,0.9) and both
CFT titres higher than 1:8 and IgG ELISA .250 optical units, i.e.
approximately 10 IU/ml, were considered latent toxoplasmosis
positive. The individuals with ambiguous diagnosis, e.g. different
result of CFT and ELISA, were excluded from the study.
The Statistica 8.0 was used for descriptive statistics, General
Linear Model tests and computing taus by standard Kendall
correlation tests. Partial Kendall correlation test suggested by
Siegel and Castellan  based on taus computed with standard
Kendall correlations was used for nonparametric analyses ; the
Effect of Toxoplasmosis and RhD on Intelligence
PLOS ONE | www.plosone.org 2 April 2013 | Volume 8 | Issue 4 | e61272
Excel sheet for this analysis is available at http://web.natur.cuni.
We obtained scores for the N-70, NEO-PI-R, WMT and Otis
tests from 502 subjects tested for RhD and latent toxoplasmosis.
One hundred and fifty-four (154, i.e. 31.4%) of 491 subjects with
unambiguous results of the test for toxoplasmosis were Toxoplasma
infected and 87 (17.3%) of 502 subjects were RhD negative. No
association between toxoplasmosis and RhD phenotype was
= 0.14, p = 0.707). Descriptive statistics for the
population under study are shown in Tables 1 and 2. For the
analysis of correlation of toxoplasmosis and RhD phenotype with
the personality profile of soldiers (ordinal variables), we used a
robust nonparametric test. To control for the effect of age, partial
Kendal correlation tests were performed with age as a covariate
and to control for the effect of RhD phenotype, RhD-positive and
RhD-negative subjects were tested separately. Table 1 shows that
Toxoplasma-infected subjects scored lower in the total N-70 score
and also in anxiety, depression, phobia, hysteria, and vegetative
lability and in the BigFive trait neuroticism. The differences were
much stronger in RhD-negative than RhD-positive subjects. No
relation between latent toxoplasmosis and nonverbal (WMT) or
verbal (Otis) intelligence was observed in RhD nonsorted
population. However, separate analyses performed for RhD-
positive and RhD-negative populations showed negative associa-
tion between intelligence and toxoplasmosis in RhD-positive
subjects and positive association between intelligence and toxo-
plasmosis in RhD-negative subjects, see Fig. 1. Again, the
correlation of intelligence with toxoplasmosis (estimated with
partial tau) was much stronger for RhD-negative subjects.
The same analyses (partial Kendall correlations with age as a
covariate) was performed for the independent binary variable
RhD phenotype, in the whole population and separately in the
Toxoplasma-infected and Toxoplasma-free subjects, see Table 2.
Significant association of RhD phenotype with the total N-70
score, hypochondria, vegetative lability, psychasteny, and the
NEO-PI-R neuroticism were observed only in Toxoplasma-infected
subjects. However, the association of RhD phenotype with
nonverbal and verbal intelligence was detected also in Toxoplas-
ma-free subjects, suggesting that not only the protective effect of
RhD positivity against consequences of toxoplasmosis but also the
main effect of RhD phenotype (or its protective effect against some
unknown third factor) probably played a role in the observed
associations between RhD phenotype and various personality
The partial Kendall correlation test can control for one
confounding variable only. To study the effect of interactions
and several potential confounding variables we performed General
Linear Model analyses with independent variables age, toxoplas-
mosis, RhD phenotype, ABO phenotype and RhD phenotype-
toxoplasmosis and ABO phenotype-toxoplasmosis interactions.
The analyses showed significant effect of RhD phenotype-
toxoplasmosis interaction on psychasteny and IQ and no
significant effects of ABO phenotype or ABO phenotype
interaction (Tab. 3).
Soldiers with and without latent Toxoplasma infection differ in
several personality traits. Generally, the infected subjects expressed
lower levels of potentially pathognomic factors measured with the
N-70 questionnaire and of neuroticism tested with the NEO-PI-R
(Big Five model). The RhD-positive, Toxoplasma-infected subjects
express lower while RhD-negative, Toxoplasma-infected subjects
express higher verbal and nonverbal intelligence than their
Toxoplasma-free peers. The observed Toxoplasma-associated differ-
ences in personality traits, including intelligence were always larger
in RhD-negative than in RhD-positive subjects.
The GLM analysis showed that the effect of RhD-toxoplasmosis
interaction on intelligence is highly significant. This analysis also
showed a significant effect RhD-toxoplasmosis interaction on
psychasteny. It must be reminded, however, that this effect is non-
significant after the correction for multiple statistical tests. The
GLM also showed absence of main effects of RhD phenotype and
toxoplasmosis (after correction for multiple tests), which contrasted
with results of partial Kendall correlation tests. The lower power of
parametric tests for ordinal data with asymmetric distribution as
well as the presence of several other independent variables and
their interactions in more complex GLM models could be
responsible for this difference between results of parametric and
nonparametric tests. GLM analysis models also showed absence of
effect of ABO phenotype and its interaction on personality and
intelligence. Absence of any effect of ABO phenotype contrasted
with existence of numerous effects of RhD phenotype – see the
Table 3, confirming the special role of RhD proteins in human
Association between Toxoplasma infection and human personal-
ity factors were studied thoroughly in the past 20 years. About 10
published studies have demonstrated associations of toxoplasmosis
with human personality traits mostly using Cattell’s 16PF and
Cloninger’s TCI questionnaires; for review, see [26,43,44]. Only
one study, showing positive association of toxoplasmosis with
extroversion and its negative association with conscientiousness,
used the NEO-PI-R questionnaire . A correlation study has
also shown that the difference in the prevalence of latent
toxoplasmosis between the general populations of particular
countries can explain a significant portion of the variance in
aggregate neuroticism among populations .
Surprisingly, the results obtained in the present study performed
on military personnel differed from those observed earlier on
university students. For example, Toxoplasma-infected and Toxo-
plasma-free soldiers expressed no differences in extroversion or
conscientiousness and Toxoplasma-infected and Toxoplasma-free
students expressed no difference in neuroticism. Moreover, the
results of the correlation study comparing the prevalence of latent
toxoplasmosis with aggregate neuroticism in the general popula-
tions of particular countries suggest that Toxoplasma-infected
subjects have higher rather than lower neuroticism . It was
also suspicious that infected soldiers expressed lower and not
higher levels of psychopathognomic traits measured with the N-70
questionnaire. Our present hypothesis is that Toxoplasma-infected
soldiers express stronger tendency to mask any negative property
when responding to questions in questionnaires. Several studies
have shown a lower superego strength (Cattell’s factor G) and
higher suspiciousness (Cattell’s factor L) in Toxoplasma-infected
men. The testing of soldiers in the current study was a part of their
entrance examination for a voluntary (and well-paid) participation
in an international military mission and (in contrast with university
students or blood donors tested in the previous anonymous studies)
the subjects were objectively motivated to mask their negative (e.g.
the pathognomic) and to accentuate their positive properties. It is
urgently needed to confirm our results in an anonymous research
study where the motivation for intentional distortion of data is
Existence of the interaction between toxoplasmosis, RhD
phenotype and human behaviour has been confirmed in four
studies. Two of them have shown resistance of RhD-positive
Effect of Toxoplasmosis and RhD on Intelligence
PLOS ONE | www.plosone.org 3 April 2013 | Volume 8 | Issue 4 | e61272
subjects, especially the RhD-positive heterozygotes, to impairment
of reaction times after Toxoplasma infection [27,28] and one
prospective study performed on 3900 military drivers has found an
increased risk of traffic accidents in Toxoplasma-infected, RhD-
negative subjects . The fourth study has reported opposite
relation of toxoplasmosis with Cattell’s ego strength, praxernia,
and ergic tension and Cloninger’s cooperativeness in RhD-positive
and RhD-negative blood donors . The latter study also
indicates that RhD phenotype might play an important role not
only in the toxoplasmosis-associated differences but also in the age-
associated differences in specific personality traits.. Another recent
study shows that RhD phenotype could also play a role in
correlations of age and smoking with psychomotor performance,
intelligence and health of draftees . The results of the current
study are in an agreement with the already published data. The
correlations of toxoplasmosis with personality of soldiers (reflected
by the absolute values of Kendall tau shown in Tables 1 and 2)
were always much stronger in RhD-negative than RhD-positive
subjects, see Table 1. Moreover, the higher verbal and nonverbal
intelligence of RhD-positive Toxoplasma-free subjects than Rh-
negative Toxoplasma-free soldiers suggests that RhD positivity could
protect not only against detrimental effects of latent toxoplasmosis
but also against other (still unknown) factors. At the present time,
we have no explanation for the opposite relation between RhD
phenotype and intelligence in Toxoplasma-infected and Toxoplasma-
free subjects. We cannot exclude a possibility that some unknown
gene that is in linkage disequilibrium with RHD gene, rather than
RHD gene itself, is responsible for the observed phenomena. We
cannot even exclude a possibility that the observed phenomena are
caused by some unknown confounding variables that co-vary with
RhD phenotype and also other observed variables, namely risk of
Toxoplasma infection and human personality and intelligence.
However, the present data could explain the controversial results
concerning the existence (and direction) of the correlation between
latent toxoplasmosis on intelligence [48,49].
The mechanism responsible for physiological and behavioural
effects of RhD phenotype is unknown. The RhD molecule is part
of a molecular complex (RhAG) on the membrane of red cells
[50,51]. Structural data suggest that the complex is a membrane
or possibly CO
pump with unknown function [52–54]. In
RhD-negative subjects, the gene RHD is absent in chromosomes
of both maternal and paternal origin due to a large deletion and
therefore also the RhD molecule is missing and is probably
substituted with another related molecule in the complex .
RhD-containing and RhD-free complexes may differ in the
specificity, activity and most probable also response to regulation
signals. The membrane pump could directly or indirectly influence
the partial tension of oxygen and water balance in various tissues,
including the brain tissue [56–58].
Limitations of the present study
The major limitation of the present study was that the study
subjects were objectively motivated to accent positive and to hide
negative traits of their personality as their results were to be used as
a part of the entrance examination for the participation in a
military (peacekeeping) mission. The resulting bias probably
Figure 1. Differences in nonverbal (WMT) and verbal (OTIS) intelligence between
positive and RhD-negative subjects. The graph shows arithmetic means, standard errors (whiskers), medians, and 25% and 75% quartiles. The
presented values differ from raw data listed in Tables 1 and 2 because the intelligence has been controlled for the age of men, that is, the intelligence
has been computed for covariate (age) as its mean.
Effect of Toxoplasmosis and RhD on Intelligence
PLOS ONE | www.plosone.org 4 April 2013 | Volume 8 | Issue 4 | e61272
Table 1. Descriptive statistics and results of testing differences in personality traits and intelligence between Toxoplasma-infected and Toxoplasma-free RhD-negative and RhD-
positive male soldiers.
N mean N mean N mean
Tau p Toxo
Tau p Toxo
Age 337 154 26.70 27.83 280 125 26.77 28.26 57 28 26.35 26.26
Total N-70 335 152 18.97 16.57 20.09 0.002 278 123 18.97 17.21 20.07 0.032 57 28 18.96 13.50 20.23 0.002
Anxiety 335 152 4.31 3.68 20.10 0.001 278 123 4.28 3.74 20.09 0.009 57 28 4.47 3.39 20.19 0.009
Depression 335 152 2.18 1.80 20.07 0.018 278 123 2.16 1.86 20.05 0.102 57 28 2.26 1.50 20.18 0.016
Phobia 335 152 2.87 2.50 20.07 0.024 278 123 2.86 2.57 20.06 0.096 57 28 2.95 2.14 20.13 0.069
Hysteria 335 152 2.87 2.34 20.11 0.000 278 123 2.91 2.42 20.10 0.002 57 28 2.68 2.00 20.12 0.095
Hypochondria 335 152 2.51 2.24 20.06 0.062 278 123 2.54 2.36 20.03 0.295 57 28 2.40 1.71 20.16 0.031
Vegetative lability 335 152 3.15 2.71 20.08 0.013 278 123 3.18 2.82 20.06 0.089 57 28 3.00 2.18 20.16 0.033
Psychasteny 335 152 2.13 1.91 20.05 0.074 278 123 2.14 2.10 20.02 0.566 57 28 2.11 1.00 20.24 0.001
Neuroticism 314 143 69.06 65.15 20.07 0.025 259 117 68.86 66.49 20.04 0.253 55 25 69.98 59.32 20.22 0.005
Extroversion 314 143 116.84 116.70 0.00 0.887 259 117 116.79 116.83 0.01 0.678 55 25 117.11 116.80 20.00 0.957
Openness 314 143 101.81 102.40 20.00 0.943 259 117 102.89 101.41 20.03 0.393 55 25 100.47 106.88 0.130 0.089
Agreeableness 318 144 122.42 123.45 0.03 0.265 259 117 121.80 123.28 0.05 0.174 55 25 125.35 123.68 20.03 0.689
Conscientiousness 316 144 128.81 130.07 0.03 0.265 259 117 128.73 130.12 0.04 0.272 55 25 129.18 130.00 0.03 0.745
Row WMT 314 143 23.19 23.04 20.01 0.695 278 123 23.38 22.72 20.07 0.044 57 28 22.28 24.46 0.24 0.001
IQ WMT 312 142 101.49 101.09 20.01 0.712 278 123 101.95 100.37 20.06 0.083 57 28 99.25 104.54 0.21 0.004
Row Otis 311 141 14.53 14.12 20.03 0.368 273 117 14.75 13.86 20.07 0.027 53 27 13.38 15.41 0.21 0.007
IQ Otis 309 140 101.97 100.78 20.02 0.595 273 117 102.62 100.14 20.06 0.099 53 27 98.60 104.30 0.18 0.017
Tau shows effect size and sign, p shows statistical significance measured with partial Kendall tests. Significant results (p,0.05, two-sided test) are printed in bold. Toxoplasma-free and Toxoplasma-infected subjects are coded with 0
and 1, respectively. Therefore, negative Tau means lower test score in Toxoplasma infected subjects. Formal correction for multiple (51) tests was not performed. Theoretically, 2–3 of 51 tests presented in this table should provide
false positive results.
Effect of Toxoplasmosis and RhD on Intelligence
PLOS ONE | www.plosone.org 5 April 2013 | Volume 8 | Issue 4 | e61272
Table 2. Descriptive statistics and results of testing differences in personality traits and intelligence between RhD-negative and RhD-positive Toxoplasma-infected and
Toxoplasma-free male soldiers.
N mean N mean N mean
Tau p RhD
Tau p RhD
Age 87 415 26.36 27.26 57 280 26.35 26.77 28 125 26.26 28.26
Total N-70 87 411 16.97 18.36 0.05 0.108 57 278 18.96 18.97 0.00 0.980 28 123 13.50 17.21 0.12 0.027
Anxiety 87 411 4.08 4.11 0.00 0.890 57 278 4.47 4.28 20.03 0.440 28 123 3.39 3.74 0.06 0.303
Depression 87 411 1.97 2.04 0.00 0.869 57 278 2.26 2.16 20.04 0.291 28 123 1.50 1.86 0.05 0.401
Phobia 87 411 2.66 2.75 0.03 0.377 57 278 2.95 2.86 0.00 0.979 28 123 2.14 2.57 0.07 0.189
Hysteria 87 411 2.44 2.74 0.06 0.057 57 278 2.68 2.91 0.05 0.194 28 123 2.00 2.42 0.07 0.204
Hypochondria 87 411 2.18 2.46 0.05 0.108 57 278 2.40 2.54 0.02 0.565 28 123 1.71 2.36 0.12 0.029
Vegetative lability 87 411 2.68 3.08 0.06 0.050 57 278 3.00 3.18 0.02 0.666 28 123 2.18 2.82 0.13 0.021
Psychasteny 87 411 1.70 2.13 0.09 0.003 57 278 2.11 2.14 0.02 0.655 28 123 1.00 2.10 0.21
Neuroticism 82 386 57.90 59.16 0.03 0.314 55 259 60.75 59.72 20.02 0.639 25 117 51.92 58.01 0.13 0.018
Extroversion 82 386 95.21 95.52 0.01 0.827 55 259 95.20 95.52 20.01 0.843 25 117 94.84 95.44 0.05 0.344
Openness 82 386 82.70 82.22 20.01 0.814 55 259 81.24 82.51 0.02 0.600 25 117 86.28 81.80 20.06 0.270
Agreeableness 82 386 104.63 102.00 20.06 0.045 55 259 105.45 101.64 20.08 0.027 25 117 103.08 103.03 20.01 0.838
Conscientiousness 82 386 109.18 108.84 20.01 0.763 55 259 108.75 108.31 20.01 0.795 25 117 109.72 109.65 20.01 0.905
Row WMT 87 411 22.94 23.20 0.03 0.362 57 278 22.28 23.38 0.09 0.010 28 123 24.46 22.72 20.15 0.005
IQ WMT 87 411 100.79 101.55 0.03 0.347 57 278 99.25 101.95 0.08 0.027 28 123 104.54 100.37 20.13 0.016
Row Otis 82 399 13.93 14.45 0.05 0.094 53 273 13.38 14.75 0.12 0.002 27 117 15.41 13.86 20.12 0.030
IQ Otis 82 399 99.99 101.76 0.05 0.137 53 273 98.60 102.62 0.10 0.007 27 117 104.30 100.14 20.11 0.047
Tau shows effect size and sign, p shows statistical significance measured with partial Kendall. RhD-negative and RhD-positive subjects are coded with 0 and 1, respectively. Therefore, negative Tau means lower test score in RhD-
positive subjects. Formal correction for multiple (51) tests was not performed. Theoretically, 2–3 of 51 tests presented in this table should provide false positive results.
Effect of Toxoplasmosis and RhD on Intelligence
PLOS ONE | www.plosone.org 6 April 2013 | Volume 8 | Issue 4 | e61272
cannot influence the result of the intelligence tests; however, it
makes it difficult to interpret psychological meanings of the
observed relations of toxoplasmosis and RhD phenotype with the
personality profile. Many subjects were probably aware about
their RhD phenotype; however, nobody was aware either about
the hypothesis under study or about their toxoplasmosis status and
therefore no systematic bias in the obtained data could be
The second important limitation of the study was the fact that
only RhD phenotype and not RhD genotype of the subjects was
tested. Results of a previous study suggested that in contrast to
RhD-positive heterozygotes, the RhD-positive homozygotes were
only transiently protected against some negative effects of
toxoplasmosis (namely against prolongation of reaction times)
. It is very easy (and cheap) to determine RhD phenotype
using the standard agglutination technique. However, a much
more sophisticated (and expensive) technique must be used for the
determination of RhD genotype. It is also highly probable that a
much lower fraction of the soldiers would consent to be involved in
a study that would include also DNA analysis. Due to these
technical limitations, we compared RhD-negative homozygotes
with a mixed population of RhD-positive homozygotes and
heterozygotes in all our statistical tests. It is therefore possible
that we underestimated the strength of real effects. Only male
soldiers were included into the present study. It is critically needed
to perform similar study on female subjects in the future because
toxoplasmosis usually induces opposite direction shifts in male and
female subjects [26,59].
The third limitation of the present study concerns the fact that
the existence of a significant statistical effect does not imply the
existence of the real effect of a particular independent variable, e.g.
the toxoplasmosis, on a dependent variable, e.g. the intelligence.
The observed statistical effect could be caused by an effect of the
intelligence on the risk of Toxoplasma infection or even by an effect
of some unknown third factor on both intelligence and risk of
It is highly probable that similar or even stronger associations
could exist between infection with other pathogens, e.g. chlamyd-
ia, yeasts and herpetic viruses, and behavioural and psychological
traits. For example, not only the infection with Toxoplasma but also
with human cytomegalovirus is accompanied by decreased
Cloninger’s personality factor Novelty seeking . Our subjects
were not tested for presence of other infectious agents except
Toxoplasma and therefore we could not include these potential
confounding factors into our models. It must be stressed, however,
that the absence of these factors in the models could cause false
negative but not false positive results of statistical tests.
The effect of blood groups on personality and intelligence was
the subject of many earlier studies. Despite the widespread believe
in the existence of such effects in some cultures, e.g. in Japan,
rigorous tests usually provided only negative results. It must be
reminded, however, that the ABO blood group system rather than
the Rhesus factor system was nearly always examined in these
studies, see [61–64]. Our results imply that in future behavioural
studies the attention should be focused not only on the ABO
system but also on RhD phenotype and that important
confounding variables, especially Toxoplasma infection and smoking
 should be controlled.
Conceived and designed the experiments: JF. Performed the experiments:
JK MP. Analyzed the data: JF. Contributed reagents/materials/analysis
tools: JF JK. Wrote the paper: JF.
Table 3. Results of testing the effects of age, toxoplasmosis, RhD phenotype, ABO phenotype, and RhD-toxoplasmosis and ABO-
toxoplasmosis interaction on personality traits and intelligence.
age ABO RhD Toxo ABO-Toxo RhD-Toxo
Total N-70 0.819 0.677 0.076 0.034 0.807 0.149
Anxiety 0.999 0.637 0.541 0.032 0.578 0.395
Depression 0.467 0.476 0.513 0.119 0.798 0.392
Phobia 0.410 0.674 0.353 0.121 0.907 0.289
Hysteria 0.674 0.992 0.237 0.089 0.677 0.560
Hypochondria 0.522 0.168 0.016 0.174 0.378 0.280
Vegetative lability 0.647 0.765 0.188 0.168 0.685 0.470
Psychasteny 0.287 0.552 0.936 0.148 0.163 0.019
Neuroticism 0.443 0.846 0.200 0.052 0.791 0.164
Extroversion 0.825 0.793 0.964 0.671 0.336 0.999
Openness 0.618 0.483 0.471 0.549 0.562 0.144
Agreeableness 0.447 0.844 0.357 0.493 0.848 0.264
Conscientiousness 0.863 0.351 0.903 0.746 0.562 0.760
Row WMT 0.308 0.243 0.651 0.203 0.794 0.010
IQ WMT 0.422 0.237 0.806 0.317 0.943 0.037
Row Otis 0.167 0.611 0.783 0.081 0.132 0.003
IQ Otis 0.287 0.551 0.936 0.148 0.163 0.019
The table shows p-values of particular GLM tests. Significant results (p,0.05, two-sided test) are printed in bold. Formal correction for multiple tests was not performed.
Theoretically, about one false positive result should be present in each column.
Effect of Toxoplasmosis and RhD on Intelligence
PLOS ONE | www.plosone.org 7 April 2013 | Volume 8 | Issue 4 | e61272
1. Moore J, Adamo S, Thomas F (2005) Manipulation: expansion of the paradigm.
Behav Processes 68: 283–287.
2. Barnard CJ, Behnke JM (1990) Parasitism and Host Behaviour. New York:
Taylor and Francis.
3. Webster JP, McConkey GA (2010) Toxoplasma gondii -altered host behaviour:
clues as to mechanism of action. Folia Parasitol 57: 95–104.
4. Webster JP (2007) The effect of Toxoplasma gondii on animal behavior: Playing cat
and mouse. Schizophr Bull 33: 752–756.
5. Xiao J, Kannan G, Jones-Brando L, Brannock C, Krasnova IN, et al. (2012)
Sex-specific changes in gene expression and behavior induced by chronic
Toxoplasma infection in mice. Neuroscience 206: 39–48.
6. Hay J, Aitken PP, Hutchison WM, Graham DI (1983) The effect of congenital
and adult-acquired Toxoplasma infections on the motor performance of mice.
Ann Trop Med Parasitol 77: 261–277.
7. Hay J, Aitken PP, Arnott MA (1985) The influence of Toxoplasma infection on the
spontaneous running activity of mice. Z Parasitenkd 71: 459–462.
8. Hodkova´ H, Kodym P, Flegr J (2007) Poorer results of mice with latent
toxoplasmosis in learning tests: impaired learning processes or the novelty
discrimination mechanism? Parasitology 134: 1329–1337.
9. Skallova´ A, Kodym P, Frynta D, Flegr J (2006) The role of dopamine in
Toxoplasma-induced behavioural alterations in mice: an ethological and
ethopharmacological study. Parasitology 133: 525–535.
10. Hutchison WM, Aitken PP, Wells BW (1980) Chronic Toxoplasma infections and
motor performance in the mouse. Ann Trop Med Parasitol 74: 507–510.
ˇ, Voty´pka J, Kodym P, Flegr J (2000) Transient nature of Toxoplasma
gondii-induced behavioral changes in mice. J Parasitol 86: 657–663.
12. Kannan G, Moldovan K, Xiao JC, Yolken RH, Jones-Brando L, et al. (2010)
Toxoplasma gondii strain-dependent effects on mouse behaviour. Folia Parasitol
13. Hay J, Aitken PP, Graham DI (1984) Toxoplasma infection and response to
novelty in mice. Z Parasitenkd 70: 575–588.
14. Berdoy M, Webster JP, Macdonald DW (2000) Fatal attraction in rats infected
with Toxoplasma gondii. Proc R Soc Biol Sci Ser B 267: 1591–1594.
15. Vyas A, Kim SK, Giacomini N, Boothroyd JC, Sapolsky RM (2007) Behavioral
changes induced by Toxoplasma infection of rodents are highly specific to aversion
of cat odors. Proc Natl Acad Sci U S A 104: 6442–6447.
16. House PK, Vyas A, Sapolsky R (2011) Predator cat odors activate sexual arousal
pathways in brains of Toxoplasma gondii infected rats. PLoS ONE 6.
ˇ, Kodym P, Flegr J (2011) Direct evidence of Toxoplasma-induced
changes in serum testosterone in mice. Exp Parasitol 128: 181–183.
18. Gaskell EA, Smith JE, Pinney JW, Westhead DR, McConkey GA (2009) A unique
dual activity amino acid hydroxylase in Toxoplasma gondii PLoS ONE 4: e4801.
19. Prandovszky E, Gaskell E, Martin H, Dubey JP, Webster JP, et al. (2011) The
neurotropic parasite Toxoplasma gondii increases dopamine metabolism. PLoS
ONE 6: e23866.
20. Tenter AM, Heckeroth AR, Weiss LM (2000) Toxoplasma gondii: from animals to
humans. Int J Parasitol 30: 1217–1258.
21. Thomas F, Lafferty KD, Brodeur J, Elguero E, Gauthier-Clerc M, et al. (2012)
Incidence of adult brain cancers is higher in countries where the protozoan
parasite Toxoplasma gondii is common. Biol Lett 8: 101–103.
22. Ling VJ, Lester D, Mortensen PB, Langenberg PW, Postolache TT (201 1)
Toxoplasma gondii seropositivity and suicide rates in women. J Nerv Ment Dis 199:
23. Yazar S, Gur M, Ozdogru I, Yaman O, Oguzhan A, et al. (2006) Anti-
Toxoplasma gondii antibodies in patients with chronic heart failure. J Med
Microbiol 55: 89–92.
24. Yolken RH, Dickerson FB, Torrey EF (2009) Toxoplasma and schizophrenia.
Parasite Immunol 31: 706–715.
25. Flegr J, Lenochova´P,Hodny´ Z, Vondrova´ M (2011) Fatal attraction
phenomenon in humans: cat odour attractiveness increased for Toxoplasma-
infected men while decreased for infected women. PLoS Neglect Trop Dis 5:
26. Flegr J (2010) Influence of latent toxoplasmosis on the phenotype of intermediate
hosts. Folia Parasitol 57: 81–87.
27. Novotna´ M, Havlı
ˇek J, Smith AP, Kolbekova´ P, Skallova´ A, et al. (2008)
Toxoplasma and reaction time: Role of toxoplasmosis in the origin, preservation
and geographical distribution of Rh blood group polymorphism. Parasitology
28. Flegr J, Novotna´ M, Lindova´ J, Havlı
ˇek J (2008) Neurophysiological effect of
the Rh factor. Protective role of the RhD molecule against Toxoplasma-induced
impairment of reaction times in women. Neuroendocrinol Lett 29: 475–481 .
29. Flegr J, Novotna´ M, Fialova´ A, Kolbekova´P,Gasˇova´ Z (2010) The influence of
RhD phenotype on toxoplasmosis- and age-associated changes in personality
profile of blood donors. Folia Parasitol 57: 143–150.
30. Flegr J, Klose J, Novotna´ M, Berenreitterova´ M, Havlı
ˇek J (2009) Increased
incidence of traffic accidents in Toxoplasma-infect ed military drivers and
protective effect RhD molecule revealed by a large-scale prospective cohort
study. BMC Infect Dis 9: art. 72.
ˇulc J, Flegr J (2010) Increased pregnancy weight gain in women
with latent toxoplasmosis and RhD-positivity protection against this effect.
Parasitology 137: 1773–1779.
32. Flegr J, Hampl R, C
ˇernochova´ D, Preiss M, Bic
´kova M, et al. (2012) The
relation of cort isol and sex hormone levels to resu lts of psychological,
performance, IQ and memory tests in military men and women. Neuroendo-
crinol Lett 33: 224–235.
ˇK (1973) Follow up of decissive processes in time pressure (In Czech:
´sni) [Doctoral thesis]. Faculty of
Philosophy: Charles University.
ˇkova´ M (2002) Internal consistency of the Czech version of the NEO
Personality Inventory (NEO-PI-R). Cesk Psychol 46: 521–535.
35. Formann AK, Piswanger K (1979) Wiener Matrizen -Test. Weinheim: Beltz.
36. Rasch G (1960) Probabilistic models for some intelligence and attainment tests.
Chicago, IL: MESA Press.
37. Raven JC (1947) Advanced progressiv e matrices. London: Lewis.
38. Raven JC (1958) Advanced progressiv e matrices (2nd ed.). London: Lewis.
39. Raven JC (1958) Standard progressiv e matrices. London: Lewis.
40. Klose J, C
ˇernochova´D,Kra´l P (2002) Vienna Matrix Test (Vı
test). Prague: Testcentrum.
41. Otis AS (1954) Otis Quick-Scoring Mental Abi lity Test, New E dition.
Tarrytown-on-Hudson, NY: Word Book Co.
42. Siegel S, Castellan NJ (1988) Nonparametric statistics for the behavioral
sciences. New York: McGraw-Hill. xxiii, 399 p.
43. Webster JP (2001) Rats, cats, people and parasites: the impact of latent
toxoplasmosis on behaviour. Microb Infect 3: 1037–1045.
44. Flegr J (2007) Effects of Toxoplas ma on human behavior. Schizophr Bull 33: 757–
´platova´ L, Flegr J (2012) Higher extraversion and lower
conscientiousness in humans infected with Toxoplasma. Eur J Person 26: 285–291.
46. Lafferty KD (2006) Can the common brain parasite, Toxoplasma gondii, influence
human culture? Proc R Soc Biol Sci Ser B 273: 2749–2755.
47. Flegr J, Geryk J, Volny J, Klose J, C
ˇernochova´ D (2012) Rhesus factor
modulation of effects of smoking and age on psychomotor performance,
intelligence, personality profile, and health in Czech soldiers. PLoS ONE 7.
48. Flegr J, Zitkova S, Kodym P, Frynta D (1996) Induction of changes in human
behaviour by the parasitic protozoan Toxoplasma gondii Parasitology 113: 49–54.
49. Flegr J, Havlı
ˇek J (1999) Changes in the personality profile of young women
with latent toxoplasmosis. Folia Parasitol 46: 22–28.
50. Carritt B, Kemp TJ, Poulter M (1997) Evolution of the human RH (rhesus)
blood group genes: A 50 year old prediction (partially) fulfilled. Hum Mol Genet
51. Flegel WA (2006) Molecular genetics of RH and its clinical application. Transfus
Clin Biol 13: 4–12.
52. Biver S, Scohy S, Szpirer J, Szpirer C, Andre B, et al. (2006) Physiological role of
the putative ammonium transporter RhCG in the mouse. Transfus Clin Biol 13:
53. Kustu S, Inwood W (2006) Biological gas channels for NH
that Rh (rhesus) proteins are CO
channels. Transfus Clin Biol 13: 103–110.
54. Gruswitz F, Chaudhary S, Ho JD, Schlessinger A, Pezeshki B, et al. (2010)
Function of human Rh based on structure of RhCG at 2.1 A. Proc Natl Acad
Sci U S A 107: 9638–9643.
55. Wagner FF, Flegel WA (2000) RHD gene deletion occurred in the Rhesus box.
Blood 95: 3662–3668.
56. Prandota J (2004) Possible pathomechanisms of sudden infant death syndrome:
key role of chronic hypoxia, infection/inflammation states, cytokine irregularities,
and metabolic trauma in genetically predisposed infants. Am J Ther 11: 517–546.
57. Prandota J (2010) Migraine associated with patent foramen ovale may be caused
by reactivation of cerebral toxoplasmosis triggered by arterial blood oxygen
desaturation. Int J Neurosci 120: 81–87.
58. Prandota J (2012) Rhesus-associated glycoprotein (RhAG) phenotype of the red
blood cells modulates T. gondii infection-associated psychomotor performance
reaction times and changes in the human personality profile. Impaired function
of the CO
, AQP1, and AQP4 gas channels may cause hypoxia and thus
enhance neuroinflammation in autistic individuals. In: Gemma C, editor.
Neuroinflammation: Pathogenesis, Mechanisms and Management. New York:
59. Lindova´ J, Kube
ˇna AA, S
ˇivohlava´ R, Novotna´ M, et al. (2010)
Pattern of money allocation in experimental games supports the stress hypothesis
of gender differences in Toxoplasma gondii-induced behavioural changes. Folia
Parasitol 57: 136–142.
60. Novotna´ M, Hanusˇova´ J, Klose J, Preiss M, Havlı
ˇek J, et al. (2005) Probable
neuroimmunological link between Toxoplasma and cytomegalovirus infections
and personality changes in the human host. BMC Infect Dis 5: 54.
61. Wiener AS (1965) Blood groups and personality traits. Am J Hum Genet 17:
62. Cattell RB (1972) Blood-groups and personality traits. Am J Hum Genet 24:
63. Rogers M, Glendon AI (2003) Blood type and personality. Pers Individ Diff 34:
64. Wu KH, Lindsted KD, Lee JW (2005) Blood type and the five factors of
personality in Asia. Pers Individ Diff 38: 797–808.
Effect of Toxoplasmosis and RhD on Intelligence
PLOS ONE | www.plosone.org 8 April 2013 | Volume 8 | Issue 4 | e61272