Behavioral patterns, including sexual behavioral patterns, are usually understood as biological adaptations increasing the fitness of their carriers. Many parasites, so-called manipulators, are known to induce changes in the behavior of their hosts to increase their own fitness. Such changes are also induced by a parasite of cats, Toxoplasma gondii. The most remarkable change is the fatal attraction phenomenon, the switch of infected mice’s and rat’s native fear of the smell of cats toward an attraction to this smell. The stimuli that activate fear-related circuits in healthy rodents start to also activate sex-related circuits in the infected animals. An analogy of the fatal attraction phenomenon has also been observed in infected humans. Therefore, we tried to test a hypothesis that sexual arousal by fear-, violence-, and danger-related stimuli occurs more frequently in Toxoplasma -infected subjects. A cross-sectional cohort study performed on 36,564 subjects (5,087 Toxoplasma free and 741 Toxoplasma infected) showed that infected and noninfected subjects differ in their sexual behavior, fantasies, and preferences when age, health, and the size of the place where they spent childhood were controlled ( F (24, 3719) = 2.800, p < .0001). In agreement with our a priori hypothesis, infected subjects are more often aroused by their own fear, danger, and sexual submission although they practice more conventional sexual activities than Toxoplasma -free subjects. We suggest that the later changes can be related to a decrease in the personality trait of novelty seeking in infected subjects, which is potentially a side effect of increased concentration of dopamine in their brain.

Biologists are usually inclined to explain sexual preferences and behavior as biological adaptations covering individual reproductive success (Barbaro, Pham, & Shackelford, 2015; Barthes, Crochet, & Raymond, 2015; Hellstrand & Chrysochoou, 2015; Russell, DelPriore, Butterfield, & Hill, 2013). Such an interpretation concerns not only the “normal” sexual behavior and preferences expressed by a majority of people but also less frequent behavioral patterns, such as homosexuality, sadism, masochism, fetishism, and so on. Alternative sexual patterns are present in all populations in relatively high and constant frequencies, suggesting that these are sustained there by some form of selection, for example, frequency dependent selection rather than represent a part of sexual pathology. It has been, for example, suggested that male homosexuality can increase either the direct fitness of its carrier (Dewar, 2003; Macintyre & Estep, 1993) or it can increase his inclusive fitness by channeling resources toward his female relatives (Kirby, 2003; Rahman & Hull, 2005). Similarly, sexual dominance and sexual submissiveness have been suggested to increase the biological fitness of individuals by increasing the likelihood of women expressing sexual submissiveness, for example, masochism, to acquire “good genes” or “good resources” from dominant men (Jozifkova, Bartos, & Flegr, 2012). It has also been suggested that sexual dominance and submissiveness could increase in-pair cohesion and cooperation which could consequently result in an increased number of offspring in hierarchically disparate couples even within a modern community (Jozifkova, Konvicka, & Flegr, 2014).

An alternative evolutionary explanation of less frequent sexual behavior traits and sexual preferences is suggested by the general conception of extended phenotype (Dawkins, 1983) and its special application, the parasite manipulation theory (Moore, 2002). Certain categories of phenotypic traits of an organism could be the products of genes sitting within a body of other biological species and increasing their own between-generation transmission potential often at the expense of the fitness of carriers of these traits. Many parasites can change the morphology or behavior of their host in such a way that increases the efficiency of their transmission from an infected to noninfected host. Such manipulative activity was observed in many parasites transmitted from intermediate hosts to definitive hosts by predation. In human parasites, manipulative activity, both the induction of morphological and behavioral changes, was observed in the protozoan parasite Toxoplasma gondii (Flegr & Hrdý, 1994; Webster, 1994). This parasite can infect any warm-blooded animal, including about one third of humans worldwide (Pappas, Roussos, & Falagas, 2009; Tenter, Heckeroth, & Weiss, 2000). Toxoplasma can reproduce sexually in an intestine of its definitive host, a cat. It has been known for a long time that the parasite may live dormant for years in tissue cysts in immunoprivileged organs, inducing many behavioral changes in its intermediate host. For example, it prolongs the reaction times of its host, increases its vigility, and alters the tendency to seek new stimuli (Flegr et al., 2003; Hodková, Kodym, & Flegr, 2007; Hrdá, Votýpka, Kodym, & Flegr, 2000). The most remarkable toxoplasmosis-associated behavioral change is the so-called fatal attraction phenomenon—the switch from the mice’s and rats’ native fear of the smell of cats toward an attraction to this smell (Berdoy, Webster, & Macdonald, 2000). The existence of this phenomenon has been observed in mice and rats in about 20 studies performed in several laboratories worldwide and its analogy, higher ratings of attractiveness of smell of highly diluted cat (but not other species) urine was observed even in humans (Flegr, Lenochová, Hodný, & Vondrová, 2011). The neurological mechanism of this change in rats was revealed recently. It was shown that in the infected rats expressing fatal attraction, Toxoplasma is able to reprogram the brain’s genetic machinery by specific demethylation of certain regulatory elements of genes (Dass & Vyas, 2014). The cat odor activates fear-associated medial amygdala circuits in normal rodents. In the Toxoplasma-infected rodents, the same odor also activates the amygdala circuits responsible for sexual behavior. It is possible that Toxoplasma could increase its chances for alimentary transmission from infected rodents to cat intestine by making any perceived danger (not just the odor of cats) “smell sexy” to the infected host. Currently, between 10% and 80% of people are infected in most countries (Pappas et al., 2009; Tenter et al., 2000). However, less than 100 years ago, most of the population was probably infected in all countries where feline hosts of Toxoplasma lived, that is, nearly everywhere. It is therefore possible that sexual preferences and behaviors are at least partly influenced by the Toxoplasma infection. It is even possible that the frequent association of sexual arousal with violence, danger, fear, and exchange of power could be a product of manipulation activity of Toxoplasma, which was adaptive in its natural hosts—the rodents (Flegr & Markos, 2014).

In the present study, we tested a hypothesis that Toxoplasma-infected and Toxoplasma-free subjects differ in their sexual behavior, desires, and preferences. Specifically, we tested our animal studies-based hypothesis that the infected subjects were more often sexually aroused by their own fear, danger, and sexual submission. For this purpose, we ran a large-scale cross-sectional questionnaire study on the Internet population with a precise number of 36,564 Czech and Slovak people who completed the survey.

Material and Method Subjects The Internet questionnaire was distributed as a Qualtrics survey. The subjects were invited to participate in the study using a Facebook-based snowball method (Kankova, Flegr, & Calda, 2015) by posting an invitation to participate in a “study testing certain evolutionary psychological and parasitological hypotheses, containing many questions related to sexual life” on the wall of the Facebook page “guinea pigs” (“Pokusní králíci” in Czech) for Czech and Slovak nationals willing to take part in diverse evolutionary psychological experiments (www.facebook.com/pokusnikralici). The participants were informed about the aims of the study on the first page of the electronic questionnaire. They were also provided with the following information: “The questionnaire is anonymous and obtained data will be used exclusively for scientific purposes. Your cooperation in the project is voluntary and you can terminate it at any time by closing this web page. You can also skip any uncomfortable questions; however, the most valuable are the complete data. Only subjects above 15 years old are allowed to take the questionnaire. If you agree to participate in the research and are above 15, press the ‘Next’ button.” Some pages of the questionnaire contained the Facebook share button. These buttons were pressed by 1,163 participants, which resulted in obtaining data from 36,564 responders in total between January 22, 2015, and February 11, 2016. The project, including the method of obtaining an electronic consent with a participation in the study, was approved by the institutional review board of the Faculty of Science, Charles University (Komise pro práci s lidmi a lidským materiálem Přírodovědecké Fakulty Univerzity Karlovy), No. 2015/01. Questionnaires The electronic survey = Sexual Preferences and Behaviors Inventory 2015 (SPBI-2015) consisted of five already published questionnaires studying various facets of human sexuality, such as the Hurlbert Index of Sexual Narcissism (Hurlbert, Apt, Gasar, & Wilson, 1994), the Revised Sociosexual Orientation Inventory (SOI–R) (Penke & Asendorpf, 2008), the Three-Domain Disgust Scale (Tybur, Lieberman, & Griskevicius, 2009), the International Personality Item Pool (IPIP)–Dominance Scale (Goldberg, 1999; Goldberg et al., 2006), and the Attraction to Sexual Aggression Scale (Malamuth, 1989) modified and supplemented with questions to cover a broader spectrum of sexual preferences and sexual behaviors. The survey also contained a questionnaire collecting various socioeconomic, demographic, health-related, epidemiologic and psychological data, and three projective psychological tests. Altogether, the survey consisted of 701 questions (a few more in female version) and the mean time necessary to complete it was about 89 min (the mode was 72 min). In the present study, we used only the information about gender, age, the size of the population of the town where the responders spent most of their childhood rated on 6-point scale, sexuality-related questions, and three health-related questions (physical and psychological conditions rated on 6-point scales and number of specialized medical doctors the subject had to regularly attend [not for prevention] at least once in the past 5 years). The subject also had to answer a question “Are you infected with Toxoplasma, the cat parasite that is dangerous especially to pregnant women?” by ticking one of the three suggested answers: “I do not know or am not sure, I was not laboratory tested,” “No (I was tested by a medical doctor and the blood test gave a negative result,” and “Yes (I was tested by a medical doctor and the blood test gave a positive result.” Implicitly, the first answer (“I do not know …”) was ticked. At the end of the questionnaire, the participants could provide their unique “guinea pig code.” Because of the rather sensitive sex- and health-related contents of this questionnaire, it was “signed” only by 8% of the responders. However, other questionnaires distributed in this community were signed by most of responders (Flegr & Hodny, 2016). These results showed that most of participants who were aware of their toxoplasmosis status (and nearly all male responders) had been tested for toxoplasmosis in our lab. We always used complement fixation test, IgG enzyme-linked immunosorbent assay (ELISA), and IgM ELISA tests to reveal the Toxoplasma infection and to discriminate between acute and latent form of the infection (Flegr, Kodym, & Tolarová, 2000). Statistical Method Before statistical analysis, we filtered out less than 1% of our data because it appeared suspicious (too high or too short body height, too low or too high body mass or age, too short duration of the test, etc.). IBM SPSS Statistics 21.0 was used for all statistical tests including factor analysis (principal axis factoring [PAF], mean substitution of missing data, and direct oblimin normalized rotation). We computed optimal number of independent factors using parallel analysis (O’Connor, 2000). Associations between ordinal and binary data were analyzed by partial Kendall’s correlation test (Kaňková, Kodym, & Flegr, 2011; Siegel & Castellan, 1988). This test measures the strength and significance of association between binary, ordinal, and continuous data regardless of their distributions. The partial Kendall’s τ reflects the probability that the value of a particular dependent variable for the Subject A is higher than for Subject B when the value of an independent variable for Subject A is higher than for the Subject B. This technique enabled us to control for one confounding variable, for example, the age of a responder. The Excel sheet for computing partial Kendall’s τ and the significance between Variables A and B after the Variable C is controlled based on Kendall τ’s AB, AC, and BC. It is available at http://web.natur.cuni.cz/flegr/programy.php. Toxoplasmosis is known to have different, often opposite impacts on the behavior and personality men and women. Therefore, we performed all analyses for all responders and also separately for the male and female responders.

Results The final data set of 36,564 responders contained records of 2,470 Toxoplasma-free men (age 37.86, SD = 13.99), 212 Toxoplasma-infected men (age 36.15, SD = 13.97), 2,617 Toxoplasma-free women (age 33.73, SD = 11.91), and 529 Toxoplasma-infected women (age 34.83, SD = 11.28). Infected women were older than noninfected women (t(3146) = −2.034, p = .042); the difference in age between infected and noninfected men was not significant (t(2682) = 1.711, p = .088). The prevalence of toxoplasmosis in women (16.8%) was higher than in men (7.9%), χ2 = 103.575, p < .00001. The sexual behavior, desires, and preference of responders were characterized by 350 variables, including their responses to abovementioned standard questionnaires (Sexual Narcissism, Sexual Attitude Scale SOI-R, Disgust Scale, Dominance Scale, and modified Attraction to Sexual Aggression Scale) and questions of our SPBI-2015 (see Online Supplement 1) and the questionnaire concerning sexual preferences and types of pornography watched. We computed the optimal number of 24 independent factors using parallel analysis. The actual eigenvalues from PAF and the random order eigenvalues from parallel analysis are illustrated in Figure 1. Download Open in new tab Download in PowerPoint Therefore, the factor analysis reduced variables to 24 independent factors with eigenvalues higher than 2.361 that together explained 53.034% of the between-subject’s variance of sexual behavior and preferences. The nature of most of these factors was able to be identified on the basis of variables that positively or negatively loaded particular factors—factor names as well as example items defining the factors and the eigenvalue for each factor are represented in Table 1 (for full detail, see Online Supplement 2). Table 1. The Listing of Factor Names as Well as Example Items Defining the Factors and Eigenvalues for Each Factor. View larger version A multivariate analysis of variance with all 24 factors as dependent variables showed a significant effect of toxoplasmosis for all subjects (F(24, 5828) = 3.506, p < .0001), men (F(24, 2682) = 2.358, p < .0001), and women (F(24, 3146) = 1.798, p = .001). Regardless of the fact that age correlated with most of sexual life–related factors, the multivariate analyses of covariance with toxoplasmosis status and the age of subjects as independent variables gave nearly identical results (F(24, 5828) = 3.484, p < .0001), men (F(24, 2682) = 2.290, p < .0001), and women (F(24, 3146) = 1.782, p = .011). Very similar results were also obtained when a larger set of potential confounding variables, namely, age, population size of the place of residence, self-rated physical conditions, psychical conditions, and the number of medical specialists visited more than once during the past 5 years were controlled: all (F(24, 3719) = 2.800, p < .0001), men (F(24, 1542) = 1.899, p = .005), and women (F(24, 2177) = 1.732, p = .015). Here, the number of subjects was lower, and therefore p values were higher as not all subjects responded to all questions. Most sexual life–related factors had nonnormal distribution. To avoid performing a different type of transformation for each of 24 different factors, we used the nonparametric Kendall method for searching for association between toxoplasmosis and particular factors. We used nonparametric partial Kendall correlation test that enabled us to control for one confounding variable, here the age of responders. The results presented in Table 2 show that 18 of the 24 sex life–related factors, included the factor F3 (violence-associated arousal), expressed significant association with Toxoplasma infection for all subject, 11 for women, and 12 for men. Most of the observed associations (32) were significant after backward sequential correction for multiple tests (Table 2) and many of them (21), including that for sadism, remained significant even after the most conservative simple Bonferroni’s correction for multiple tests. Moreover, the number of observed significant associations was 41, that is, 1010 times higher than was the theoretical number of false negative results for 72 tests. Table 2. Association Between Sex-Related Factors and Toxoplasma Infection. View larger version Results of partial Kendall’s τ correlations between 24 sex-related factors obtained by factor analysis and Toxoplasma infection. The effect of age of subject was controlled. The absence and presence of Toxoplasma infection was coded with 1 and 2, respectively. Therefore, positive τs corresponded to positive association between particular factor and toxoplasmosis. Significant results are marked bold and .000 denote p < .0005. The asterisks denote that the associations are significant after backward sequential correction for multiple tests.

Limitations of the Present Study The major limitation of the present study is that it is based on self-reported information on subjects’ sexual life and self-reported Toxoplasma infection status. It is highly probable that some subjects intentionally or unintentionally provided false information. Probably, only highly motivated people finished the 90-min questionnaire. At the end of the questionnaire, the responders were also asked to rate the percentage of truthfully answered sexual life–related questions. The mean answer was about 96%. We believe that most of responders really try to provide truthful answers. It is, of course, clear that some subjects that were tested negative for toxoplasmosis in the past could have acquired the Toxoplasma infection in meantime. Such misclassification could increase the risk of false negative not the risk of false positive results of statistical tests. Another limitation of the present study is a strong sieve effect that probably influenced the composition of the study population. People entered the study absolutely voluntarily and obtained no reward for their participation. It is highly probable that only certain kind of people (e.g., extreme altruists or people extremely interested in sex) voluntarily spent about 90 min answering the questions of the present electronic questionnaire. Therefore, the obtained results cannot be generalized to whole Czech population. The Facebook community Guinea Pigs (Czech version of the website) primarily consists of subjects willing to regularly participate in various evolutionary psychology studies, and the present test was advertised as a part of the study focused on testing a nonspecified “evolutionary psychology and parasitology hypothesis.” The whole 36,000 sets were used for the computation of sexuality-related factors. This Facebook community consists of people of various ages, education levels, occupations, and places of residence. However, most of the subjects (and nearly all the male subjects) who know their Toxoplasma-infection status are former students of biology who were tested for toxoplasmosis during systematic research of behavioral effects of latent toxoplasmosis which has been running at the Faculty of Science for the past 23 years. In last 2 years, the members of the Guinea Pigs community participated in several Internet studies that have mostly no relation to toxoplasmosis. The question on toxoplasmosis status was just one of several hundreds of questions to be responded by the participants of the study. The participants did not know that the present study tested the hypothesis about relation between toxoplasmosis and sexual life and especially the hypothesis concerning sexual dominance and toxoplasmosis. However, the personality profile of infected and noninfected subjects is known to differ (Flegr, 2013) and therefore observed differences in sexual life–related factors could be just side effects of these general personality differences. In the future, instrumental sexological methods should be used to confirm the existence of differences in sexual preferences of Toxoplasma-infected and Toxoplasma-free subjects. Many of the observed effects are highly significant even after the most conservative Bonferroni’s correction for multiple tests partly because of the large number of participants. However, their effect sizes are relatively low but comparable with those of other already published behavioral effects of latent toxoplasmosis. It has been discussed earlier (Flegr, 2013) that due to the large variability of human populations in particular behavioral traits and also in the size and direction of behavioral responses to particular environmental and genetic factors, toxoplasmosis usually explains only between 1% and 5% of the variability of behavioral traits. For example, the recently observed effect of toxoplasmosis on performance of students in acoustic reaction time test explained between 2% and 3% of the variability in the subjects’ performance (Priplatova, Sebankova, & Flegr, 2014). Probably the strongest effect of latent toxoplasmosis on human behavior observed in past 25 years, its effect on attraction to the smell of highly diluted cat urine in men, explained 9.8% of the between-subjects variability in this trait (Flegr et al., 2011).

Conclusions Our study confirmed the existence of specific differences in sexual behavior, desires, and preferences between Toxoplasma-infected and Toxoplasma-free subjects. The character of these changes, that is, the higher attraction to bondage, violence, and, in men, to masochism and raping supports our hypothesis about the coactivation of sex-related and fear-related medial amygdala circuits in humans. It must be stressed that the Toxoplasma infection explains only small part of the variability in BDSM-associated traits. It was shown that sensitivity of current serological tests is not ideal and that even in populations of young seronegative subjects, 5–15% individuals are, in fact, Toxoplasma infected (Flegr & Havlíček, 1999; Flegr, Hrdá, & Kodym, 2005). In older age strata, the seroprevalence of toxoplasmosis decreases (Kolbeková, Kourbatova, Novotná, Kodym, & Flegr, 2007), which suggests that the frequency of false negatives among older people is probably much higher. It could be speculated that the false negatives, that is, the subjects with the oldest infections and therefore lowest concentration of anamnestic anti-Toxoplasma antibodies, could be responsible for certain BDSM traits in seemingly Toxoplasma-free subjects. A more probable explanation, however, is that the sexual arousal by danger, fear, and so on could have a common neurophysiological mechanism (possibly the coactivation of sex-related and fear-related circuits in amygdala), however this coactivation could have various independent causes and Toxoplasma just (mis)uses this property of the mammal brain for manipulation with behavior of their intermediate hosts.

Acknowledgments We would like to thank Lenka Příplatová for her help with preparing the electronic questionnaire; Charlie Lotterman, Martin Hůla, and Julie Nováková for their help with English version of this article; and Alena Černíková for her help with statistical analysis.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article. Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The authors’ work was supported by the Charles University of Prague (GAUK 269215, Grant UNCE 204004), the Grant Agency of the Czech Republic (Grant no. 16-20958 S), and by the project “National Institute of Mental Health (NIMH-CZ)” (Grant number ED2.1.00/03.0078; and the European Regional Development Fund). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of this article. Supplementary Materials

The online [appendices/data supplements/etc.] are available at http://evp.sagepub.com/supplemental.