Most cited article - PubMed ID 17028886
Women infected with parasite Toxoplasma have more sons
Latent infection with Toxoplasma gondii (Nicolle et Manceaux, 1908) has been repeatedly correlated with behavioural and physiological changes in both humans and animals. While classically regarded as a parasite transmitted via ingestion or vertical (transplacental) transmission, accumulating evidence suggests that sexual transmission may also contribute to its epidemiology. This review explores the hypothesis that some behavioural effects of toxoplasmosis - especially those related to attraction, sexual activity, and mate choice - may have evolved to facilitate sexual transmission of the parasite. We summarise findings from animal models and human studies that show modified sexual preferences, altered sexual activity, enhanced attractiveness in infected individuals, and elevated prevalence of T. gondii in groups exhibiting high sexual activity or non-traditional sexual behaviour patterns. Particular attention is given to the role of testosterone, which may mediate both behavioural changes and reproductive consequences, such as shifts in offspring sex ratios and fertility outcomes. Direct detection of the parasite in semen and evidence of transmission through insemination in non-human species further support the plausibility of this route. The observed behavioural effects may also intersect with mechanisms previously thought to enhance predation risk, such as altered fear responses to felid odours. Taken together, these findings point to the possibility that sexual transmission, while likely secondary in humans, may have played a more substantial role in the evolutionary history and current ecology of T. gondii than previously appreciated. This perspective also provides an alternative interpretative framework for understanding the broad spectrum of phenotypic changes associated with latent toxoplasmosis. Further interdisciplinary research is required to clarify the relative contribution of sexual transmission to the parasite's life cycle and to assess its implications for public health and theory of host-parasite coevolution.
- Keywords
- manipulation, parasite manipulation., review, sexual behaviour, sexually transmitted diseases, testosterone, toxoplasmosis,
- MeSH
- Host-Parasite Interactions * MeSH
- Humans MeSH
- Sexual Behavior MeSH
- Toxoplasma * physiology MeSH
- Toxoplasmosis * transmission parasitology MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
In this article, I recount the journey of discovering the effects of latent toxoplasmosis on human psychology, behaviour, morphology, and health as I observed it from the closest perspective over the past 30+ years, during which our laboratory has been intensely focused on this research. I trace how we moved from the initial observations of differences between infected and uninfected individuals in certain personality traits to the systematic study of similar differences in behaviour, both in the laboratory and in everyday life, as well as in physiological and even morphological traits. This eventually led us to investigate the causal relationships behind these observed associations and their molecular basis. I describe some of the unexpected discoveries our research revealed - whether it was the impact of toxoplasmosis on the human sexual index, the prenatal and postnatal development, the sexual preferences and behaviour, the modulatory effect of blood Rh factor on toxoplasmosis, or the discovery of sexual transmission of toxoplasmosis. In exploring whether the toxoplasmosis-associated effects were merely side effects of an ongoing latent infection, we gradually uncovered that seemingly asymptomatic toxoplasmosis has profound (and certainly not positive) effects on the mental and physical health of infected individuals. The article also includes three separate boxes that discuss some key methodological challenges we encountered along the way, such as how to distinguish the effect of infection from mere statistical association, or how to differentiate parasitic manipulation from a simple side effect.
- Keywords
- Rh factor, Toxoplasma, behaviour, chronic toxoplasmosis, dopamine, manipulation, mental health, morbidity, parasite., personality, physical health, schizophrenia, sex ratio, testosterone,
- MeSH
- History, 20th Century MeSH
- History, 21st Century MeSH
- Humans MeSH
- Sexual Behavior MeSH
- Toxoplasmosis * psychology physiopathology parasitology MeSH
- Animals MeSH
- Check Tag
- History, 20th Century MeSH
- History, 21st Century MeSH
- Humans MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Historical Article MeSH
- Review MeSH
Secondary sex ratios of animals with genetically determined sex may considerably deviate from equality. These deviations may be attributed to several proximate and ultimate factors. Sex ratio theory explains some of them as strategic decisions of mothers improving their fitness by selective investment in sons or daughters, e.g. local resource competition hypothesis (LRC) suggests that philopatric females tend to produce litters with male-biased sex ratios to avoid future competition with their daughters. Until now, only little attention has been paid to examine predictions of sex ratio theory in snakes possessing genetic sex determination and exhibiting large variance in allocation of maternal investment. Cuban boa is an endemic viviparous snake producing large-bodied newborns (∼200 g). Extremely high maternal investment in each offspring increases importance of sex allocation. In a captive colony, we collected breeding records of 42 mothers, 62 litters and 306 newborns and examined secondary sex ratios (SR) and sexual size dimorphism (SSD) of newborns. None of the examined morphometric traits of neonates appeared sexually dimorphic. The sex ratio was slightly male biased (174 males versus 132 females) and litter sex ratio significantly decreased with female snout-vent length. We interpret this relationship as an additional support for LRC as competition between mothers and daughters increases with similarity of body sizes between competing snakes.
- Keywords
- Litter sex ratio, Sex allocation, Sexual size dimorphism, Snakes,
- MeSH
- Analysis of Variance MeSH
- Boidae anatomy & histology physiology MeSH
- Sex Ratio * MeSH
- Reproduction MeSH
- Body Size * MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
BACKGROUND: Toxoplasmosis is becoming a global health hazard as it infects 30-50% of the world human population. Clinically, the life-long presence of the parasite in tissues of a majority of infected individuals is usually considered asymptomatic. However, a number of studies show that this 'asymptomatic infection' may also lead to development of other human pathologies. AIMS OF THE STUDY: The purpose of the study was to collect available geoepidemiological data on seroprevalence of toxoplasmosis and search for its relationship with mortality and disability rates in different countries. METHODS AND FINDINGS: Prevalence data published between 1995-2008 for women in child-bearing age were collected for 88 countries (29 European). The association between prevalence of toxoplasmosis and specific disease burden estimated with age-standardized Disability Adjusted Life Year (DALY) or with mortality, was calculated using General Linear Method with Gross Domestic Product per capita (GDP), geolatitude and humidity as covariates, and also using nonparametric partial Kendall correlation test with GDP as a covariate. The prevalence of toxoplasmosis correlated with specific disease burden in particular countries explaining 23% of variability in disease burden in Europe. The analyses revealed that for example, DALY of 23 of 128 analyzed diseases and disease categories on the WHO list showed correlations (18 positive, 5 negative) with prevalence of toxoplasmosis and another 12 diseases showed positive trends (p<0.1). For several obtained significant correlations between the seroprevalence of toxoplasmosis and specific diseases/clinical entities, possible pathophysiological, biochemical and molecular explanations are presented. CONCLUSIONS: The seroprevalence of toxoplasmosis correlated with various disease burden. Statistical associations does not necessarily mean causality. The precautionary principle suggests however that possible role of toxoplasmosis as a triggering factor responsible for development of several clinical entities deserves much more attention and financial support both in everyday medical practice and future clinical research.
- MeSH
- Asymptomatic Diseases epidemiology MeSH
- Accidents, Traffic statistics & numerical data MeSH
- Gross Domestic Product MeSH
- Internationality * MeSH
- Quality-Adjusted Life Years MeSH
- Humans MeSH
- Prevalence MeSH
- Suicide statistics & numerical data MeSH
- Seroepidemiologic Studies MeSH
- Toxoplasmosis blood epidemiology mortality transmission MeSH
- Humidity MeSH
- Geography MeSH
- Check Tag
- Humans MeSH
- Male MeSH
- Female MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
BACKGROUND: Rhesus-positive and rhesus-negative persons differ in the presence-absence of highly immunogenic RhD protein on the erythrocyte membrane. This protein is a component of NH(3) or CO(2) pump whose physiological role is unknown. Several recent studies have shown that RhD positivity protects against effects of latent toxoplasmosis on motor performance and personality. It is not known, however, whether the RhD phenotype modifies exclusively the response of the body to toxoplasmosis or whether it also influences effects of other factors. METHODOLOGY/PRINCIPAL FINDINGS: In the present cohort study, we searched for the effects of age and smoking on performance, intelligence, personality and self-estimated health and wellness in about 3800 draftees. We found that the positive effect of age on performance and intelligence was stronger in RhD-positive soldiers, while the negative effect of smoking on performance and intelligence was of similar size regardless of the RhD phenotype. The effect of age on four Cattell's personality factors, i.e., dominance (E), radicalism (Q(1)), self-sentiment integration (Q(3)), and ergic tension (Q(4)), and on Cloninger's factor reward dependency (RD) was stronger for RhD-negative than RhD-positive subjects, while the effect of smoking on the number of viral and bacterial diseases was about three times stronger for RhD-negative than RhD-positive subjects. CONCLUSIONS: RhD phenotype modulates the influence not only of latent toxoplasmosis, but also of at least two other potentially detrimental factors, age and smoking, on human behavior and physiology. The negative effect of smoking on health (estimated on the basis of the self-rated number of common viral and bacterial diseases in the past year) was much stronger in RhD-negative than RhD-positive subjects. It is critically needed to confirm the differences in health response to smoking between RhD-positive and RhD-negative subjects by objective medical examination in future studies.
- MeSH
- Adult MeSH
- Phenotype MeSH
- Intelligence genetics MeSH
- Smoking genetics MeSH
- Rh-Hr Blood-Group System genetics metabolism MeSH
- Humans MeSH
- Adolescent MeSH
- Young Adult MeSH
- Personality genetics MeSH
- Military Personnel * MeSH
- Psychomotor Performance * MeSH
- Toxoplasmosis genetics MeSH
- Age Factors MeSH
- Check Tag
- Adult MeSH
- Humans MeSH
- Adolescent MeSH
- Young Adult MeSH
- Male MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Rh-Hr Blood-Group System MeSH
- Rho(D) antigen MeSH Browser
BACKGROUND: About 30% of the population worldwide are infected with the protozoan parasite Toxoplasma gondii. Latent toxoplasmosis has many specific behavioral and physiological effects on the human organism. Modified reactivity of the immune system has been suggested to play a key role in many of these effects. For example, the immunosuppression hypothesis explains the higher probability of the birth of male offspring observed in Toxoplasma-positive humans and mice by the protection of the (more immunogenic) male embryos against abortion. METHODS: Here we searched for indices of immunosuppression in Toxoplasma-positive subjects by comparing clinical records of immunology outpatients. RESULTS: Our cohort study showed that the male patients with latent toxoplasmosis had decreased and the Toxoplasma-positive women had increased leukocyte, NK-cell and monocyte counts in comparison with controls. The B-cell counts were reduced in both Toxoplasma-positive men and women. The difference between Toxoplasma-positive and Toxoplasma-negative subjects diminished with the decline of the specific Toxoplasma antibody titre (a proxy for the length of infection), which is consistent with the observed decreasing strength of the effect of latent toxoplasmosis on human reproduction. The prevalence of toxoplasmosis in 128 male patients was unusually low (10.9%) which contrasted with normal prevalence in 312 female patients (23.7%) and in general population Prague (20-30%). CONCLUSIONS: Latent toxoplasmosis has immunomodulatory effects in human and probably protects men against some classes of immunopathological diseases. The main limitation of the present study was the absence of the data on the immunoreactivity of immune cells subpopulations. Therefore further studies are needed to search for indices of immunosuppression in human using more specific markers.
- MeSH
- Asymptomatic Diseases * MeSH
- Adult MeSH
- Immune Tolerance * MeSH
- Cohort Studies MeSH
- Middle Aged MeSH
- Humans MeSH
- Mice MeSH
- Prospective Studies MeSH
- Toxoplasma immunology MeSH
- Toxoplasmosis immunology MeSH
- Animals MeSH
- Check Tag
- Adult MeSH
- Middle Aged MeSH
- Humans MeSH
- Male MeSH
- Mice MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Czech Republic MeSH
The immunosuppression hypothesis suggests that the increased sex ratio in mice and women with latent toxoplasmosis, retarded embryonic growth in the early phases of pregnancy, prolonged pregnancy of Toxoplasma-infected women, and increased prevalence of toxoplasmosis in mothers of children with Down syndrome can be explained by the presumed immunosuppressive effects of latent toxoplasmosis. Here, we searched for indices of immunosuppression in mice experimentally infected with Toxoplasma gondii. Our results showed that mice in the early phase of latent infection exhibited temporarily increased production of interleukin (IL)-12 and decreased production of IL-10. In accordance with the immunosuppression hypothesis, the mice showed decreased production of IL-2 and nitric oxide and decreased proliferation reaction (synthesis of DNA) in the mixed lymphocyte culture in the early and also in the late phases of latent toxoplasmosis. Since about 30% of the world population are latently infected by T. gondii, the toxoplasmosis-associated immunosuppression might have serious public health consequences.
- MeSH
- Asymptomatic Infections * MeSH
- Immune Tolerance * MeSH
- Interleukin-10 metabolism MeSH
- Interleukin-12 metabolism MeSH
- Humans MeSH
- Lymphocytes immunology MeSH
- Disease Models, Animal MeSH
- Mice MeSH
- Nitric Oxide metabolism MeSH
- Cell Proliferation MeSH
- Reproduction physiology MeSH
- Toxoplasma immunology MeSH
- Toxoplasmosis complications immunology MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Mice MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Interleukin-10 MeSH
- Interleukin-12 MeSH
- Nitric Oxide MeSH
BACKGROUND: The purpose of this study was to confirm that women with latent toxoplasmosis have developmentally younger fetuses at estimated pregnancy week 16 and to test four exclusive hypotheses that could explain the observed data. METHODS: In the present retrospective cohort study we analysed by the GLM (general linear model) method data from 730 Toxoplasma-free and 185 Toxoplasma-infected pregnant women. RESULTS: At pregnancy week 16 estimated from the date of the last menstruation, the mothers with latent toxoplasmosis had developmentally younger fetuses based on ultrasound scan (P = 0.014). Pregnancy of Toxoplasma-positive compared to Toxoplasma-negative women was by about 1.3 days longer, as estimated both from the date of the last menstruation (P = 0.015) and by ultrasonography (P = 0.025). CONCLUSION: The most parsimonious explanation for the observed data is retarded fetal growth during the first weeks of pregnancy in Toxoplasma-positive women. The phenomenon was only detectable in multiparous women, suggesting that the immune system may play some role in it.
- MeSH
- Time Factors MeSH
- Adult MeSH
- Cohort Studies MeSH
- Toxoplasmosis, Congenital complications physiopathology MeSH
- Humans MeSH
- Linear Models MeSH
- Pregnancy Complications, Parasitic physiopathology MeSH
- Parity MeSH
- Antibodies, Protozoan analysis MeSH
- Retrospective Studies MeSH
- Fetal Growth Retardation etiology physiopathology MeSH
- Pregnancy MeSH
- Ultrasonography, Prenatal MeSH
- Fetal Development physiology MeSH
- Check Tag
- Adult MeSH
- Humans MeSH
- Pregnancy MeSH
- Female MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Antibodies, Protozoan MeSH
Although latent infection with Toxoplasma gondii is among the most prevalent of human infections, it has been generally assumed that, except for congenital transmission, it is asymptomatic. The demonstration that latent Toxoplasma infections can alter behavior in rodents has led to a reconsideration of this assumption. When infected human adults were compared with uninfected adults on personality questionnaires or on a panel of behavioral tests, several differences were found. Other studies have demonstrated reduced psychomotor performance in affected individuals. Possible mechanisms by which T. gondii may affect human behavior include its effect on dopamine and on testosterone.
- MeSH
- Cattell Personality Factor Questionnaire * MeSH
- Chronic Disease MeSH
- Adult MeSH
- Humans MeSH
- Toxoplasmosis, Cerebral diagnosis immunology parasitology psychology MeSH
- Antibodies, Protozoan blood MeSH
- Psychomotor Performance physiology MeSH
- Reaction Time MeSH
- Schizophrenic Psychology * MeSH
- Schizophrenia diagnosis immunology parasitology MeSH
- Pregnancy MeSH
- Toxoplasma * immunology MeSH
- Age Factors MeSH
- Animals MeSH
- Check Tag
- Adult MeSH
- Humans MeSH
- Male MeSH
- Pregnancy MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Czech Republic MeSH
- Names of Substances
- Antibodies, Protozoan MeSH