The boy-to-girl ratio at birth (secondary sex ratio) is around 0.51 in most populations. The sex ratio varies between societies and may be influenced by many factors, such as stress and immunosuppression, age, primiparity, the sex of the preceding siblings and the socioeconomic status of the parents. As parasite infection affects many immunological and physiological parameters of the host, we analyzed the effect of latent toxoplasmosis on sex ratios in humans. Clinical records of 1,803 infants born from 1996 to 2004 contained information regarding the mother's age, concentration of anti-Toxoplasma antibodies, previous deliveries and abortions and the sex of the newborn. The results of our retrospective cohort study suggest that the presence of one of the most common parasites (with a worldwide prevalence from 20 to 80%), Toxoplasma gondii, can influence the secondary sex ratio in humans. Depending on the antibody concentration, the probability of the birth of a boy can increase up to a value of 0.72, C.I.95 = (0.636, 0.805), which means that for every 260 boys born, 100 girls are born to women with the highest concentration of anti-Toxoplasma antibodies. The toxoplasmosis associated with immunosuppression or immunomodulation might be responsible for the enhanced survival of male embryos. In light of the high prevalence of latent toxoplasmosis in most countries, the impact of toxoplasmosis on the human population might be considerable.
The sex ratio may be influenced by many factors, such as stress and immunosuppression, age of parents, parity and sex of preceding siblings. In animal systems, parasitism often changes the sex ratio of infected hosts, which can increase the probability of their transmission. The most common human protozoan parasite in developed countries, Toxoplasma gondii (prevalence 20%-80%), is known to change the behaviour of its intermediate hosts, thereby increasing the probability of transmission to its definitive host (the cat) by predation. The intermediate hosts, which under natural conditions are rodents, serve as the vector for Toxoplasma. Therefore, we speculate that Toxoplasma can alter the secondary sex ratio (i.e. male to female ratio in the offspring) of infected females to increase the proportion of (congenitally infected) male offspring, which are the more migratory sex in most rodent species. Here we studied the sex ratio of experimentally infected laboratory mice, expressed here as the proportion of males in the litter. In accordance with our hypothesis and results of previous retrospective cohort studies on human subjects, mice with toxoplasmosis produced a higher sex ratio than controls, in the early phase of latent infection. In the later phase of infection, mice with congenital toxoplasmosis had a lower sex ratio than controls, which is in accord with the Trivers-Willard hypothesis of sex ratio manipulation, suggesting that females in poor physical condition give birth to more female offspring.
The most parsimonious explanation for the observed data is that the RhD-positive phenotype might protect infected subjects against a broad spectrum of detrimental effects of latent toxoplasmosis, including excessive gestational weight gain.
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.
Maintenance of genetic polymorphism remains one of the big questions of evolutionary biology, which for a long time tended to be explained by balancing selection. This explanation was later criticized, but now is again accepted as an important mechanism in evolution. Human blood group systems seem affected by balancing selection especially strongly. In this preregistered study, we focused on stable coexistence of RhD‐positive and RhD‐negative subjects in a population. This is an evolutionary conundrum, because carriers of the less frequent negative allele suffer from lower fecundity due to haemolytic disease of the newborn affecting RhD‐positive infants born to RhD‐negative women. One explanation of persisting stability of RhD polymorphism points to heterozygote advantage. Over the past decade, numerous studies demonstrated that RhD‐positive subjects score better than RhD‐negative homozygotes in psychomotor tests and physical health‐related variables. Still, evidence of better health and performance of heterozygotes is scarce and merely indirect. We compared the physical and mental health of 2,539 subjects whose RhD genotype was estimated based on their and their parents' RhD phenotype. We confirmed that RhD‐negative homozygotes fare worse in terms of physical and mental health than subjects with RhD‐positive phenotype and that RhD‐positive heterozygotes enjoy better health than both homozygotes. For the first time, we demonstrated that RhD‐positive homozygotes might suffer from worse health than RhD‐negative homozygotes. Our results strongly support the hypothesis that RhD polymorphism is maintained by heterozygote advantage and that balancing selection may have played an important role in human evolution in this context and in general.
Several studies have investigated the association between infection with Toxoplasma gondii (Nicolle et Manceaux, 1908), pregnancy and fertility, but the results of studies focused on the fertility are rather ambiguous. Here we report results of four new cross-sectional studies. The studies were performed in the General University Hospital, Prague (study A with n = 1 165, and study C with n = 317), in private clinics of the Centre of Reproductive Medicine, Prague (study B with n = 1 016), and in a population of Czech and Slovak volunteers from the Facebook page 'Guinea Pigs' willing to participate in various basic science studies (study D with n = 524). In studies A and B, the clinical records were used to assess the fertility problems, whereas in studies C and D, the women were asked to rate their fertility problems using a six-point scale. Pregnant T. gondii-infected women were older than T. gondii-free women (study A: 33.1 vs 31.2, P < 0.001; study B: 30.6 vs 29.6, P = 0.012) and more often used assisted reproductive technology to conceive (study A: 17.2% vs 12.4%, P = 0.041; study B: 13.4% vs 9.2%, P = 0.317). Pregnant T. gondii-infected primiparous women were older than T. gondii-free primiparas (study A: 31.1 vs 29.5, P < 0.001; study B: 29.7 vs 28.9, P = 0.064) and more often used assisted reproductive technology to conceive (study A: 24.7% vs 14.4%, P = 0.010; study B: 15.9% vs 15.5%, P = 0.888). T. gondii-infected women reported to take a longer time to conceive than T. gondii-free women (P = 0.015). They also claimed to have more fertility problems than T. gondii-free women (P < 0.0001). Our results suggest that 'asymptomatic' latent toxoplasmosis could be a more serious source of fertility problems and health-associated burden than more severe but far rarer congenital toxoplasmosis.
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