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Influence of latent toxoplasmosis on the secondary sex ratio in mice

  • Š. KAŇKOVÁ (a1), P. KODYM (a2), D. FRYNTA (a3), R. VAVŘINOVÁ (a1), A. KUBĚNA (a1) and J. FLEGR (a1)...


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.


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*Corresponding author: Department of Parasitology, Faculty of Science, Charles University, Viničná 7, CZ-128 44 Praha 2, Czech Republic. Tel: +420 221951821. Fax: +420 224919704. E-mail:


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Aasen, E. and Medrano, J. (1990). Amplification of the ZFY and ZFX genes for sex identification in humans, cattle, sheep and goats. Bio-Technology 8, 12791281.
Altmann, J., Hausfater, G. and Altmann, S. A. (1988). Determinants of reproductive success in savannah baboons. In Reproductive Success (ed. Clutton-Brock, T. H.), pp. 403413. University of Chicago Press, Chicago, USA.
Beattie, C. P. (1982). The ecology of toxoplasmosis. Ecology of Disease 1, 1320.
Berdoy, M., Webster, J. P. and MacDonald, D. W. (1995). Parasite-altered behaviour: is the effect of Toxoplasma gondii on Rattus norvegicus specific? Parasitology 111, 403409.
Berdoy, M., Webster, J. P. and MacDonald, D. W. (2000). Fatal attraction in rats infected with Toxoplasma gondii. Proceedings of the Royal Society of London, B 267, 15911594.
Brown, J. E. (1969). Field experiments on the movements of Apodemus sylvaticus L., using trapping and tracking techniques. Oecologia 2, 198222.
Bryja, J. and Konečný, A. (2003). Fast sex identification in wild mammals using PCR amplification of the Sry gene. Folia Zoologica 52, 269274.
Chacon-Pugnau, G. C. and Jaffe, K. (1996). Sex ratio at birth deviations in modern Venezuela: the Trivers-Willard effect. Social Biology 43, 257270.
Christiansen, O. B., Pedersen, B., Nielsen, H. S. and Andersen, A. M. N. (2004). Impact of the sex of first child on the prognosis in secondary recurrent miscarriage. Human Reproduction 19, 29462951.
Clark, A. B. (1978). Sex ratio and local resource competition in a Prosimian primate. Science 201, 163165.
Clutton-Brock, T. H. and Iason, G. R. (1986) Sex ratio variation in mammals. Quarterly Review of Biology 61, 339374.
Čiháková, J. and Frynta, D. (1996). Intraspecific and interspecific behavioural interactions in the Wood mouse (Apodemus sylvaticus) and the Yellow-necked mouse (Apodemus flavicollis) in a neutral cage. Folia Zoologica 45, 105113.
Dunn, A. M., Terry, R. S. and Smith, J. E. (2001). Transovarial transmission in the microsporidia. Advances in Parasitology 48, 57100.
Elenkov, I. J. and Chrousos, G. P. (2002). Stress hormones, proinflammatory and antiinflammatory cytokines, and autoimmunity. Annals of the New York Academy of Sciences 966, 290303.
Evdokimova, V. N., Nikita, T. V., Lebedev, I. N., Sukhanova, N. N. and Nazarenko, S. A. (2000). Sex ratio in early embryonal mortality in man. Ontogenes 31, 251257.
Fahrmeir, L. and Tutz, G. (2002). Multivariate Statistical Modelling Based on Generalized Linear Models, 2nd Edn, Springer Series in Statistics, Springer Verlag, New York.
Filisetti, D. and Candolfi, E. (2004). Immune response to Toxoplasma gondii. Annali Dell'Istituto Superiore di Sanità 40, 7180.
Fisher, R. A. (1958). The Genetical Theory of Natural Selection, 2nd Edn. Dover Publications, New York.
Flegr, J., Hrušková, M., Hodný, Z., Novotná, M. and Hanušová, J. (2005). Body height, body mass index, waist-hip ratio, fluctuating asymetry and second to fourth digit ratio in subjects with latent toxoplasmosis. Parasitology 130, 621628.
Frynta, D. (1994). Exploratory behaviour in 12 Palaearctic mice species (Rodentia: Muridae): A comparative study using “free exploration” test. Acta Societatis Zoologicae Bohemicae 57, 173182.
Frynta, D., Munclinger, P., Slábová, M., Volfová, R. and Třeštíková, H. (2005). Aggression and commensalism in house mouse: a comparative study across Europe and Near East. Aggressive Behavior 31, 283293.
Hamilton, W. D. (1967). Extraordinary sex ratios. Science 156, 477478.
Hostomská, L., Jírovec, O., Horáčková, M. and Hrubcová, M. (1957). Účast toxoplasmické infekce matky při vniku mongoloidismu dítěte. (The role of toxoplasmosis in the mother in the development of mongolism in the child). Československá Pediatrie 12, 713723.
Hutchison, W. M., Bradley, M., Cheyne, V. M., Welh, B. W. P. and Hay, J. (1980 a). Behavioural abnormalities in Toxoplasma-infected mice. Annals of Tropical Medicine and Parasitology 74, 337345.
Hutchison, W. M., Aitken, P. P., Wells, B. W. P. (1980 b). Chronic Toxoplasma infection and motor performance in the mouse. Annals of Tropical Medicine and Parasitology 74, 507510.
Jacobsen, R., Moller, H. and Mouritsen, A. (1999). Natural variation in the human sex ratio. Human Reproduction 14, 31203125.
James, W. H. (1986). Hormonal control of sex ratio. Journal of Theoretical Biology 118, 427441.
James, W. H. (1996). Evidence that mammalian sex ratios at birth are partially controlled by parental hormone levels at the time of conception. Journal of Theoretical Biology 180, 271286.
Kaňková, Š., Šulc, J., Nouzová, K., Fajfrlík, K., Frynta, D. and Flegr, J. (2007). Women infected with parasite Toxoplasma have more sons. Naturwissenschaften 94, 122127.
Kellokumpu-Lehtinen, P. and Pelliniemi, L. J. (1984). Sex ratio of human conceptuses. Obstetrics and Gynecology 64, 220222.
Kinsley, C. and Svare, B. (1985). Prenatal stress alters maternal aggression in mice. Physiology & Behavior 42, 713.
Kirby, D. R. S. (1970). The egg and immunology. Proceedings of the Royal Society of Medicine 63, 59.
Kirby, D. R. S., McWhirter, K. G., Teitelbaum, M. S. and Darlington, C. D. (1967). A possible immunological influence on sex ratio. Lancet I, 139140.
Knight, J. (2001). Meet the Herod bug. Nature, London 412, 1214.
Kodym, P., Blažek, K., Malý, M. and Hrdá, Š (2002). Pathogenesis of experimental toxoplasmosis in mice with strains differing in virulence. Acta Parasitologica 47, 239248.
Krackow, S. and Burgoyne, P. S. (1998). Timing of mating, developmental asynchrony and the sex ratio in mice. Physiology & Behavior 63, 8184.
Krackow, S. and Gruber, F. (1990). Sex ratio litter size in relation to parity and mode of conception in the three inbred strains of mice. Laboratory Animals 24, 345352.
Krackow, S. and Hoeck, H. N. (1989). Sex ratio manipulation, maternal investment and behaviour during concurrent pregnancy and lactation in house mice. Animal Behaviour 37, 177186.
Krackow, S. and Tkadlec, E. (2001). Analysis of broad sex ratio: implication of offspring clustering. Behavioral Ecology and Sociobiology 50, 293301.
Larralde, C., Morales, J., Terrazas, I., Govezensky, T. and Romano, M. C. (1995). Sex hormone changes induced by the parasite lead to feminization of the male host in murine Taenia crassiceps cysticercosis. The Journal of Steroid Biochemistry and Molecular Biology 52, 575580.
Marshall, P. A., Hughes, J. M., Williams, R. H., Smith, J. E., Murphy, R. G. and Hide, G. (2004). Detection of high levels of congenital transmission of Toxoplasma gondii in natural urban populations of Mus domesticus. Parasitology 128, 3942.
Milki, A. A., Jun, S. H., Hinckley, M. D., Westphal, L. W., Giudice, L. C. and Behr, B. (2003). Comparison of the sex ratio with blastocyst transfer and cleavage stage transfer. Journal of Assisted Reproduction and Genetics 20, 323326.
Myers, R. H., Montgomery, L. C. and Vining, G. G. (2002). Generalized Linear Models: with Applications in Engineering and the Sciences. John Wiley & Sons, New York.
Neuhauser, M. and Krackow, S. (2007). Adaptive-filtering of trisomy 21: risk of Down Syndrome depends on family size and age of previous child. Naturwissenschaften 94, 117121.
Ondriska, F., Čatár, G. and Vozarová, G. (2003). The significance of complement fixation test in clinical diagnosis of toxoplasmosis. Bratislavské Lekárske Listy 104, 189196.
Owen, M. R. and Trees, A. J. (1998). Vertical transmission of Toxoplasma gondii from chronically infected house (Mus musculus) and field (Apodemus sylvaticus) mice determined by polymerase chain reaction. Parasitology 116, 299304.
Pocock, M. J. O., Hauffe, H. C. and Searle, J. B. (2005). The genus Mus as a model for evolutionary studies. Biological Journal of the Linnean Society 84, 565583.
Renkonen, K. O., Makela, R. and Lehtovaara, R. (1962). Factors affecting the human sex ratio. Nature, London 194, 308.
Rice, W. R. and Gaines, S. D. (1994). The ordered-heterogeneity family of tests. Biometrics 50, 746752.
Rozsa, L. (2000). Spite, xenophobia, and collaboration between hosts and parasites. Oikos 91, 396400.
Shalev, A., Nelson, N. A. and Hamerton, J. L. (1980). Evidence for the role of the maternal immune system in balancing the sex ratio in mice. Journal of Reproductive Immunology 2, 187198.
Sheskin, D. J. (2003). Handbook of Parametric and Nonparametric Statistical Procedures (3rd Edn). Chapman and Hall/CRC Press, Boca Raton, FL, USA.
Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. (2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 12171258.
Trivers, R. L. and Willard, D. E. (1973). Natural selection of parental ability to vary the sex ratio of offspring. Science 179, 9092.
Vatten, L. J. and Skjaerven, R. (2004). Offspring sex and pregnancy outcome by length of gestation. Early Human Development 76, 4754.
Webster, J. P. (1994). The effect of Toxoplasma gondii and other parasites on activity levels in wild and hybrid Rattus norvegicus. Parasitology 109, 583589.
Witting, P. A. (1979). Learning capacity and memory of normal and Toxoplasma-infected laboratory rats and mice. Zeitschrift für Parasitenkunde 61, 2951.


Influence of latent toxoplasmosis on the secondary sex ratio in mice

  • Š. KAŇKOVÁ (a1), P. KODYM (a2), D. FRYNTA (a3), R. VAVŘINOVÁ (a1), A. KUBĚNA (a1) and J. FLEGR (a1)...


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