Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-20T16:16:01.292Z Has data issue: false hasContentIssue false

Influence of latent toxoplasmosis on the secondary sex ratio in mice

Published online by Cambridge University Press:  26 July 2007

Š. KAŇKOVÁ
Affiliation:
Department of Parasitology, Faculty of Science, Charles University in Prague, Viničná 7, CZ-128 44 Prague 2, Czech Republic
P. KODYM
Affiliation:
National Reference Laboratory for Toxoplasmosis, National Institute of Public Health, Šrobárova 48, CZ-100 42 Prague 10, Czech Republic
D. FRYNTA
Affiliation:
Department of Zoology, Faculty of Science, Charles University in Prague, Viničná 7, CZ-128 44 Prague 2, Czech Republic
R. VAVŘINOVÁ
Affiliation:
Department of Parasitology, Faculty of Science, Charles University in Prague, Viničná 7, CZ-128 44 Prague 2, Czech Republic
A. KUBĚNA
Affiliation:
Department of Parasitology, Faculty of Science, Charles University in Prague, Viničná 7, CZ-128 44 Prague 2, Czech Republic
J. FLEGR*
Affiliation:
Department of Parasitology, Faculty of Science, Charles University in Prague, Viničná 7, CZ-128 44 Prague 2, Czech Republic
*
*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: flegr@cesnet.cz

Summary

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.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

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.Google ScholarPubMed
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.Google Scholar
Beattie, C. P. (1982). The ecology of toxoplasmosis. Ecology of Disease 1, 1320.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Brown, J. E. (1969). Field experiments on the movements of Apodemus sylvaticus L., using trapping and tracking techniques. Oecologia 2, 198222.CrossRefGoogle ScholarPubMed
Bryja, J. and Konečný, A. (2003). Fast sex identification in wild mammals using PCR amplification of the Sry gene. Folia Zoologica 52, 269274.Google Scholar
Chacon-Pugnau, G. C. and Jaffe, K. (1996). Sex ratio at birth deviations in modern Venezuela: the Trivers-Willard effect. Social Biology 43, 257270.Google Scholar
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.CrossRefGoogle ScholarPubMed
Clark, A. B. (1978). Sex ratio and local resource competition in a Prosimian primate. Science 201, 163165.CrossRefGoogle Scholar
Clutton-Brock, T. H. and Iason, G. R. (1986) Sex ratio variation in mammals. Quarterly Review of Biology 61, 339374.CrossRefGoogle ScholarPubMed
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.Google Scholar
Dunn, A. M., Terry, R. S. and Smith, J. E. (2001). Transovarial transmission in the microsporidia. Advances in Parasitology 48, 57100.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
Fahrmeir, L. and Tutz, G. (2002). Multivariate Statistical Modelling Based on Generalized Linear Models, 2nd Edn, Springer Series in Statistics, Springer Verlag, New York.Google Scholar
Filisetti, D. and Candolfi, E. (2004). Immune response to Toxoplasma gondii. Annali Dell'Istituto Superiore di Sanità 40, 7180.Google ScholarPubMed
Fisher, R. A. (1958). The Genetical Theory of Natural Selection, 2nd Edn. Dover Publications, New York.Google Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
Hamilton, W. D. (1967). Extraordinary sex ratios. Science 156, 477478.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Jacobsen, R., Moller, H. and Mouritsen, A. (1999). Natural variation in the human sex ratio. Human Reproduction 14, 31203125.CrossRefGoogle ScholarPubMed
James, W. H. (1986). Hormonal control of sex ratio. Journal of Theoretical Biology 118, 427441.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Kellokumpu-Lehtinen, P. and Pelliniemi, L. J. (1984). Sex ratio of human conceptuses. Obstetrics and Gynecology 64, 220222.Google ScholarPubMed
Kinsley, C. and Svare, B. (1985). Prenatal stress alters maternal aggression in mice. Physiology & Behavior 42, 713.CrossRefGoogle Scholar
Kirby, D. R. S. (1970). The egg and immunology. Proceedings of the Royal Society of Medicine 63, 59.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Knight, J. (2001). Meet the Herod bug. Nature, London 412, 1214.CrossRefGoogle ScholarPubMed
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.Google Scholar
Krackow, S. and Burgoyne, P. S. (1998). Timing of mating, developmental asynchrony and the sex ratio in mice. Physiology & Behavior 63, 8184.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Krackow, S. and Tkadlec, E. (2001). Analysis of broad sex ratio: implication of offspring clustering. Behavioral Ecology and Sociobiology 50, 293301.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
Ondriska, F., Čatár, G. and Vozarová, G. (2003). The significance of complement fixation test in clinical diagnosis of toxoplasmosis. Bratislavské Lekárske Listy 104, 189196.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Renkonen, K. O., Makela, R. and Lehtovaara, R. (1962). Factors affecting the human sex ratio. Nature, London 194, 308.CrossRefGoogle ScholarPubMed
Rice, W. R. and Gaines, S. D. (1994). The ordered-heterogeneity family of tests. Biometrics 50, 746752.CrossRefGoogle Scholar
Rozsa, L. (2000). Spite, xenophobia, and collaboration between hosts and parasites. Oikos 91, 396400.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Sheskin, D. J. (2003). Handbook of Parametric and Nonparametric Statistical Procedures (3rd Edn). Chapman and Hall/CRC Press, Boca Raton, FL, USA.CrossRefGoogle Scholar
Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. (2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 12171258.CrossRefGoogle ScholarPubMed
Trivers, R. L. and Willard, D. E. (1973). Natural selection of parental ability to vary the sex ratio of offspring. Science 179, 9092.CrossRefGoogle ScholarPubMed
Vatten, L. J. and Skjaerven, R. (2004). Offspring sex and pregnancy outcome by length of gestation. Early Human Development 76, 4754.CrossRefGoogle ScholarPubMed
Webster, J. P. (1994). The effect of Toxoplasma gondii and other parasites on activity levels in wild and hybrid Rattus norvegicus. Parasitology 109, 583589.CrossRefGoogle ScholarPubMed
Witting, P. A. (1979). Learning capacity and memory of normal and Toxoplasma-infected laboratory rats and mice. Zeitschrift für Parasitenkunde 61, 2951.CrossRefGoogle ScholarPubMed