Skip to main content

Advertisement

SpringerLink
Log in

Reduction in testosterone concentration and its effect on the reproductive output of chronic malaria-infected male mice

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

An experimental host-parasite association involving BALB/c male mice infected with Plasmodium chabaudi chabaudi was used in order to investigate the influence of the parasite on the sexual physiology and behavior of infected hosts. Infected males displayed complete courtship behavior leading to ejaculation and sired litters on several occasions. A weekly assay of testosterone and corticosterone plasma concentrations revealed a twofold decrease in the testosterone level at 4 and 5 weeks post-injection, during recrudescence. This imbalance was accompanied by a decrease in the overall duration of the social investigation contacts occurring during courtship and by a reduction in the fertilization rate of the infected animals. These physiological perturbations can be regarded as an adaptive response of the host to the recrudescing parasites, which illustrates the rodents’ capacity for regulating the testosterone profiles needed to balance the competing demands of immunity and reproduction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Akingbade O, Aina AO, Folashade BA, Modupe MJ (1990) Malaria parasitization and hormonal imbalance in virgin mice. J Med Assoc Thai 73:228–233

    PubMed  Google Scholar 

  • Allison AC (1956) The sickle-cell and haemoglobin C genes in some African populations. Ann Hum Genet 21:67–89

    CAS  PubMed  Google Scholar 

  • Andrade HF, Corbett CEP, Laurent MD, Duarte MIS (1991) Comparative and sequential histopathology of Plasmodium chabaudi-infected Balb/C mice. Braz J Med Biol Res 24:1209–1218

    PubMed  Google Scholar 

  • Barnard CJ, Behnke JM, Gage AR, Brown H, Smithurst PR (1998) The role of parasite-induced immunodepression, rank and social environment in the modulation of behavior and hormone concentration in male laboratory mice (Mus musculus). Proc R Soc Lond B Biol Sci 265:693–701

    Article  CAS  PubMed  Google Scholar 

  • Barthelemy M, Gourbal BEF, Gabrion C, Petit G (2004a) BALB/c male mouse calling behavior during mating: influence of the sexual cycle of the female. Naturwissenschaften 91:135–138

    CAS  PubMed  Google Scholar 

  • Barthelemy M, Vuong PN, Gabrion C, Petit G (2004b) Plasmodium chabaudi chabaudi malaria and pathologies of the urogenital tract in male and female BALB/c mice. Parasitology 128:113–122

    Article  CAS  PubMed  Google Scholar 

  • Bateman A, Singh A, Kral T, Solomon S (1989) The immune-hypothalamic-pituitary-adrenal axis. Endocr Rev 10:92–112

    CAS  PubMed  Google Scholar 

  • Baudoin M (1975) Host castration as a parasitic strategy. Evolution 29:335–352

    Google Scholar 

  • Baum MJ (1999) Mating behaviors, mammals. In: Knobil E, Neill JD (eds) Encyclopedia of reproduction. Academic Press, Oxford, pp 137–141

  • Benten WP, Wunderlich F, Mossmann H (1992) Testosterone-induced suppression of self-healing Plasmodium chabaudi malaria: an effect not mediated by androgen receptors? J Endocrinol 135:407–413

    CAS  PubMed  Google Scholar 

  • Benten WP, Ulrich P, Kuhn-Velten WN, Vohr HW, Wunderlich F (1997) Testosterone-induced susceptibility to Plasmodium chabaudi malaria: persistence after withdrawal of testosterone. J Endocrinol 153:275–281

    CAS  PubMed  Google Scholar 

  • Bilbo SD, Klein SL, DeVries AC, Nelson RJ (1999) Lipopolysaccharide facilitates partner preference behaviors in female prairie voles. Physiol Behav 68:151–156

    Article  CAS  PubMed  Google Scholar 

  • Blanco-Rodriguez J, Martinez-Garcia C (1997) Mild hypothermia induces apoptosis in rat testis at specific stages of the seminiferous epithelium. J Androl 18:535–539

    CAS  PubMed  Google Scholar 

  • Bronson FH (1979) The reproductive ecology of the house mouse. Q Rev Biol 54:265–299

    Article  CAS  PubMed  Google Scholar 

  • Bronson FH (1989) Mammalian reproductive biology. University of Chicago Press, Chicago

  • Brown RE (1994) An introduction to neuroendocrinology. Cambridge University Press, Cambridge

  • Chernin J, Morinan A (1985) Analysis of six serum components from rats infected with tetrathyridia of Mesocestoides corti. Parasitology 90:441–447

    PubMed  Google Scholar 

  • Cox FEG (1988) Major animal models in malaria research: rodent. In: Wersdorfer WH, MacGregor I (eds) Malaria: principles and practices of malariology. Churchill Livingston, Edinburgh, pp 1503–1543

  • De Catanzaro D, Gorzalka BB (1979) Isolation-induced facilitation of male sexual behavior in mice. J Comp Physiol Psychol 93:211–222

    PubMed  Google Scholar 

  • Duckworth RA, Mendonca MT, Hill GE (2001) A condition dependent link between testosterone and disease resistance in the house finch. Proc R Soc Lond B Biol Sci 268:2467–2472

    Article  CAS  PubMed  Google Scholar 

  • Dunlap KD, Schall JJ (1995) Hormonal alterations and reproductive inhibition in male fence lizards (Sceloporus occidentalis) infected with the malarial parasite Plasmodium mexicanum. Physiol Zool 68:608–921

    CAS  Google Scholar 

  • Eaton JW, Mucha JI (1971) Increased fertility in males with the sickle cell trait? Nature 231:456–457

    CAS  PubMed  Google Scholar 

  • Edwards JC, barnard CJ (1987) The effects of Trichinella infection on intersexual interactions between mice. Anim Behav 35:533–540

    Google Scholar 

  • Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622

    Article  Google Scholar 

  • Grossman CJ (1985) Interactions between the gonadal steroids and the immune system. Science 227:257–261

    CAS  PubMed  Google Scholar 

  • Hublart M, Tetaert D, Croix D, Boutignon F, Degand P, Boersma A (1990) Gonadotropic dysfunction produced by Trypanosoma brucei brucei in the rat. Acta Trop 47:177–184

    Article  CAS  PubMed  Google Scholar 

  • Kamis AB, Ibrahim JB (1989) Effects of testosterone on blood leukocytes in Plasmodium berghei-infected mice. Parasitol Res 75:611–613

    CAS  PubMed  Google Scholar 

  • Kerr JB (1999) Temperature, effects on testicular function. In: Knobil E, Neill JD (eds) Encyclopedia of reproduction. Academic Press, Oxford, pp 725–734

  • Klein SL, Hairston JE, Devries AC, Nelson RJ (1997) Social environment and steroid hormones affect species and sex differences in immune function among voles. Horm Behav 32:30–39

    Article  CAS  PubMed  Google Scholar 

  • Landau I, Boulard Y (1978) Life cycles and morphology. In: Killick-Kendrick R, Peters W (eds) Rodent malaria. Academic Press, London, pp 54–84

  • Landau I, Gautret P (1998) Animal models: rodents. In: Sherman IW (eds) Malaria: parasite biology, pathogenesis, and protection. ASM Press, Washington, D.C., pp 401–417

  • Larralde C, Morales J, Terrazas I, Govezensky T, Romano MC (1995) Sex hormone changes induced by the parasite lead to feminization of the male host in murine Taenia crassiceps cysticercosis. J Steroid Biochem Mol Biol 52:575–580

    Article  CAS  PubMed  Google Scholar 

  • Lin YC, Rikihisa Y, Kono H, Gu Y (1990) Effects of larval tapeworm (Taenia taeniaeformis) infection on reproductive functions in male and female host rats. Exp Parasitol 70:344–352

    Article  CAS  PubMed  Google Scholar 

  • Morales J, Larralde C, Arteaga M, Govezensky T, Romano MC, Morali G (1996) Inhibition of sexual behavior in male mice infected with Taenia crassiceps cysticerci. J Parasitol 82:689–693

    CAS  PubMed  Google Scholar 

  • Olsen NJ, Kovacs WJ (1996) Gonadal steroids and immunity. Endocr Rev 17:369–384

    Article  CAS  PubMed  Google Scholar 

  • Propes MJ, Johnson RW (1997) Role of corticosterone in the behavioral effects of central interleukin-1 beta. Physiol Behav 61:7–13

    Article  CAS  PubMed  Google Scholar 

  • Rudali G, Roudier R, Vives C (1974) The preputial gland of the male mouse. Pathol Biol (Paris) 22:895–899

    Google Scholar 

  • Spindler KD (1988) Parasites and hormones. In: Melhorn H (eds) Parasitology in focus: facts and trends. Springer, Berlin Heidelberg New York, pp 465–476

  • Tavares MC, Carraro AA, Favaretto AL, Petenusci SO, Lopes RA, Ribeiro RD, Carvalho TL (1994) The male reproductive organs in experimental Chagas’ disease. III. Plasma testosterone and accessory sex glands in the acute phase of the disease. Exp Toxicol Pathol 46:243–246

    CAS  PubMed  Google Scholar 

  • Taylor GT, Weiss J, Frechmann T, Haller J (1985) Copulation induces an acute increase in epididymal sperm numbers in rats. J Reprod Fertil 73:323–327

    Article  CAS  PubMed  Google Scholar 

  • Thornton JE, Finn PD (1999) Estrus. In: Knobil E, Neill JD (eds) Encyclopedia of reproduction. Academic Press, Oxford, pp 136–141

  • Vuong PN, Richard F, Snounou G, Coquelin F, Renia L, Gonnet F, Chabaud AG, Landau I (1999) Development of irreversible lesions in the brain, heart and kidney following acute and chronic murine malaria infection. Parasitology 119:543–553

    Article  PubMed  Google Scholar 

  • Wedekind C, Folstad I (1994) Adaptive or nonadaptive immunosuppression by sex hormones? Am Nat 143:936–938

    Article  Google Scholar 

  • Welsh TC, Kemper-Green CN, Livingston KN (1999) Stress and reproduction. In: Knobil E, Neill JD (eds) Encyclopedia of reproduction. Academic Press, Oxford, pp 662–674

  • White NR, Prasad M, Barfield RJ, Nyby JG (1998) 40- and 70-kHz vocalizations of mice (Mus musculus) during copulation. Physiol Behav 63:467–473

    Article  CAS  PubMed  Google Scholar 

  • Wunderlich F, Mossmann H, Helwig M, Schillinger G (1988) Resistance to Plasmodium chabaudi in B10 mice: influence of the H-2 complex and testosterone. Infect Immun 56:2400–2406

    CAS  PubMed  Google Scholar 

  • Wunderlich F, Maurin W, Benten WP, Schmitt-Wrede HP (1993) Testosterone impairs efficacy of protective vaccination against P. chabaudi malaria. Vaccine 11:1097–1099

    Article  CAS  PubMed  Google Scholar 

  • Zirkin BR (1999) Hormonal control of spermatogenesis. In: Knobil E, Neill JD (eds) Encyclopedia of reproduction. Academic Press, Oxford, pp 556–563

  • Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1024

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors gratefully acknowledge Elise Le Capitaine for monitoring the tests, Claudy Haussy for her assistance during the steroid assays, and Deborah Kay for revising the manuscript. This work was financed by a grant allocated to M. Barthélémy by the French Educational Ministry of Research and Technology. The authors adhered to the European recommendations (décret no. 87–848) for the care and use of laboratory animals adopted by the French government in October 1987.

Author information

Authors and Affiliations

  1. Laboratoire de Parasitologie Evolutive CNRS UMR 7103, Université Pierre et Marie Curie, 9 Quai Saint Bernard, Case 175, 75252 , Paris Cedex 05, France

    Mathieu Barthelemy, Claude Gabrion & Gilles Petit

Authors
  1. Mathieu Barthelemy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Claude Gabrion
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gilles Petit
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mathieu Barthelemy.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barthelemy, M., Gabrion, C. & Petit, G. Reduction in testosterone concentration and its effect on the reproductive output of chronic malaria-infected male mice. Parasitol Res 93, 475–481 (2004). https://doi.org/10.1007/s00436-004-1160-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-004-1160-2

Keywords

Search

Navigation