Skip to main content

Testosterone and Immunosuppression in Vertebrates: Implications for Parasite-Mediated Sexual Selection

  • Chapter

Abstract

Females of many species prefer to mate with males that have the fewest parasites (Møller, 1990; Read,1990; Kirkpatrick and Ryan, 1991; Clayton, 1991; McLennen and Brooks, 1991; Clayton et al., 1992; Sullivan, 1991; Zuk, 1992). Females appear to discriminate among males on the basis of the expression of secondary sex characters, such as comb color and feather lenth in junglefowl (Gallus gallus) (Zuk et al., 1990), red plumage in house finches (Cardodacus mexicanus) (Hill, 1991); eye spot number on the tail-like train of peafowl (Pavo cristatus) (Petrie et al., 1991), or tail length in barn swallows (Hirundo rustica)(Møller, 1991). Experimental manipulation of parasite load can alter and hinder the expression of secondary sex characters (Zuk et al., 1990, Møller, 1991, Hillgarth, 1990). Therefore, females choosing males with well-developed secondary sex characters are likely to choose relatively parasite-free mates.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Ahmed, S. A., Dauphinee, J., and Talal, N. (1985). Effects of short-term administration of sex hormones on normal and autoimmune mice. J. Immunol. 134:204–210.

    CAS  Google Scholar 

  • Astheimer, L. B., Buttemer, W. A., and Wingfield, J. C. (1994). Gender and seasonal differences in the adrenocortical response to ACTH challenge in an arctic passerine, Zonotricia leucophrys gambelii. Gen. Comp. Endocrinol. 94:33–44.

    Article  PubMed  CAS  Google Scholar 

  • Barnard, C. J., Behnke, J. M., and Sewell, J. (1994). Social behaviour and susceptibility to infection in house mice (Mus musculus): Effects of group size, aggressive behaviour and status-related hormonal responses prior to infection on resistance to Babesia microti. Parasitology 108:487–496.

    Article  PubMed  CAS  Google Scholar 

  • Benton, W. P. M., Wunderlick, F., and Mossmann, H. (1992). Testosterone-induced suppression of self-healing Plasmodium chabaudi malaria: An effect not mediated by androgen receptors? J. Endocrinol. 135:407–413.

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Cox, F. E. G. (1993). Immunology. In: Modern parasitology. F. E. G. Cox, ed. Oxford: Blackwell Scientific Publications. 193–218.

    Chapter  Google Scholar 

  • Clayton, D. H. (1991). The influence of parasites on host sexual selection. Parasitol Today. 7:329–334.

    Article  PubMed  CAS  Google Scholar 

  • Clayton, D. H., Pruett-Jones, S. G., and Lande, R. (1992). Reappraisal of the interspecific prediction of parasite-mediated sexual selection: Opportunity knocks. J. Theor. Biol. 157:95–108.

    Article  Google Scholar 

  • De Vaney, J. A., Elissalde, M. H., Steel, E. G., Hogan, B. F., and Del var Petersen, H. (1977). Effect of the Northern fowl mite Ornithonyssus sylviarum on White Leghorn roosters. Poult. Sci. 56:1585–1590.

    Article  Google Scholar 

  • Deviche, P., Balthazart, J., Malacare, G., and Hendrick, J. C. (1982). Effects of in vitro corticosterone treatment on the metabolism of testosterone in the comb and brain of the young male chicken. Gen. Comp. Endocrinol. 48:398–402.

    Article  PubMed  CAS  Google Scholar 

  • Dunlap, K. P., and Schall, J. J. (1995). Hormonal alterations and reproductive inhibition in male fence lizards (Sceloporus occidentalis) infected with the malarial parasite Plasmodium mexicanum. Physiol. Zool. 68:608–621.

    CAS  Google Scholar 

  • Fleming, M. W. (1985). Steroidal enhancement of growth in parasitic larvae of Acaris suum: Validation of a bioassey. J. Exp. Zool. 233:229–233.

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Fowles, J. R., Fairbrother, A., Fix, M, Schiller, S., and Kerkvliet, N. I. (1993). Glucocorti coid effects on natural and humoral immunity in mallards. Dev. Comp. Immunol. 17:165–177.

    Article  PubMed  CAS  Google Scholar 

  • Friedlander, R. C., Olsen, L. D., and McCune, E. L. (1992). Comparative susceptability of caponized and uncaponized torn turkeys to Pasteurella multicodia. Avian Dis. 10:97–100.

    Article  Google Scholar 

  • Garrido, E., Gomariz, R. P., Lecata. J, and Zapata, A. (1989) Different sensitivity to the dexamethasone treatment of the lymphoid organs of Ranaperezi in two different seasons. Dev. Comp. Immunol. 13:57–64.

    Article  PubMed  CAS  Google Scholar 

  • Gause, W. C., and Marsh, J. A. (1986). Effect of testosterone treatments for varying periods on autoimmune development and on specific infiltrating leukocyte populations in the thyroid gland of obese strain chickens. Clin. Immunol. Immunopathol. 39:464–478.

    Article  PubMed  CAS  Google Scholar 

  • Glick, B. (1986). Immunophysiology. In Avian physiology (P. D. Sturkie, ed.), pp. 87–101. New York: Springer-Verlag.

    Chapter  Google Scholar 

  • Greenburg, N., and Wingfield, J. C. (1987). Stress and reproduction: Reciprocal relation ships. In Hormones and reproduction in fishes, amphibians and reptiles (D. O. Norris and R. E. Jones, eds.), pp. 389–426. New York: Plenum.

    Google Scholar 

  • Grossman, C. J. (1990). Are there underlying immune-neuroendocrine interactions respon sible for immunological sexual dimorphism? Prog. NeuroEndocrinlmmunol. 3:75–82.

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Gustafsson, L., Nordling, D., Andersson, M. S., Sheldon, B. C., and Qvarnstrom, A. (1994). Infectious diseases, reproductive effort and the cost of reproduction in birds. Phil. Trans. R. Soc. Lond. B. Biol. Sci. 260:323–331.

    Google Scholar 

  • Hamilton, W. D., and Zuk, M. (1982). Heritable true fitness and bright birds: A role for parasites? Science 218:384–387.

    Article  PubMed  CAS  Google Scholar 

  • Harder, A. (1992). Effects of testosterone on Heterakis spumosa infections in mice. Parasitology 105:335–342.

    Article  PubMed  CAS  Google Scholar 

  • Harder, A., Danneschewski, A., and Wunderlick, F. (1994). Genes of the mouse H-2 complex control the efficacy of testosterone to suppress immunity against the intestinal nematode Heterakis spumosa. Parasitol. Res. 80:446–8.

    Article  PubMed  CAS  Google Scholar 

  • Hausfauter, G., Gerhardt, H. C., and Klump, G. M. (1990). Parasites and mate choice in green treefrogs, Hyla versicolor. Am. Zool. 30:299–312.

    Google Scholar 

  • Hill, G. E. (1991). Plumage coloration is a sexually selected indicator of male quality. Nature (Lond.) 350:337–339.

    Article  Google Scholar 

  • Hillgarth, N. (1990). Parasites and female choice in the ring-necked pheasant. Am. Zool. 30:227–233.

    Google Scholar 

  • Hillgarth, N., and Wingfield, J. C. (1997). Parasite-mediated sexual selection: Endocrine aspects. In Host-parasite evolution: General principles and avion models (D. Clayton and J. E. Moore, eds.), pp. 78–104. Oxford: Oxford University Press.

    Google Scholar 

  • Hirota, Y., Suzuki, Y., Chazono, Y., and Bito, Y. (1976). Humoral immune responses characteristic of testosterone-oropionate-treated chickens. Immunology 30:341–348.

    PubMed  CAS  Google Scholar 

  • Horton, J. D., Amphibians. (1994). In Immunology: A comparative approach (R. J. Turner, ed.) pp. 101–136. Chichester: Wiley.

    Google Scholar 

  • Isserhoff, H., Sylvester, P. W., and Held, W. A. (1986). Effects of Schistosoma mansoni on androgen regulated gene expression in the mouse. Mol. Biochem. Parasitol. 18:401–412.

    Article  Google Scholar 

  • Jurd, R. D. (1994). Reptiles and birds. In Immunology: a comparative approach (R. J. Turner, ed.), pp. 137–172. Chichester: Wiley.

    Google Scholar 

  • Kirkpatrick, M., and Ryan, M. J. (1991). The evolution of mating preferences and the paradox of the lek. Nature (Lond.) 350:33–38.

    Article  Google Scholar 

  • Lehmann, D., Siebold, K., Emmons, L. R., and Muller, H. J. (1988). Androgens inhibit proliferation of human peripheral blood lymphocytes in vitro. Clin. Immunol. Immunopathol. 46:122–128.

    Article  PubMed  CAS  Google Scholar 

  • Manning, M. J. (1994). Fishes. In Immunology: A comparative approach. (R. J. Turner, ed.) pp. 69–100. Chichester: Wiley.

    Google Scholar 

  • Marsh, J. A., and Scanes, C. G. (1994). Neuroendocrine-immune interactions. Poult. Sci. 73:1049–1061.

    Article  PubMed  CAS  Google Scholar 

  • McLennan, D. A., and Brooks, D. R. (1991). Parasites and sexual selection: A macroevolu tionary perspective. Quart. Rev. Biol. 66:255–286.

    Article  PubMed  CAS  Google Scholar 

  • McMinn, H. (1990). Effects of the nematode parasite Camallanus cotti on the sexual and non-sexual behaviors in the guppy (Poecilia reticulata). Am. Zool. 30:245–249.

    Google Scholar 

  • Milinski, M., and Bakker, T. C. M. (1990). Female sticklebacks use male coloration in mate choice and hence avoid parasitised males. Nature (Lond.) 344:330–333.

    Article  Google Scholar 

  • Møller, A. P. (1988). Female choice selects for male sexual tail ornaments in the monoga mous swallow. Nature (Lond.) 332:640–642.

    Article  Google Scholar 

  • Møller, A. P. (1990). Parasites and sexual selection: current status of the Hamilton and Zuk hypothesis.J. Evol. Biol. 3:319–328.

    Article  Google Scholar 

  • Møller, A. P. (1991). Parasites, sexual ornaments and mate choice in the barn swallow. In Bird-parasite interactions, ecology, evolution and behaviour (J. E. Loye and M. Zuk, eds.) pp. 328–343. Oxford: Oxford University Press.

    Google Scholar 

  • Norris, K., Anwar, M., and Read, A. F. (1994). Reproductive effort influences the preva lence of haematozoan parasites in great tits. J. Anim. Ecol. 63:601–610.

    Article  Google Scholar 

  • Owens, I. P. E., and Short, R. V. (1995). Hormonal basis for sexual dimorphism in birds: implications for new theories of sexual selection. Trends Ecol. Evol. 10:44–47.

    Article  PubMed  CAS  Google Scholar 

  • Petrie, M., Halliday, T., and Sanders, C. (1991). Peahens prefer peacocks with elaborate trains. Anim. Behav. 41:323–331.

    Article  Google Scholar 

  • Potts, W. K., and Wakeland, E. K. (1993). Evolution of MHC genetic diversity: A tale of incest, pestilence and sexual preference. Trends Genet. 9:408–412.

    Article  PubMed  CAS  Google Scholar 

  • Read, A. F. (1990). Parasites and the evolution of host sexual behavior. In Parasitism and Host Behaviour (C. J. Barnard and J. M. Behnke, eds.), pp. 78–99. London: Taylor and Francis.

    Google Scholar 

  • Read, A. F., and Harvey, P. H. (1989). Reassessment of comparative evidence for Hamilton and Zuk theory on the evolution of secondary sexual characters. Nature (Lond.) 339:618–620.

    Article  Google Scholar 

  • Redig, P. T., Dunnette, J. L., Mauro, L., Sivanandan, V., and Markham, F. (1985). The in vitro response of turkey lymphocytes to steroid hormones. Avian Dis. 29:373–383.

    Article  PubMed  CAS  Google Scholar 

  • Ressell, S., and Schall, J. J. (1989). Parasites and showy males. Malarial infection and color variation in fenze lizards. Oecologica, 78:158–64.

    Article  Google Scholar 

  • Roitt, I. M. (1994). Essential immunology. Oxford: Blackwell Scientific.

    Google Scholar 

  • Roitt, I. M., Brostoff, J., and Male, D. K. (1993). Immunology. London: Mosby.

    Google Scholar 

  • Saad, A. H., Khalek, N. A., and El Ridi, R. (1990). Blood testosterone level: A season dependent factor regulating immune reactivity in lizards. Immunobiology 180:184–194.

    Article  PubMed  CAS  Google Scholar 

  • Slater, C. H., and Schreck, C. B. (1993). Testosterone alters the immune response of chinook salmon Oncorhynchus tshawytscha. Gen. Comp. Endocrinol. 89:291–298.

    Article  PubMed  CAS  Google Scholar 

  • Spindler, K. D. (1988). Parasites and hormones. In Parasitology in focus (H. Mehlhorn and D. Bunnag, eds.) pp. 134–148.

    Google Scholar 

  • Staples, L. D., Binnes, R. M., and Heap, R. B. (1983). Influences of certain steroids on lymphocyte transformation in sheep and goats studied in vitro. J. Endocrinol. 98:55–69.

    Article  PubMed  CAS  Google Scholar 

  • Sullivan, B. K., (1991). Parasites and sexual selection: Separating causes and effects. Herpetologica. 47:250–264.

    Google Scholar 

  • Talal, N. (1992). In Encyclopedia of immunology (I. M. Roitt and P. J. Delves, eds.), pp. 1112–1114. London: Academic Press.

    Google Scholar 

  • Tinsley, R. C. (1990). The influence of parasite infection on mating success in spadefoot toads, Scaphiopus couchii. Am. Zool. 30:313–325.

    Google Scholar 

  • Turner, R. J. Mammals. (1994). In Immunology: A comparative approach. (R. J. Turner, ed.) pp. 173–214. Chichester: Wiley.

    Google Scholar 

  • Wakelin, D., and Appanus, V. (1997). Genetic control of immune responses. In Host parasite evolution: General principles and avion models (D. Clayton and J. E. Moore, eds.), pp. 30–58. Oxford: Oxford University Press.

    Google Scholar 

  • Wedekind, C. (1992). Detailed information about parasites revealed by sexual ornamentation. Proc. R. Soc. of Lond. BioL Sci. 247:169–174.

    Article  Google Scholar 

  • Wedekind, C. (1994). Mate choice and maternal selection for specific parasite resistences before, during and after fertilization. Proc. R. Soc. of Lond. Biol. Sci. 249:303–311.

    Article  Google Scholar 

  • Wedekind, C., and Folstad, I. (1994). Adaptive or non-adaptive immunosuppression by sex hormones? Am. Nat. 143:936–938.

    Article  Google Scholar 

  • Wingfield, J. C. (1990). Interrelationships of androgens, aggression, and mating systems. In Endocrinology of birds: Molecular to behavioral (M. Wada, S. Ishii, and C. G. Scanes, eds.) pp. 187–205. Tokyo: Japan Scientific Societies Press/Berlin: Springer-Verlag.

    Google Scholar 

  • Wingfield, J. C. (1994). Modulation of the adrenocortical response to stress in birds. In Perspectives in comparative endocrinology (K. G. Davey, R. E. Peter, and S. S. Tobe, eds.) pp. 1012–1022. Canada: National Research Council.

    Google Scholar 

  • Wingfield, J. C., Whaling, C. S., and Marier, P. (1994). Communication in vertebrate aggression and reproduction: the role of hormones. In The physiology of reproduction (E. Knobil and J. D. Neill, eds.) pp. 303–342. New York: Raven Press.

    Google Scholar 

  • Wingfield, J. C., Hegner, R. E., Dufty, A. M., and Ball, G. F. (1990). The “Challenge Hypothesis”: Theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am. Nat. 136:829–846.

    Article  Google Scholar 

  • Zapata, A. G., Varas, A., and Torroba, M. (1992). Seasonal variations in the immune system of lower vertebrates. Immunol. Today. 113:142–147.

    Article  Google Scholar 

  • Zuk, M. (1992). The role of parasites in sexual selection: current evidence and future directions. Adv. Study Behav. 21:39–68.

    Article  Google Scholar 

  • Zuk, M., Thornhill, R., Ligon, J. D., and Johnson, K. (1990). Parasites and mate choice in red jungle fowl. Am. Zool. 30:235–244.

    Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1997 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Hillgarth, N., Wingfield, J.C. (1997). Testosterone and Immunosuppression in Vertebrates: Implications for Parasite-Mediated Sexual Selection. In: Beckage, N.E. (eds) Parasites and Pathogens. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-5983-2_7

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-5983-2_7

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-7742-9

  • Online ISBN: 978-1-4615-5983-2

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics