Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks
- PMID: 16191605
- PMCID: PMC1559883
- DOI: 10.1098/rspb.2005.3178
Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks
Abstract
Avian eggs contain considerable amounts of maternal yolk androgens, which have been shown to beneficially influence the physiology and behaviour of the chick. As androgens may suppress immune functions, they may also entail costs for the chick. This is particularly relevant for colonial species, such as the black-headed gull (Larus ridibundus), in which the aggregation of large numbers of birds during the breeding season enhances the risk of infectious diseases for the hatching chick. To test the effect of maternal yolk androgens on the chick's immune function, we experimentally manipulated, in a field study, yolk androgen levels within the physiological range by in ovo injection of either androgens (testosterone and androstenedione) or sesame oil (control) into freshly laid eggs. We determined cell-mediated immunity (CMI) and humoral immunity of the chicks at the beginning of the nestling period to evaluate early modulatory effects of yolk androgens on immune function. Embryonic exposure to elevated levels of androgens negatively affected both CMI and humoral immunity in nestling gull chicks. Consequently, maternal yolk androgens not only entail benefits of enhanced competitiveness and growth as previously shown, but also costs in terms of immunosuppression. The outcome of embryonic yolk androgen exposure thus likely depends on the post-hatching circumstances for the developing offspring such as parasite exposure and degree of sibling competition.
Figures
Similar articles
-
Yolk androgens and the development of avian immunity: an experiment in jackdaws (Corvus monedula).J Exp Biol. 2009 Mar;212(Pt 6):815-22. doi: 10.1242/jeb.022111. J Exp Biol. 2009. PMID: 19251998
-
Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development.Proc Biol Sci. 2001 Apr 22;268(1469):839-46. doi: 10.1098/rspb.2001.1594. Proc Biol Sci. 2001. PMID: 11345330 Free PMC article.
-
Balancing between costs and benefits of maternal hormone deposition in avian eggs.Biol Lett. 2005 Mar 22;1(1):78-81. doi: 10.1098/rsbl.2004.0233. Biol Lett. 2005. PMID: 17148133 Free PMC article.
-
Yolk androgens as pleiotropic mediators of physiological processes: a mechanistic review.Comp Biochem Physiol A Mol Integr Physiol. 2008 Aug;150(4):378-86. doi: 10.1016/j.cbpa.2008.05.002. Epub 2008 May 9. Comp Biochem Physiol A Mol Integr Physiol. 2008. PMID: 18550405 Review.
-
Orchestration of avian reproductive effort: an integration of the ultimate and proximate bases for flexibility in clutch size, incubation behaviour, and yolk androgen deposition.Biol Rev Camb Philos Soc. 2006 Nov;81(4):629-66. doi: 10.1017/S1464793106007147. Epub 2006 Oct 12. Biol Rev Camb Philos Soc. 2006. PMID: 17038202 Review.
Cited by
-
Effects of maternal androgens and their metabolite etiocholanolone on prenatal development in birds.J Exp Biol. 2024 Aug 1;227(15):jeb247205. doi: 10.1242/jeb.247205. Epub 2024 Aug 5. J Exp Biol. 2024. PMID: 39037123 Free PMC article.
-
Elevated third trimester corticosteroid levels are associated with fewer offspring infections.Sci Rep. 2023 Jun 28;13(1):10461. doi: 10.1038/s41598-023-36535-0. Sci Rep. 2023. PMID: 37380711 Free PMC article.
-
Perinatal androgens organize sex differences in mast cells and attenuate anaphylaxis severity into adulthood.Proc Natl Acad Sci U S A. 2020 Sep 22;117(38):23751-23761. doi: 10.1073/pnas.1915075117. Epub 2020 Sep 11. Proc Natl Acad Sci U S A. 2020. PMID: 32917815 Free PMC article.
-
Maternal effects and urbanization: Variation of yolk androgens and immunoglobulin in city and forest blackbirds.Ecol Evol. 2020 Feb 4;10(4):2213-2224. doi: 10.1002/ece3.6058. eCollection 2020 Feb. Ecol Evol. 2020. PMID: 32128150 Free PMC article.
-
Racial Differences in Immunological Landscape Modifiers Contributing to Disparity in Prostate Cancer.Cancers (Basel). 2019 Nov 25;11(12):1857. doi: 10.3390/cancers11121857. Cancers (Basel). 2019. PMID: 31769418 Free PMC article. Review.
References
-
- Al-Afaleq A.I, Homeida A.M. Effects of low doses of oestradiol, testosterone and dihydrotestosterone on the immune response of broiler chicks. Immunopharmacol. Immunotoxicol. 1998;20:315–327. - PubMed
-
- Andersson J, Sjöberg O, Möller G. Induction of immunoglobulin and antibody synthesis in vitro by lipopolysaccharides. Eur. J. Immunol. 1972;2:349–353. - PubMed
-
- Andersson J, Coutinho A, Melchers F. Stimulation of murine B lymphocytes to IgG synthesis and secretion by the mitogens lipopolysaccharide and lipoprotein and its inhibition by anti-immunoglobulin antibodies. Eur. J. Immunol. 1978;8:336–343. - PubMed
-
- Andersson S, Uller T, Lõhmus M, Sundström F. Effects of yolk testosterone on growth and immunity in a precocial bird. J. Evol. Biol. 2004;17:501–505. - PubMed
-
- Apanius V. Ontogeny of immune function. In: Starck J.M, Ricklefs R.E, editors. Avian growth and development—evolution within the altricial–precocial. ch. 8. Oxford University Press; 1998. pp. 203–222.
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Research Materials