Yolk androgens and the development of avian immunity: an experiment in jackdaws (Corvus monedula)

Abstract

SUMMARYMaternally derived androgens have been shown to influence offspring phenotype in various ways. In birds, the benefits of prenatal androgen exposure, such as increased competitiveness and accelerated growth in nestlings, have been suggested to be balanced by costs, such as reduced immune function. In this study, we used an integrative approach to examine the influence of yolk androgens on the development of immune function in jackdaw (Corvus monedula) nestlings. Specifically, we tested whether the effects of yolk androgens on offspring immunity may extend over the first few days of life and be detectable even after several weeks. We manipulated yolk androgen concentrations in jackdaw eggs and estimated immune responsiveness by challenging the young with different pathogens at different stages of the nestling period. Six-day-old chicks hatched from eggs with elevated yolk androgen levels had lower pre-challenge antibody titres against lipopolysaccharide (LPS) than control chicks. However, antibody titres against LPS did not differ between treatment groups eight days after a challenge with LPS. During the late nestling phase, both humoral (towards diphtheria/tetanus antigens) and cell-mediated (towards phytohaemagglutinin) immune responsiveness were lower in chicks from yolk androgen-treated eggs compared with control chicks. Our experimental study on jackdaw chicks shows that elevated yolk androgen levels result in a general immunosuppression in offspring; this conclusion was based on results for several immunological tests of both humoral and cell-mediated immunity conducted at 1-2 and 3-4 weeks of age.

Experimentally increased in ovo testosterone leads to increased plasma bactericidal activity and decreased cutaneous immune response in nestling house wrens

“…Such effects include suppression of immune responsiveness, at least in the short term, when in ovo testosterone is experimentally increased (e.g. Müller et al, 2005;Navara et al, 2005;Sandell et al, 2009) and when natural variation in nestling testosterone is examined (López-Rull et al, 2010). The underlying cause of immune suppression by yolk testosterone may be a trade-off between resources allocated to two energetically expensive physiological tasks: growth (increased by androgens) and immune-system use and maintenance (decreased by androgens) (Sheldon and Verhulst, 1996;Lochmiller and Deerenberg, 2000); however, this has by no means been clearly established as the sole cause (reviewed in Groothuis et al, 2005;Gil, 2008).…”

Sex-Specific Effects of High Yolk Androgen Levels on Constitutive and Cell-Mediated Immune Responses in Nestlings of an Altricial Passerine

“…For instance, cell-mediated and humoral immunity were found to be reduced in black-headed gull chicks (Larus ridibundus) that had been exposed to high levels of androgens in the egg (Groothuis et al 2005a;Müller et al 2005). A similar reduction in both branches of the immune system was found in jackdaws (Corvus monedula; Sandell et al 2009). In the same line, experimentally infected house martins (Delichon urbica) and great tits (Parus major) laid eggs with lower androgen levels than control birds (Tschirren et al 2004;Gil et al 2006), although a recent study failed to find an effect after a similar experimental approach (Heylen et al 2012).…”

“…Indeed, theory predicts that benefits derived from high androgen levels are counteracted by negative effects on immunity (Folstad and Karter 1992). In the case of yolk androgen levels, several studies have found support for this hypothesis, in both the cellular and humoral axes of immunity (Müller et al 2005;Groothuis et al 2008;Sandell et al 2009). However, other studies have found no effects (Rubolini et al 2006b) or conflicting evidence.…”

“…Thus, our results show that immunosuppression resulting from high yolk androgen levels affected components of both the innate and adaptive axes of the immune system in males. Yolk androgens may prime the development and expression of various components of the immune system, such as cell-mediated and humoral immune function, differently (Sandell et al 2009), with sex-and context-specific consequences (Pigeon et al 2013). Immunosuppression due to high androgen levels could make individuals more susceptible to disease.…”

Immune responses link parasite genetic diversity, prevalence and plumage morphs in common buzzards

“…The mean age of the nestlings was 18 days (10-26). After taking a plasma sample at primary sampling, we injected naïve nestlings with 200 ll of tetanus-diphtheria vaccine (Mérieux, 500 ll containing 20 IE tetanus and 2 IE diphtheria toxoids) in the pectoral muscle (Råberg et al 2000;Sandell et al 2009). Seven days later, the nests were climbed again, and a second blood sample was taken, from which plasma was extracted and stored at -20°C.…”