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

Abstract

Avian embryos are exposed to yolk androgens that are incorporated into the egg by the ovulating female. These steroids can affect several aspects of embryo development, often resulting in increases in overall size or the speed of growth of different traits. However, several studies suggest that they also entail immune costs to the offspring. In this study, we explored whether variation in yolk androgen concentration affected several measures of the constitutive and cell-mediated immune axes in the spotless starling (Sturnus unicolor). Using a within-brood design, we injected different doses of androgens (testosterone and androstenedione) into the eggs. Our study showed that experimentally increased yolk androgens led to sex-specific immunosuppression in both the innate and adaptive axes of the immune system. Both cell-mediated immune response (CMI) and lysozyme activity decreased with increasing androgen levels injected into the egg in the case of male nestlings, whereas there were no effects on females. The effects that we found were always linear: no quadratic or threshold patterns were detected. We found no effects of the experimental treatment in hemolysis or agglutination capacity, but these measures were negatively correlated with CMI, suggesting negative correlation among different branches of the immune system. Blood (trypanosomes and hemosporidians) and intestinal (coccidia) parasites were not affected by the experimental increase of yolk androgen levels. Our results show that in our study species yolk androgens induce immunosuppression in some axes of the male nestling immune system. Further studies should analyze the proximate causes for these contrasting effects in different axes of the immune system and the reason for the differential impact on males and females.

Harsh conditions during early development influence telomere length in an altricial passerine: Links with oxidative stress and corticosteroids

“…Of two previous studies manipulating breeding stress in the closely related European starling ( Sturnus vulgaris ), one found that negative effects were restricted to female offspring (Rowland, Love, Verspoor, Sheldon, & Williams, ), whereas the other study found negative effects in males (Nettle et al., ). Although this discrepancy does not allow us to derive a general conclusion, it does underline the fact that the two sexes tend not to respond equally to developmental stressors (Muriel et al., ).…”

“…The fact that only females responded with higher corticosterone levels could be explained by their smaller size, which probably results in a lower competitive ability to access food from parents (Oddie, ). It is often found that sexes differ in environmental sensitivity to stressors (Muriel, Perez‐Rodriguez, Ortiz‐Santaliestra, Puerta, & Gil, ), but a large meta‐analysis has shown that there are no general patterns across animals in relation to sex or size (Jones et al., ). Most likely, the phenomenon is specific to different taxonomic groups and is possibly explained by differences in their developmental mode.…”

Yeast β-Glucan Altered Intestinal Microbiome and Metabolome in Older Hens

“…Antioxidant, antiviral, and anti-inflammatory activities were contributed by several metabolites (13,16-docosadienoic acid, erucic acid, eicosadienoic acid, and 5Z,8Z,11Z,14Z,17Z-eicosapentaenoic acid) engaged in the biosynthesis of the unsaturated fatty acid pathway (Weldon et al, 2007;Chen et al, 2020;Liang et al, 2020). Immunosuppressive effects were manifested by the metabolites (androstenedione, 5-androstene-3, 17-dione, testosterone, 5-α-androstane-3, 17-dione, dehydroepiandrosterone, and 3,4-dihydroxy-9,10-secoandrosta-1,3,5(10)-triene-9,17-dione) pertaining to steroid degradation (Muriel et al, 2017). The adhesion of flagellum, biofilm formation, virulence factor gene transcription, and production of toxins of bacteria are affected by bacterial pheromones (N-hexanoyl-l-homoserine lactone, N-heptanoylhomoserine lactone, and N-octanoyl-l-homoserine lactone) involved in the quorum-sensing pathway, thereby directly promoting the infection by pathogens (Yang et al, 2013;Li et al, 2018).…”

Prenatal manipulation of yolk androgen levels affects egg size but not egg colour in a songbird

“…on the immune system (e.g. the cell-mediated immune response, Muriel et al 2017) or on the resistance to oxidative stress (Alonso-Alvarez et al 2017). Following the logic of previous research on androgen associated trade-offs (Folstad and Karter 1992), it has been suggested that there may be similar tradeoffs between costs and benefits of maternal androgens (Groothuis et al 2005;Muriel et 7 al.…”

“…To our knowledge, no study to date has covered the entire lifespan of individuals. Still, these kind of studies are decisive to evaluate the overall effects of maternal hormones on fitness and their adaptive role, especially in the perspective of their sex-specific activity (Muriel et al 2017). Although the strength and direction of effects vary depending on the species, many of the studies involving egg-androgen manipulation suggest that female nestlings do not benefit from elevated androgen levels, whereas males do (Saino et al 2006;von Engelhardt et al 2006;Ruuskanen and Laaksonen 2010;Muriel et al 2015bMuriel et al , 2017.…”