How a territorial challenge changes sex steroid-related gene networks in the female brain: A field experiment with the tree swallow

Territorial competition can stimulate secretion of testosterone (T), which is thought to act on neural circuits of aggression to promote further aggression. Here, we test the hypothesis that competition modulates sex steroid sensitivity and conversion in the brain, focused on the female tree swallow (Tachycineta bicolor). In this bird species, exogenous T enhances female aggression, but social competition for limited nesting territories does not stimulate systemic T elevation. We exposed free-living females to simulated territorial intrusions and sampled five regions of the vertebrate social behavior network (SBN). Using quantitative PCR, we measured mRNA abundance of: androgen receptor, 5-alpha reductase, estrogen receptor alpha, and aromatase. Using standard analyses, we found essentially no treatment effect on mRNA abundance in any one brain area; however, network analyses revealed marked socially-induced changes in gene co-expression across the SBN. After a territorial challenge, gene expression was more positively correlated with T, and genes specific to the androgen-signaling pathway were also more positively correlated with one another. The challenged brain also exhibited stronger negative correlations among genes in the nucleus taeniae, but stronger positive correlations between the lateral septum and bed nucleus of the stria terminalis. Together, these findings suggest that, in response to female-female territorial challenges, T acts on androgen-mediated circuits of aggression, with some divergence in gene regulation in the nucleus taeniae. The post-transcriptional consequences of these shifts require more research, but their existence underscores insights to be gained from analyzing the neuroendocrine properties of the SBN using network-level perspectives.