Aggressive interactions rapidly increase androgen synthesis in the brain during the non-breeding season

Abstract

In male song sparrows (Melospiza melodia), territorial challenges during the breeding season can rapidly increase circulating levels of testosterone (T). During the non-breeding season, male song sparrows are highly aggressive, but the gonads are regressed and plasma T levels are non-detectable and unaffected by territorial challenges. The pro-hormone dehydroepiandrosterone (DHEA) is elevated in song sparrow plasma and brain during the non-breeding season and may be locally converted to sex steroids in the brain to regulate aggression. The enzyme 3β-hydroxysteroid dehydrogenase/Δ5-Δ4 isomerase (3β-HSD) converts DHEA to androstenedione (AE) using the cofactor NAD+, and this is a critical rate-limiting step. We predicted that brain 3β-HSD activity varies seasonally and is rapidly modulated by aggressive challenges. In the first study, brain 3β-HSD activity was highest in the non-breeding season in specific regions. In the second study, a simulated territorial challenge rapidly increased aggressive behavior in non-breeding song sparrows. Brain 3β-HSD activity, when measured without exogenous NAD+, increased by ∼250 to 500% in telencephalic regions of challenged subjects. When brain 3β-HSD activity was measured with exogenous NAD+, these effects of territorial challenges were not observed. These data suggest that territorial challenges rapidly increase endogenous NAD+levels or increase 3β-HSD activity specifically within a NAD-rich subcellular compartment. Together, these two studies suggest a shift from systemic to local sex steroid signaling in the non-breeding season. Local steroid signaling produces high spatial and temporal specificity of steroid signals and avoids the costs of high systemic T levels during the non-breeding season.

The agonistic adrenal: melatonin elicits female aggression via regulation of adrenal androgens

“…Further, these findings demonstrate a key role of melatonin in regulating both peripheral androgens and aggression in females; this is the first finding of a direct action of melatonin on adrenal DHEA release. This peripheral mechanism provides an alternative to the previously described actions of gonadal steroids acting on the brain to regulate behaviour [17,18], and described actions of DHEA regulating aggression [7,16,33,41]. From a comparative perspective, this seasonal mechanism may also regulate aggression in other vertebrate species, including frogs, lizards, mammals and snakes, where melatonin also facilitates seasonal changes ( [20][21][22][23]; reviewed in [7]).…”

“…In song sparrows that exhibit year-round territorial aggression, DHEA serves as a critical regulator of aggression when sex steroids are low [16,33]. These non-gonadal mechanisms of aggression are likely shared across vertebrates.…”

A mechanism for rapid neurosteroidal regulation of parenting behaviour

“…This local mechanism of neural steroidogenesis could be advantageous for the speed of action, thus reducing the inappropriate expression of behaviour in unpredictable environments. Although our study focused on the role of neural 11b-HSD in regulating parenting, we suggest that this mechanism of local regulation could have broad importance in the context of other enzymes, such as aromatase, 5b-reductase and 3b-hydroxysteroid dehydrogense and other classes of social behaviour [17,20,21,23].…”

“…In many species, neural steroidogenic enzymes are sensitive to changes in seasons [20], life history stages [21,22] and sexual behaviour [23]. Neural steroidogenic enzyme expression also varies during territory acquisition, courtship and parenting [15,22].…”

Up to the challenge? Hormonal and behavioral responses of free-ranging male Cassin's Sparrows, Peucaea cassinii, to conspecific song playback

“…Rather, it seems that neural signaling mechanisms may control rapid changes in aggressive behavior, such as those induced by STI. Support for this proposition is provided by recent research in non-breeding Song Sparrows, Melospiza melodia, demonstrating that exposure to STI stimulates the brain conversion of the prohormone dehydroepiandrosterone to androstenedione (Pradhan et al, 2010). Estradiol acts centrally to mediate many behavioral effects of T (e.g., Callard, 1989, 1990) and in the Whitecrowned Sparrow, Zonotrichia leucophrys, stimulation of aggressive behavior by STI is associated with rapid changes in concentration of estrogen and aromatase, the enzyme that converts androgens into estrogens, in discrete brain regions (Charlier et al, 2011).…”