Neural sensitivity to sex steroids predicts individual differences in aggression: implications for behavioural evolution

Abstract

Testosterone (T) regulates many traits related to fitness, including aggression. However, individual variation in aggressiveness does not always relate to circulating T, suggesting that behavioural variation may be more closely related to neural sensitivity to steroids, though this issue remains unresolved. To assess the relative importance of circulating T and neural steroid sensitivity in predicting behaviour, we measured aggressiveness during staged intrusions in free-living male and female dark-eyed juncos (Junco hyemalis). We compared aggressiveness to plasma T levels and to the abundance of androgen receptor (AR), aromatase (AROM) and oestrogen receptor alpha (ORa) mRNA in behaviourally relevant brain areas (avian medial amygdala, hypothalamus and song control regions). We also asked whether patterns of covariation among behaviour and endocrine parameters differed in males and females, anticipating that circulating T may be a better predictor of behaviour in males than in females. We found that circulating T related to aggressiveness only in males, but that gene expression for ORa, AR and AROM covaried with individual differences in aggressiveness in both sexes. These findings are among the first to show that individual variation in neural gene expression for three major sex steroid-processing molecules predicts individual variation in aggressiveness in both sexes in nature. The results have broad implications for our understanding of the mechanisms by which aggressive behaviour may evolve.

To flock or fight: Neurochemical signatures of divergent life histories in sparrows

“…Thus, because male-male interactions typically elevate levels of testosterone (2), we must consider that any positive correlations between neurochemistry and behavior may be the product of male-male interactions and not the cause of it. For instance, ARO gene expression correlates positively with both aggression and plasma T in juncos (40). Nonetheless, most of the strongest relationships described here for neurochemistry and aggression are negative.…”

Estrogen receptor α polymorphism in a species with alternative behavioral phenotypes

“…This result strongly suggests that sensitivity to plasma steroid manipulations differs between the morphs. Other authors have suggested that steroid-sensitive behaviors are often better correlated with steroid receptors than with plasma steroid levels (10,11,(32)(33)(34). In dark-eyed juncos (Junco hyemalis), a relative of white-throated sparrows, aggressive responses to STI were positively correlated with ERα mRNA expression in the ventral telencephalon, which contains MeA, and negatively correlated with it in the hypothalamus (11).…”

“…Morph differences in behavior cannot be entirely explained by these hormones, however, because the differences persist even when plasma levels are experimentally equalized (9). Individual variation in steroid-dependent behavior may be better explained by neural sensitivity to the hormones, for example by variation in the distribution and abundance of steroid receptors (10,11).…”

Mates of Competitive Females: The Relationships between Female Aggression, Mate Quality, and Parental Care

“…Junco females vary in their level of same-sex aggression and maternal care [3,11,21,[36][37][38][39][40][41]. Aggressive females spend less time brooding and in some years produce smaller eggs, but provision more frequently [11].…”