Testosterone, signal coloration, and signal color perception in male zebra finch contests.

Many animals use assessment signals to resolve contests over limited resources while minimizing the costs of those contests. The carotenoid-based orange to red bills of male zebra finches (Taeniopygia guttata) are thought to function as assessment signals in male-male contests, but behavioral analyses relating contest behaviors and outcomes to bill coloration have yielded mixed results. We examined the relationship between bill color and contests while incorporating measurements of color perception and testosterone (T) production, for an integrative view of aggressive signal behavior, production, and perception. We assayed the T production capabilities of 12 males in response to a gonadotropin-releasing hormone (GnRH) challenge. We then quantified the initiation, escalation, and outcome of over 400 contests in the group, and measured bill color using calibrated photography. Finally, because signal perception can influence signal function, we tested how males perceive variation in bill coloration, asking if males exhibit categorical perception of bill color, as has been shown recently in female zebra finches. The data suggest that males with greater T production capabilities than their rivals were more likely to initiate contests against those rivals, while males with redder bills than their rivals were more likely to win contests. Males exhibited categorical color perception, but individual variation in the effect of categorical perception on color discrimination abilities did not predict any aspects of contest behavior or outcomes. Our results are consistent with the hypotheses that T plays a role in zebra finch contests and that bill coloration functions as an aggressive signal. We suggest future approaches, based on animal contest theory, for how links among signals, perception, and assessment can be tested.

Evaluating testosterone as a phenotypic integrator: From tissues to individuals to species.

Hormones have the potential to bring about rapid phenotypic change; however, they are highly conserved over millions of years of evolution. Here, we examine the evolution of hormone-mediated phenotypes, and the extent to which regulation is achieved via independence or integration of the many components of endocrine systems. We focus on the sex steroid testosterone (T), its cognate receptor (androgen receptor) and related endocrine components. We pose predictions about the mechanisms underlying phenotypic integration, including coordinated sensitivity to T within and among tissues and along the HPG axis. We then assess these predictions with case studies from wild birds, asking whether gene expression related to androgenic signaling naturally co-varies among individuals in ways that would promote phenotypic integration. Finally, we review how mechanisms of integration and independence vary over developmental or evolutionary time, and we find limited support for integration.

Neural steroid sensitivity and aggression: comparing individuals of two songbird subspecies.

Hormones coordinate the expression of complex phenotypes and thus may play important roles in evolutionary processes. When populations diverge in hormone-mediated phenotypes, differences may arise via changes in circulating hormones, sensitivity to hormones or both. Determining the relative importance of signal and sensitivity requires consideration of both inter- and intrapopulation variation in hormone levels, hormone sensitivity and phenotype, but such studies are rare, particularly among closely related taxa. We compared males of two subspecies of the dark-eyed junco (Junco hyemalis) for territorial aggression and associations among behaviour, circulating testosterone (T), and gene expression of androgen receptor (AR), aromatase (AROM) and oestrogen receptor α in three behaviourally relevant brain regions. Thus, we examined the degree to which evolution may shape behaviour via changes in plasma T as compared with key sex steroid binding/converting molecules. We found that the white-winged junco (J. h. aikeni) was more aggressive than the smaller, less ornamented Carolina junco (J. h. carolinensis). The subspecies did not differ in circulating testosterone, but did differ significantly in the abundance of AR and AROM mRNA in key areas of the brain. Within populations, both gene expression and circulating T co-varied significantly with individual differences in aggression. Notably, the differences identified between populations were opposite to those predicted by the patterns among individuals within populations. These findings suggest that hormone-phenotype relationships may evolve via multiple pathways, and that changes that have occurred over evolutionary time do not necessarily reflect standing physiological variation on which current evolutionary processes may act.

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

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 (ORα) 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 ORα, 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.