Combined aromatase inhibitor and antiandrogen treatment decreases territorial aggression in a wild songbird during the nonbreeding season.

Male song sparrows (Melospiza melodia morphna) defend territories throughout the year in western Washington State. In the nonbreeding season (autumn and winter), aggression and song are robustly expressed but plasma testosterone (T) levels are basal. Also, castration does not decrease nonbreeding territoriality. In this field experiment, we asked whether nonbreeding aggression is independent of T. T can act via androgen receptors or T can be aromatized to 17beta-estradiol (E(2)) and act via estrogen receptors. We treated free-living nonbreeding birds with an aromatase inhibitor (ATD) and an androgen receptor antagonist (flutamide) in combination. We then challenged subjects with a live decoy and playback of tape-recorded songs. ATD+flutamide treatment decreased several aggressive behaviors. However, ATD+flutamide treatment did not affect body condition, suggesting that subjects were healthy and that foraging behavior was not reduced. As expected, ATD+flutamide treatment increased plasma T, probably by blocking negative feedback on luteinizing hormone. Surprisingly, ATD+flutamide treatment increased plasma E(2). Most other studies using aromatase inhibitors have not measured plasma E(2). However, it is possible that ATD+flutamide treatment decreased local E(2) levels in the brain but not in plasma. Finally, ATD+flutamide treatment increased plasma corticosterone, perhaps in response to increased plasma T or E(2). To our knowledge, these are the first data to suggest that nonbreeding territoriality is regulated by endogenous steroid hormones. Nongonadal production of sex steroids may support aggression in the nonbreeding season.

Soma KK ，Sullivan K ，Wingfield J 《GENERAL AND COMPARATIVE ENDOCRINOLOGY》

Testosterone and year-round territorial aggression in a tropical bird.

Testosterone (T) regulates avian behaviors such as song and aggression during the breeding season. However, the role of T in year-round territorial birds is still enigmatic, especially in tropical birds. Spotted antbirds (Hylophylax n. naevioides) defend territories in the Panamanian rainforest year-round but have low plasma T levels (0.1-0.2 ng/ml), except during brief periods of social challenges. We manipulated T action in captive male Spotted antbirds to test whether this hormone is involved in the regulation of song and aggression. T-implants increased plasma androgen levels (T and dihydrotestosterone) and enhanced song in nonbreeding males. During a staged male-male encounter, T-implanted males sang more and were more aggressive than controls. In a second experiment, we blocked the two known T actions: its binding to androgen receptors and its conversion into estradiol by the enzyme aromatase. For this, we administered the androgen receptor antagonist flutamide (Flut) in combination with the aromatase inhibitor 1-4-6 androstatrien-3, 17-dione (ATD) to birds in breeding condition. ATD + Flut treatment significantly elevated plasma levels of luteinizing hormone, presumably via the lack of T feedback from its receptors. ATD + Flut-treated birds gave fewer spontaneous songs than control-implanted males. During staged male-male encounters, ATD + Flut-treated males did not sing at all and showed reduced aggressive behavior. Our data indicate that T can regulate aggressive behavior in these tropical birds. Although plasma T levels can be low year-round, Spotted antbirds may use T either by secreting it briefly during social challenges, by having a high sensitivity to T action, or by enzymatically converting circulating T precursors directly at the site of action. We hypothesize that plasma T levels are kept low in these year-round territorial birds to avoid potentially detrimental effects of tonically elevated T. Future treatment of nonbreeding birds with ATD + Flut will reveal whether T is indeed involved year-round in regulating aggressive behavior.

Hau M ，Wikelski M ，Soma KK ，Wingfield JC ... -  《GENERAL AND COMPARATIVE ENDOCRINOLOGY》

Dehydroepiandrosterone in songbird plasma: seasonal regulation and relationship to territorial aggression.

Many male animals are territorial in the breeding season, when plasma testosterone (T) levels are high, and nonterritorial in the nonbreeding season, when plasma T levels are basal. In contrast to this common pattern, male song sparrows (Melospiza melodia morphna) are territorial year-round, except briefly during molt. Song sparrows are highly aggressive in the nonbreeding season (autumn and winter), even though plasma T, 5 alpha-dihydrotestosterone, androstenedione (AE), and 17beta-estradiol levels are undetectable (<or=0.1 ng/ml). Castration has no effect on nonbreeding territoriality. However, aromatase inhibitors decrease aggression in the nonbreeding season, indicating a role for estrogens in winter. The androgenic substrate for brain aromatase in winter is unclear, because plasma T and AE levels are basal. Here, we measured plasma levels of dehydroepiandrosterone (DHEA). DHEA is a precursor to AE and T, and the avian brain can convert DHEA into sex steroids. In nonbreeding male song sparrows, plasma levels of DHEA were detectable and several times higher than plasma AE and T levels. Plasma DHEA levels were similar in the breeding and nonbreeding seasons, but significantly lower during molt, which parallels seasonal changes in male aggression. Adrenal glands and testes from nonbreeding males had high concentrations of DHEA, suggesting that both tissues may secrete DHEA. However, stress and gonadotropin-releasing hormone (GnRH) did not increase plasma DHEA in nonbreeding birds. We hypothesize that in the nonbreeding season, circulating DHEA, possibly of adrenal origin, is converted into active sex steroids by steroidogenic enzymes in the brain. This mechanism would create high local levels of sex steroids in the brain to support winter aggression.

Soma KK ，Wingfield JC 《GENERAL AND COMPARATIVE ENDOCRINOLOGY》

The role of androgen receptors in regulating territorial aggression in male song sparrows.

This paper examines the role that androgen receptors (ARs) play in modulating aggressive behavior in male song sparrows, Melospiza melodia morphna. Song sparrows are seasonally breeding, territorial birds that maintain year-round territories with male-female pair bonds formed during the spring breeding season. Plasma testosterone levels peak as territories are established and mates acquired. In late summer, testosterone levels fall and remain basal during the non-breeding season. We examined the role of ARs in regulating territorial aggression in captive song sparrows under short- and long-day conditions as well as just prior to, and at the start of the breading season in freely living birds using the nonsteroidal antiandrogen flutamide to block AR function. Birds were implanted with either empty or drug filled silastic implants for 18 to 42 days and then challenged with a novel male decoy to assess the individual birds level of male-male aggression. Freely living birds remained on their home territory and underwent a simulated territorial intrusion, whereas laboratory-held birds were assessed using a laboratory simulated territorial intrusion and remained in their home cage. Experimental treatment of male song sparrows decreased aggressive behavior during the pre-breeding life history substage (March-April) in freely living birds as well as in laboratory-held birds under long-day (16L:8D) conditions. During the early breeding substage (April-May) there was no measurable effect of flutamide treatment on aggressive behavior, nor was there a difference in behavior in the (8L:16D) laboratory birds. This demonstrates that ARs are an important component of the neuroendocrine control of aggressive behavior. Given that flutamide only affected aggression during the pre-breeding substage and in LD birds, the results suggest that AR dependent control of aggressive behavior changes as song sparrow life history states change.

Sperry TS ，Wacker DW ，Wingfield JC 《-》

Dehydroepiandrosterone (DHEA) increases territorial song and the size of an associated brain region in a male songbird.

In many species, male territorial aggression is tightly coupled with gonadal secretion of testosterone (T). In contrast, in song sparrows (Melospiza melodia morphna), males are highly aggressive during the breeding (spring) and nonbreeding (autumn and early winter) seasons, but not during molt (late summer). In aggressive nonbreeding song sparrows, plasma T levels are basal (< or = 0.10 ng/ml), and castration has no effect on aggression. However, aromatase inhibitors reduce nonbreeding aggression, indicating a role for estrogen in wintering males. In the nonbreeding season, the substrate for brain aromatase is unclear, because plasma T and androstenedione levels are basal. Aromatizable androgen may be derived from plasma dehydroepiandrosterone (DHEA), an androgen precursor. DHEA circulates at elevated levels in wintering males (approximately 0.8 ng/ml) and might be locally converted to T in the brain. Moreover, plasma DHEA is reduced during molt, as is aggression. Here, we experimentally increased DHEA in wild nonbreeding male song sparrows and examined territorial behaviors (e.g., singing) and discrete neural regions controlling the production of song. A physiological dose of DHEA for 15 days increased singing in response to simulated territorial intrusions. In addition, DHEA treatment increased the volume of a telencephalic brain region (the HVc) controlling song, indicating that DHEA can have large-scale neuroanatomical effects in adult animals. The DHEA treatment also caused a slight increase in plasma T. Exogenous DHEA may have been metabolized to sex steroids within the brain to exert these behavioral and neural effects, and it is also possible that peripheral metabolism contributed to these effects. These are the first results to suggest that exogenous DHEA increases male-male aggression and the size of an entire brain region in adults. The data are consistent with the hypothesis that DHEA regulates territorial behavior, especially in the nonbreeding season, when plasma T is basal.

Soma KK ，Wissman AM ，Brenowitz EA ，Wingfield JC ... -  《HORMONES AND BEHAVIOR》