Territorial aggression, circulating levels of testosterone, and brain aromatase activity in free-living pied flycatchers

Abstract

Testosterone (T) is a critical endocrine factor for the activation of many aspects of reproductive behavior in vertebrates. Castration completely eliminates the display of aggressive and sexual behaviors that are restored to intact level by a treatment with exogenous T. There is usually a tight correlation between the temporal changes in plasma T and the frequency of reproductive behaviors during the annual cycle. In contrast, individual levels of behavioral activity are often not related to plasma T concentration at the peak of the reproductive season suggesting that T is available in quantities larger than necessary to activate behavior and that other factors limit the expression of behavior. There is some indication from work in rodents that individual levels of brain aromatase activity (AA) may be a key factor that limits the expression of aggressive behavior, and in agreement with this idea, many studies indicate that estrogens produced in the brain by the aromatization of T may contribute to the activation of reproductive behavior, including aggression. We investigated here in pied flycatcher ( Ficedula hypoleuca) the relationships among territorial aggression, plasma T, and brain AA at the peak of the reproductive season. In a first experiment, blood samples were collected from unpaired males holding a primary territory and, 1 or 2 days later, their aggressive behavior was quantified during standardized simulated territorial intrusions. No relationship was found between individual differences in aggressive behavior and plasma T or dihydrotestosterone levels but a significant negative correlation was observed between number of attacks and plasma corticosterone. In a second experiment, aggressive behavior was measured during a simulated territorial intrusion in 22 unpaired males holding primary territories. They were then immediately captured and AA was measured in their anterior and posterior diencephalon and in the entire telencephalon. Five males that had attracted a female (who had started egg-laying) were also studied. The paired males were less aggressive and correlatively had a lower AA in the anterior diencephalon but not in the posterior diencephalon and telencephalon than the 22 birds holding a territory before arrival of a female. In these 22 birds, a significant correlation was observed between number of attacks/min displayed during the simulated territorial intrusion and AA in the anterior diencephalon but no correlation was found between these variables in the two other brain areas. Taken together, these data indicate that the level of aggression displayed by males defending their primary territory may be limited by the activity of the preoptic aromatase, but plasma T is not playing an important role in establishing individual differences in aggression. Alternatively, it is also possible that brain AA is rapidly affected by agonistic interactions and additional work should be carried out to determine whether the correlation observed between brain AA and aggressive behavior is the result of an effect of the enzyme on behavior or vice versa. In any case, the present data show that preoptic AA can change quite rapidly during the reproductive cycle (within a few days after arrival of the female) indicating that this enzymatic activity is able to regulate rapid behavioral transitions during the reproductive cycle in this species.