Neuroendocrine patterns underlying seasonal song and year-round territoriality in male black redstarts

Background: The connection between testosterone and territoriality in free-living songbirds has been well studied in a reproductive context, but less so outside the breeding season. To assess the effects of seasonal androgenic action on territorial behavior, we analyzed vocal and non-vocal territorial behavior in response to simulated territorial intrusions (STIs) during three life-cycle stages in free-living male black redstarts: breeding, molt and nonbreeding. Concurrently, we measured changes in circulating testosterone levels, as well as the mRNA expression of androgen and estrogen receptors and aromatase in the preoptic, hypothalamic and song control brain areas that are associated with social and vocal behaviors.
Results: Territorial behavior and estrogen receptor expression in hypothalamic areas did not differ between stages. But plasma testosterone was higher during breeding than during the other stages, similar to androgen receptor and aromatase expression in the preoptic area. The expression of androgen receptors in the song control nucleus HVC was lower during molt when birds do not sing or sing rarely, but similar between the breeding and the nonbreeding stage. Nevertheless, some song spectral features and the song repertoire differed between breeding and nonbreeding. Territorial behavior and song rate correlated with the expression of steroid receptors in hypothalamic areas, and in the song control nucleus lMAN.
Conclusions: Our results demonstrate seasonal modulation of song, circulating testosterone levels, and brain sensitivity to androgens, but a year-round persistency of territorial behavior and estrogen receptor expression in all life-cycle stages. This suggests that seasonal variations in circulating testosterone concentrations and brain sensitivity to androgens is widely uncoupled from territorial behavior and song activity but might still affect song pattern. Our study contributes to the understanding of the complex comparative neuroendocrinology of song birds in the wild.

背景：野生鸣禽中睾酮（testosterone）与领地行为（territoriality）的关联在繁殖情境下已得到充分研究，但在繁殖季之外的相关研究仍较为匮乏。为探究季节性雄激素作用对领地行为的影响，本研究针对野生雄性黑红尾鸲的三个生命周期阶段——繁殖期、换羽期与非繁殖期，分析了其在模拟领地入侵（simulated territorial intrusions，STIs）下的发声与非发声领地行为。同时，本研究检测了其循环睾酮水平的变化，以及与社交和鸣唱行为相关的视前区、下丘脑及鸣唱控制脑区中，雄激素受体、雌激素受体与芳香化酶的mRNA表达情况。
结果：不同生命周期阶段的领地行为与下丘脑区域的雌激素受体表达并无显著差异。但繁殖期的血浆睾酮水平高于其他阶段，视前区的雄激素受体与芳香化酶表达情况亦与此一致。在换羽期，鸣禽几乎不鸣唱或极少鸣唱，其鸣唱控制核团HVC（song control nucleus HVC）中的雄激素受体表达水平较低，但繁殖期与非繁殖期的该受体表达水平并无显著差异。不过，繁殖期与非繁殖期的部分鸣唱频谱特征及鸣唱曲目库存在差异。领地行为与鸣唱频率分别与下丘脑区域及鸣唱控制核团lMAN（song control nucleus lMAN）中的类固醇受体表达水平相关。
结论：本研究结果显示，鸣唱、循环睾酮水平及脑对雄激素的敏感性存在季节性调控，但领地行为与各生命周期阶段的雌激素受体表达均呈现全年持续性。这表明，循环睾酮浓度与脑对雄激素的敏感性的季节性变化，虽与领地行为及鸣唱活动广泛脱耦联，但仍可能影响鸣唱模式。本研究有助于深化对野生鸣禽复杂比较神经内分泌学（comparative neuroendocrinology）的认知。