Rendon Nikki M, Amez Andrea C, Proffitt Melissa R, Bauserman Elizabeth R, Demas Gregory E
Department of Biology, Center for the Integrative Study of Animal Behavior, Program in Neuroscience, Indiana University, Bloomington, IN 47405, USA.
Funct Ecol. 2017 May;31(5):1071-1081. doi: 10.1111/1365-2435.12816. Epub 2017 Jan 12.
Seasonally breeding animals exhibit profound physiological and behavioural responses to changes in ambient day length (photoperiod), including changes in reproductive function and territorial aggression.Species where aggression persists when gonads are regressed and circulating levels of gonadal hormones are low, such as Siberian hamsters () and song sparrows (), challenge the well-established framework that gonadal hormones are important mediators of aggression.A solution to this apparent paradox is that a season-specific increase in sensitivity to hormones in brain areas associated with aggression offsets low levels of gonadal hormones during periods of reproductive quiescence.To test this hypothesis, we manipulated photoperiod to induce natural fluctuations in seasonal phenotype across multiple stages of the annual reproductive cycle in female Siberian hamsters that display increased aggression during short-day reproductive quiescence, suggesting that behaviour persists independent of gonadal steroids.Females were housed in long "summer" days or short "winter" days for 10, 24 or 30 weeks to capture gonadal regression, transition back to a reproductively functional state and full gonadal recrudescence, respectively.Long-day animals maintained reproductive functionality and displayed low aggression across all time points. By week 10, short-day reproductively responsive females underwent gonadal regression and displayed increased aggression; non-responsive animals showed no such changes. At week 24, animals were in a transitional period and displayed an intermediate phenotype with respect to reproduction and aggression. By week 30, short-day females were fully recrudesced and returned to long-day-like levels of aggression.Consistent with our hypothesis, gonadally regressed females displayed decreases in 17β-oestradiol (oestradiol) levels, but site-specific increases in the abundance of brain oestrogen receptor-alpha (ERα) in regions associated with aggression, but not reproduction. Increased site-specific ERα may function as a compensatory mechanism to allow increased responsiveness to oestradiol in regulating aggression in lieu of high circulating concentrations of hormones.Collectively, these results broaden our understanding of how breeding phenology maps onto social behaviour and the mechanisms that have evolved to coordinate behaviours that occur in non-breeding contexts.
季节性繁殖动物对环境日长（光周期）的变化表现出深刻的生理和行为反应，包括生殖功能和领地攻击性的变化。在性腺退化且性腺激素循环水平较低时攻击性仍然存在的物种，如西伯利亚仓鼠（Phodopus sungorus）和歌带鹀（Melospiza melodia），对性腺激素是攻击性重要调节因子这一既定框架提出了挑战。解决这一明显矛盾的方法是，在与攻击性相关的脑区中，对激素的敏感性在特定季节增加，从而在生殖静止期抵消性腺激素水平的降低。为了验证这一假设，我们通过控制光周期，在雌性西伯利亚仓鼠的年度生殖周期的多个阶段诱导季节性表型的自然波动，这些仓鼠在短日照生殖静止期表现出攻击性增加，这表明其行为的持续存在独立于性腺类固醇。雌性仓鼠分别在长“夏季”日照或短“冬季”日照条件下饲养10周、24周或30周，以分别捕捉性腺退化、恢复到生殖功能状态以及性腺完全恢复的过程。长日照条件下的动物在所有时间点都保持生殖功能且攻击性较低。到第10周时，短日照条件下具有生殖反应的雌性仓鼠性腺退化且攻击性增加；无反应的动物则没有此类变化。在第24周时，动物处于过渡期，在生殖和攻击性方面表现出中间表型。到第30周时，短日照条件下的雌性仓鼠性腺完全恢复，攻击性恢复到类似长日照条件下的水平。与我们的假设一致，性腺退化的雌性仓鼠17β - 雌二醇（雌二醇）水平降低，但在与攻击性而非生殖相关的脑区中，脑雌激素受体α（ERα）的丰度在特定部位增加。特定部位ERα的增加可能作为一种补偿机制，使机体在调节攻击性时对雌二醇的反应性增加，以替代高循环浓度的激素。总的来说，这些结果拓宽了我们对繁殖物候如何映射到社会行为以及为协调非繁殖环境中发生的行为而进化出的机制的理解。
