Data from: Aggressive behaviours track transitions in seasonal phenotypes of female Siberian hamsters

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 (Phodopus sungorus) and song sparrows (Melospiza melodia), 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.季节性繁殖动物会对环境日照时长（光周期，photoperiod）的变化产生显著的生理与行为响应，其中包括生殖功能与领地攻击性的改变。性腺退化且循环性腺激素水平低下时仍维持攻击性的物种，例如西伯利亚仓鼠（Phodopus sungorus）与歌带鹀（Melospiza melodia），对“性腺激素是攻击性重要介导因子”这一公认理论框架提出了挑战。针对这一表观悖论的一种解释是：在与攻击性相关的脑区中，激素敏感性的季节特异性升高，可弥补生殖静止期内性腺激素水平低下的缺陷。为验证该假说，我们通过操控光周期，在短日照生殖静止期攻击性升高（提示该行为不依赖性腺类固醇激素）的雌性西伯利亚仓鼠中，诱导其年度生殖周期多个阶段的季节性表型自然波动。将雌性仓鼠分别饲养于长日照“夏季”或短日照“冬季”环境中10、24或30周，分别对应性腺退化、回归生殖功能状态以及完全性腺再生阶段。长日照组仓鼠在所有时间点均维持生殖功能，且攻击性维持在较低水平。饲养至第10周时，短日照组中具有生殖响应性的雌性仓鼠出现性腺退化，攻击性显著升高；而无生殖响应的个体未出现此类变化。第24周时，实验动物处于过渡阶段，其生殖与攻击性表型均呈现中间状态。至第30周，短日照组雌性仓鼠已完全性腺再生，攻击性回落至长日照组相似水平。与我们的假说一致，性腺退化的雌性仓鼠体内17β-雌二醇（雌二醇，17β-oestradiol）水平下降，但在与攻击性（而非生殖）相关的脑区中，雌激素受体α（ERα，oestrogen receptor-alpha）的丰度呈现位点特异性升高。位点特异性升高的ERα或可作为一种代偿机制，在循环激素浓度低下的情况下，增强攻击性调控通路对雌二醇的响应能力。综上，本研究结果加深了我们对繁殖物候如何与社会行为相耦合，以及演化形成的、用于协调非繁殖情境下行为的机制的认知。