thyroid hormone concentrations in female baboons: metabolic consequences of living in a highly seasonal environment

How female mammals adapt metabolically in response to environmental variation remains understudied in the wild, because direct measures of metabolic activity are difficult to obtain in wild populations. However, recent advances in the non-invasive measurement of fecal thyroid hormones, triiodothyronine (T3), an important regulator of metabolism, provide an opportunity to understand how female baboons living in the harsh Amboseli ecosystem in southern Kenya adapt to environmental variability and escape strict reproductive seasonality. Specifically, we assessed how a female's activity budget, diet, and concentrations of fecal T3 metabolites (mT3) changed over the course of the year and between years. We then tested which of several environmental variables (season, rainfall, and temperature) and behavioral variables (female activity budget and diet) best predicted mT3 concentrations. Finally, we determined if two important reproductive events – onset of ovarian cycling and conception of an offspring – were preceded by changes in female mT3 concentrations. We found female baboons' mT3 concentrations varied markedly across the year and between years as a function of environmental conditions. Further, changes in a female's behavior and diet only partially mediated the metabolic response to the environment. Finally, mT3 concentrations increased in the weeks prior to menarche and cycling resumption, regardless of the month or season in which cycling started. This pattern indicates that metabolic activation may be an indicator of reproductive readiness in female baboons as their energy balance is restored.

Methods
Seasonal and annual variation in climate were determined using daily records of rainfall and temperature that were obtained at the research field camp (located within 2-17 km of the ranges of the baboon study groups) using a rain gauge and a min-max thermometer placed in the shade.

Our behavioral data are derived from 39,292 10-minute focal animal behavioral samples from 220 adult female subjects in all reproductive states, collected between 2005-2018. During each 10-minute sample, we recorded the activity of the focal baboon, categorized as feeding (including food processing), walking while not feeding, resting, or socializing (grooming, being groomed, other social activities).When the activity during a given point sample was feeding, the type of food was recorded and whenever possible the species and plant part identified. We categorized foods into eight major food types, with five types considered high-energy foods: grass blades, fruits, flowers, tree gum, and invertebrates; and three types considered low-energy foods: grass corms, grass blade bases and seed heads, and Vachellia seeds.

Our hormonal data are derived from 7,107 fecal samples from 220 adult females. mT3 concentrations were determined using radioimmunoassays.

野生雌性哺乳动物在代谢层面响应环境变化的相关野外研究仍有待深入，原因在于直接测量野生种群的代谢活性难度极高。近年来，粪便甲状腺激素——代谢关键调节因子三碘甲状腺原氨酸（triiodothyronine, T3）——的非侵入性检测技术取得进展，这为解析栖息于肯尼亚南部严酷安博塞利生态系统中的雌性狒狒如何适应环境波动、打破严格的繁殖季节性提供了全新契机。

具体而言，本研究评估了雌性狒狒的活动预算、饮食组成以及粪便T3代谢物（mT3）浓度在年度内与年间的变化特征。随后，我们检验了多组环境变量（季节、降雨量与气温）与行为变量（雌性活动预算及饮食结构）中，哪些可最优预测mT3浓度。最后，我们探究了两项关键生殖事件——卵巢周期启动与后代受孕——发生前，雌性狒狒的mT3浓度是否存在显著变化。

研究结果显示，雌性狒狒的mT3浓度会随环境条件变化，在年度尺度与年间均呈现显著差异。此外，雌性的行为与饮食变化仅能部分介导其对环境的代谢响应。最后，无论卵巢周期重启发生在哪个月份或季节，初潮与周期恢复前数周的mT3浓度均会上升。这一模式表明，当雌性狒狒的能量平衡得以恢复时，代谢激活或可作为其生殖准备状态的指示指标。

## 研究方法
气候的季节与年度变化通过研究营地（距狒狒研究群体活动范围2-17公里）内、置于阴凉处的雨量计与最高最低温度计获取的每日降雨与气温记录确定。

我们的行为数据来源于2005至2018年间，针对220只处于各生殖状态的成年雌性个体收集的39292份10分钟焦点动物行为样本。在每份10分钟采样周期内，我们记录焦点狒狒的活动状态，分为进食（含食物处理）、非进食行走、休息与社交（理毛、被理毛及其他社交活动）四类。当采样点的活动为进食时，我们会记录食物类型，并尽可能鉴定食物的物种与植物部位。本研究将食物划分为八大类别，其中五类为高能量食物：草叶、果实、花朵、树胶与无脊椎动物；三类为低能量食物：球茎草、草叶基部与穗状种子，以及金合欢属（Vachellia）种子。

我们的激素数据来源于220只成年雌性个体的7107份粪便样本。mT3浓度通过放射免疫测定法（radioimmunoassay）进行检测。