Abstract Social interactions among conspecifics can have marked effects on individual physiology, especially through their modulation of the stress axis by affecting the production of adrenal glucocorticoids (GCs). Previous research has focused on how individual GC levels may be influenced by social status, but few studies have considered how the balance between positive (e.g. cooperation) and negative (e.g. competition) social interactions shape individual GC levels. A lack of association between individual GC levels and social factors may be confounded by opposite effects of social competition on the one hand and social cooperation on the other. We tested for these effects in the Columbian ground squirrel ( Urocitellus columbianus ), a colonial rodent. During the breeding season, females are exposed to territorial unrelated neighbors and to territorial, but more tolerant, close kin. On one hand, territoriality and competition for resources led us to predict a positive association between local colony density and female GC levels. On the other, higher tolerance of philopatric kin females and known fitness benefits led us to predict a negative association between kin numbers and female GC levels. We compared levels of fecal cortisol metabolites (FCMs) in females at two different spatial scales during lactation: local (a female’s core territory during lactation, 30-m radius about her nest burrow) and colony-wide. At the local scale, female FCM levels were neither related to colony density nor to the number of co-breeding female kin, but FCM levels increased with age. At the colony scale, female FCM levels varied in a quadratic fashion with female kin numbers. FCM levels decreased by 15% from 0 to 1 co-breeding kin present and increased with > 1 kin present. Among females that had only one co-breeding kin present, daughters (and littermate sisters and mothers, but not significantly) led to a 14% reduction in FCM levels compared with females that had no kin. Our results reject the idea that local colony density is associated with increased GC levels this species, but indicate subtle (positive and negative) effects of kin on individual GC secretion. They further call into question the importance of the nature of social relationships in modulating the stress experienced by individuals. Significance statement Few studies have tested how the balance between positive (e.g. cooperation) and negative (e.g. competition) social interactions shapes individual stress and glucocorticoid (GC) levels in group-living animals. In colonial Columbian ground squirrels, breeding females are exposed to territorial neighbors and to more tolerant close kin. We show that kin numbers have subtle (positive and negative) effects on female GC levels. Compared with breeding females with no kin, female GC levels decrease by 15% with the presence of a single co-breeding close relative, but increase with the presence of more than one co-breeding related female. Among females that have only one co-breeding kin, the presence of daughters (and littermate sisters and mothers, but not significantly) leads to a 14% reduction in female GC levels. Our results highlight how GC levels may be influenced by the specific nature of social relationships in group-living animals.

中文翻译：

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雌性哥伦比亚地松鼠的社会压力：亲属的密度独立效应导致粪便糖皮质激素代谢物的变化

摘要 同种之间的社会互动会对个体生理产生显着影响，特别是通过它们通过影响肾上腺糖皮质激素 (GC) 的产生来调节应激轴。以前的研究集中在个人 GC 水平如何受到社会地位的影响，但很少有研究考虑积极（例如合作）和消极（例如竞争）社会互动之间的平衡如何塑造个人 GC 水平。个体 GC 水平与社会因素之间缺乏关联可能会被一方面社会竞争和另一方面社会合作的相反影响所混淆。我们在哥伦比亚地松鼠 ( Urocitellus columbianus )，一种殖民地啮齿动物中测试了这些影响。在繁殖季节，雌性暴露于领土无关的邻居和领土，但更宽容，近亲。一方面，地域性和资源竞争使我们预测当地菌落密度与雌性 GC 水平之间存在正相关。另一方面，对亲近亲属女性的更高耐受性和已知的健康益处使我们预测亲属数量与女性 GC 水平之间存在负相关。我们比较了哺乳期间雌性在两个不同空间尺度上的粪便皮质醇代谢物 (FCM) 水平：局部（雌性哺乳期间的核心区域，巢穴周围 30 米半径）和群体范围。在局部尺度上，雌性 FCM 水平与菌落密度和同种雌性亲属数量无关，但 FCM 水平随年龄增加而增加。在殖民地规模上，女性 FCM 水平随女性亲属人数呈二次方变化。FCM 水平从 0 到 1 个共同繁殖亲属降低了 15%，并随着 > 1 亲属的存在而增加。在只有一个共同繁殖亲属的雌性中，与没有亲属的雌性相比，女儿（以及同窝的姐妹和母亲，但不显着）导致 FCM 水平降低 14%。我们的结果拒绝了局部菌落密度与该物种 GC 水平增加相关的观点，但表明 kin 对个体 GC 分泌的微妙（积极和消极）影响。他们进一步质疑社会关系的性质在调节个人承受的压力方面的重要性。重要性声明 很少有研究测试积极（例如合作）和消极（例如 竞争）社会互动塑造了群体生活动物的个体压力和糖皮质激素 (GC) 水平。在殖民地哥伦比亚地松鼠中，繁殖雌性暴露于领土邻居和更宽容的近亲。我们表明亲属数量对女性 GC 水平具有微妙的（正面和负面）影响。与没有亲属的繁殖雌性相比，存在一个共同繁殖近亲的雌性GC水平降低了15%，但随着存在一个以上共同繁殖相关的雌性而增加。在只有一个共同繁殖亲属的雌性中，女儿（和同窝姐妹和母亲，但不显着）的存在导致雌性 GC 水平降低 14%。我们的结果强调了 GC 水平如何受到群居动物社会关系的特定性质的影响。