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The relationship between environmental stress exposure and ageing is likely to vary with stressor severity, life-history stage and the time scale over which effects are measured. Such factors could influence whether stress exposure accelerates or slows the ageing process, but their interactions have not previously been experimentally investigated. We found that experimental exposure of zebra finches to mildly challenging environmental circumstances from young to old adulthood, which increased exposure to stress hormones, reduced breeding performance during early adulthood, but had positive effects when individuals were bred in old adulthood. This difference was not due to selective mortality, because the effectswere evident within individuals, and no evidence of habituation in the response to the stressor was found. The more stressful environment had no effects on survival during young or old adulthood, but substantially improved survival during middle age. Changes in the effects at different ages could be due to the duration and nature of the challenging exposure, or to variation in coping capacity or strategy with age. These results showthat living under challenging environmental circumstances can influence ageing trajectories in terms of both reproductive performance and longevity. Our results provide experimental support for the emerging idea that stress exposure needs to be optimized rather than minimized to obtain the best health outcomes.