Parental thermal environment affects offspring resilience to winter and spring weather anomalies

Recent increases in the frequency and intensity of thermal anomalies can result in recurrent stressful weather events. Among annual insects, this phenomenon may expose parents and offspring to a succession of different weather anomalies (e.g. summer heatwaves and late spring frosts). Parental stress can alter offspring physiology and performance, potentially affecting their tolerance of environmental variation. We investigated the transgenerational effects of thermal anomalies on a univoltine wetland butterfly. We induced parental thermal stress by exposing pupae to a constant temperature, ranging from stressfully cold to stressfully hot (10 °C, 26 °C, 28 °C, 32 °C), for three days. Offspring were then subjected to either winter heatwaves or spring thermal anomalies. In the parental generation, pupal exposure to heat stress (32 °C) reduced adult longevity by 46%, while exposure to 28 °C maximized female reproductive output. Parental exposure to thermal stress did not affect offspring larval mass at the onset of diapause, but it did reduce offspring survival during winter and spring. Under winter heatwaves, survival was significantly higher among offspring of parents exposed to 26 °C than those exposed to 10 °C. Parental thermal stress was associated with decreased offspring survivorship in spring under control conditions and after a late frost. We observed anticipatory parental effects, as offspring of heat-stressed parents had increased survival under winter heatwaves, and negative transgenerational effects, as offspring of both heat and cold-stressed parents exhibited lower spring survivorship. We demonstrate a mechanism by which altered weather patterns can result in butterfly declines, highlighting the challenges that warming temperatures pose for insects.