Seasonal constraints on maternal body size induce transgenerational fitness penalties in a sheet‐web spider

Seasonal environmental fluctuations profoundly shape the life‐history strategies of arthropod predators, frequently altering population dynamics and trophic interactions within natural systems. However, how extreme seasonal constraints, such as compounded thermal stress and nutritional bottlenecks, are transgenerationally transmitted via maternal effects remains a critical question in evolutionary ecology. We investigated these transgenerational constraints in the sheet‐web spider Hylyphantes graminicola . We collected field‐matured parental cohorts during early summer (temperate conditions with abundant aquatic insect pulses) and early autumn (severe thermal stress and aquatic resource depletion), and evaluated the developmental and reproductive performance of their F1 offspring under standardized laboratory conditions. The synergistic pressures of late‐summer heat and resource depletion significantly miniaturized early‐autumn maternal phenotypes. This environmentally induced constraint inflicted a deleterious ‘Silver Spoon’ effect on the F1 generation: despite receiving ad libitum prey, the early‐autumn F1 lineage suffered prolonged development, elevated juvenile mortality and a catastrophic collapse in egg hatching rates. Notably, mating behaviors of surviving F1 adults remained robust, indicating a profound decoupling between behavioral canalization and underlying physiological viability. Our results demonstrate a progressive manifestation of nutritional deficits, indicating that generic caloric intake cannot rescue specific maternally inherited biochemical shortfalls. Ultimately, this study illustrates that standard behavioral metrics can mask severe transgenerational physiological distress, emphasizing the evolutionary and demographic vulnerabilities of arthropod populations facing seasonal bottlenecks.