Winter Temperature Affects Fatty Acid Composition and Gene Expression, but Not Fat Content and Survival in a Northern Population of a Range‐Expanding Spider

Species expand their geographic distribution when environmental conditions are favorable or when mutations arise that allow them to live in previously unfavorable conditions. The European wasp spider, <i>Argiope bruennichi</i>, has expanded its range poleward, and populations at the northern edge show higher tolerance to cold and are genetically differentiated from the core populations. We aimed to investigate the degree and limits of plasticity in a recently cold-adapted Estonian population by exposing overwintering juveniles (spiderlings) to three fixed winter regimes over the course of three months. These regimes differed in absolute and relative day and night temperature: cold (5°C day, -15°C night), moderate (5°C day, -5°C night), and warm (15°C day, -5°C night). We expected a differential response to the winter regimes in survival, lipid content, metabolites, and gene expression patterns. The survival probability of the spiderlings decreased over winter by approximately 20% and their lipid content by 28%, with no significant differences between groups. Spiderlings also did not differ in content of saturated and monounsaturated fatty acids per dry weight. However, in spiderlings exposed to the warm winter regime, short-chain omega-3 PUFAs were less abundant (~57%) and long-chain omega-3 PUFAs more abundant (~66%) compared to the other regimes. The gene expression response was low under the cold regime and much higher under the warm regime, as compared to the moderate regime. The affected pathways suggest a more pronounced stress response under warmer winter temperatures. Taken together, our findings demonstrate that <i>A. bruennichi</i> spiderlings from a northern population can endure very different winter regimes. However, the observed physiological responses to the warmer regime suggest metabolic costs that may reduce spiderling survival probability after emergence from the egg sac. We conclude that, despite remarkable tolerance to different winter regimes, warmer winters have nuanced effects on spiderling physiology beyond survival probability.