Rapid ecological and evolutionary divergence during a poleward range expansion

In response to climate change, a northward range expansion has been observed in many species. The wasp spider, Argiope bruennichi, has expanded from its historic range in the Mediterranean ("core"), now reaching as far as the Baltic States and Scandinavia ("edge"), even faster than the pace of climate change. We explored life history traits, adult phenotypes, offspring cold tolerance, and genomic patterns across the European range of A. bruennichi, and found origin-, environment- and life stage-specific responses to the cold northern climate. Wasp spiders have shifted their phenology at the edge, with females maturing earlier and at a smaller size, but maintaining similar pigmentation, clutch sizes, and hatching success compared to the core region. Using a reciprocal common garden experiment on overwintering offspring from the core and edge, we found evidence for genetic adaptation and considerable phenotypic plasticity. Overwintering survival was lower under the cold winter treatment for spiderlings from both origins. However, the edge-origin spiderlings that survived the winter had lower lethal temperatures and enhanced supercooling ability with reduced phenotypic plasticity in supercooling points compared to core spiderlings, while the chill coma recovery time was similar. Metabolomic analysis revealed accumulations of amino acids and myo-inositol in the cold winter treatment, particularly in spiderlings from the edge population, suggesting a role of these metabolites in improving cold tolerance. Genotype-environment tests showed strong genetic association across the genome to seasonality and minimum winter temperature. The population genomic analysis across the European range splits A. bruennichi into two distinct genetic clusters through the center of Germany, which roughly aligns with turnover from an oceanic to continental climate zone, complementing the genotype-environment test results. Overall, our study highlights the importance of integrating data on phenological shifts, changes in life-history, and life stage-specific phenotypic plasticity and genetic adaptation to understand the impacts of range expansions and shifts. The nuanced processes of acclimation and adaptation we uncovered advocate for holistic investigations of evolutionary fitness and fitness-related traits in the context of organismal responses to novel and changing environments.