Morph-specific plasticity drives divergent host-shift and acclimation strategies in aphids

Abstract Understanding how organisms cope with environmental change is central to eco-evolutionary theory, yet a key unresolved challenge is distinguishing anticipatory plasticity, where phenotypes are pre-configured using predictive cues, from responsive plasticity, where phenotypes are adjusted after environmental exposure. Empirically testing these strategies is challenging because phenotypes measured after environmental transitions integrate both prior cue-dependent state configuration and post-exposure adjustment, obscuring when plastic responses are initiated. Systems with predictable environmental transitions and discrete life-history stages provide a powerful opportunity to resolve this challenge. Here, we use host-alternating aphids to test how plasticity strategies are organized across morphs experiencing the same seasonal host shift but facing different ecological constraints. We quantified fitness, transcriptomic responses, and host chemical landscapes across three morphs transferred among secondary hosts differing in phloem composition. Migratory spring morphs maintained uniformly high survival and showed minimal transcriptional change, consistent with anticipatory plasticity mediated by pre-configured metabolic and detoxification programs. In contrast, summer morphs exhibited host-dependent survival costs and extensive regulatory remodeling, indicating responsive plasticity. By integrating fitness, transcriptomics, and metabolomics, we show that predictable environmental transitions can favor the evolution and partitioning of plasticity strategies across life-history stages. More broadly, our results provide mechanistic evidence linking environmental predictability, regulatory architecture, and the evolution of plastic responses to heterogeneous environments.