Calcium-Dependent Rapid Adaptation to Long-Term Warming in Zooplankton

Abstract

Climate change is rapidly warming freshwater habitats. Here, we employed the model freshwater zooplankton Daphnia magna to address whether long-term heat selection leads to increased tolerance, and whether this adaptive response is constrained by calcium availability and regulation. We showed that D. magna populations exhibited a robust adaptive response following multigenerational selection, with increased heat tolerance and shifted phenotypic plasticity. However, this tolerance was accompanied by temperature-dependent trade-offs in growth and reproductive timing that may accumulate over generations. Such enhanced heat tolerance was contingent upon sufficient environmental calcium, with performance declining under calcium-limited conditions, thereby uncovering a previously underexplored but ecologically significant phenomenon of the calcium dependency of heat tolerance. Novel real-time near-infrared (NIR-II-Ca) imaging demonstrated that heat adaptation involved not only increased calcium demand but also an adaptive optimization of calcium flux dynamics. This physiological shift is further supported by the constitutive up-regulation of heat shock transcription factor (HSF). By mapping the HSF-centered regulatory network, we revealed that HSF may coordinate a systemic program beyond canonical stress paradigms, integrating ion homeostasis with heat tolerance. Collectively, our study highlights that while rapid adaptation to warming is feasible, it is fundamentally constrained by internal trade-offs and external calcium dependency, underscoring the complex interplay of physiology, environment, and molecular regulation in determining organismal resilience to climate warming.