Environmental predictability drives different routes to adaptation

Abstract Climate change is altering thermal environments, yet we know little about how environmental predictability shapes species' adaptive responses. Different species may rely on plasticity or evolution to survive environmental change, but how these strategies depend on environmental predictability remains unclear. Experimental evidence that distinguishes between plastic and evolutionary responses to different patterns of environmental variability has been lacking. Here, we present the first experimental demonstration that compares adaptive responses to predictable versus unpredictable thermal variation, disentangling plastic from evolutionary changes. Using Drosophila melanogaster populations evolved for 11 generations under constant, predictably fluctuating, and randomly fluctuating thermal regimes, we assessed survival and fecundity: a plasticity assay testing flies directly from their evolutionary environments to capture total phenotypic responses, and a common garden assay after two generations of standardized rearing to isolate genetic changes. Strikingly, environmental predictability shaped divergent life-history strategies that were only revealed by comparing our two assays. Populations from predictably fluctuating environments evolved enhanced survival, but this benefit was only visible in the common garden assay, not when tested directly from their evolutionary environment. Conversely, populations from randomly fluctuating environments showed reduced survival in the plasticity assay and consistently lower fecundity in the common garden assay, though this reproductive cost was completely masked in the plasticity assay. These contrasting responses demonstrate that environmental predictability fundamentally determines life-history evolution: predictable variation favors investment in stress-resistant longevity, while unpredictable variation imposes both immediate survival costs and constitutive reproductive constraints. Our findings challenge the traditional view that environmental variation uniformly selects for increased plasticity, instead revealing that the predictability of environmental change determines both the target and mechanism of adaptation. As climate change increases environmental variability and reduces environmental predictability, these insights provide crucial guidance for predicting species persistence and developing effective conservation strategies.