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Understanding how populations adapt to changing environments is a major goal in evolutionary biology and ecology, and particularly urgent for predicting resilience to climate change. Phenotypic plasticity, the ability to express multiple phenotypes from the same genome, is a widespread adaptation to short-term environmental fluctuations, but whether it facilitates adaptation to environmental change on evolutionary timescales, such as those under climate change, remains contentious. Here, we investigate plasticity and adaptive potential in an African savannah butterfly displaying extensive plasticity as adaptation to predictable dry-wet seasonality. We assess the transcriptional architecture of seasonal plasticity and find pervasive gene expression differences between the seasonal phenotypes, reflecting a genome-wide plasticity programme. Strikingly, intra-population genetic variation for this response is highly depleted, possibly reflecting strong purifying selection in its savannah habitat where an environmental cue (temperature) reliably predicts seasonal transitions and the cost of a mismatched phenotype is high. Under climate change the accuracy of such cues may deteriorate, rendering dominant reactions norm maladaptive. Therefore, depleted variation for plasticity as reported here may crucially limit evolutionary potential when conditions change, and seasonally plastic species may in fact be especially vulnerable to climate change.

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