Many organisms enter a dormant state in their life cycle to deal with predictable changes in environments over the course of a year. The timing of dormancy is therefore a key seasonal adaptation, and it evolves rapidly with changing environments. We tested the hypothesis that differences in the timing of seasonal activity are driven by differences in the rate of development during diapause in Rhagoletis pomonella, a fly specialized to feed on fruits of seasonally limited host plants. Transcriptomes from the central nervous system across a time series during diapause show consistent and progressive changes in transcripts participating in diverse developmental processes, despite a lack of gross morphological change. Moreover, population genomic analyses suggested that many genes of small effect enriched in developmental functional categories underlie variation in dormancy timing and overlap with gene sets associated with development rate in Drosophila melanogaster. Our transcriptional data also suggested that a recent evolutionary shift from a seasonally late to a seasonally early host plant drove more rapid development during diapause in the early fly population. Moreover, genetic variants that diverged during the evolutionary shift were also enriched in putative cis regulatory regions of genes differentially expressed during diapause development. Overall, our data suggest polygenic variation in the rate of developmental progression during diapause contributes to the evolution of seasonality in R. pomonella. We further discuss patterns that suggest hourglass-like developmental divergence early and late in diapause development and an important role for hub genes in the evolution of transcriptional divergence.

许多生物体在其生命周期中进入休眠状态，以应对一年中可预测的环境变化。因此，休眠时间是一个关键的季节性适应，并且随着环境的变化而迅速变化。我们测试了这样一个假设，即季节性活动时间的差异是由苹果蠹（ Rhagoletis pomonella）滞育期间发育速率的差异所驱动的，苹果蠹是一种专门以季节性有限的寄主植物的果实为食的苍蝇。尽管缺乏总体形态变化，但滞育期间整个时间序列中枢神经系统的转录组显示，参与不同发育过程的转录本出现了一致和渐进的变化。此外，群体基因组分析表明，许多在发育功能类别中富集的小效应基因是休眠时间变化的基础，并且与果蝇发育速率相关的基因集重叠。我们的转录数据还表明，最近从季节性晚寄主植物到季节性早寄主植物的进化转变推动了早期果蝇种群在滞育期间更快的发育。此外，在进化转变过程中分化的遗传变异也在滞育发育期间差异表达的基因的推定顺式调控区域中富集。总体而言，我们的数据表明滞育期间发育进展速率的多基因变异有助于苹果树的季节性进化。我们进一步讨论了滞育发育早期和晚期沙漏状发育分歧的模式，以及中枢基因在转录分歧进化中的重要作用。