Data from: Divergence of the diapause transcriptome in apple maggot flies: winter regulation and post-winter transcriptional repression

Duration of dormancy regulates seasonal timing in many organisms and may be modulated by day length and temperature. Though photoperiodic modulation has been well studied, temperature modulation of dormancy has received less attention. Here, we leverage genetic variation in diapause in the apple maggot fly, Rhagoletis pomonella, to test whether gene expression during winter or following spring warming regulates diapause duration. We used RNAseq to compare transcript abundance during and after simulated winter between an apple-infesting population and a hawthorn-infesting population where the apple population ends pupal diapause earlier than the hawthorn-infesting population. Marked differences in transcription between the two populations during winter suggests that the ‘early’ apple population is developmentally advanced compared to the ‘late’ hawthorn population prior to spring warming, with transcripts participating in growth and developmental processes relatively up-regulated in apple pupae during the winter cold period. Thus, regulatory differences during winter ultimately drive phenological differences that manifest themselves in the following summer. Expression and polymorphism analysis identify candidate genes in the Wnt and insulin signaling pathways that contribute to population differences in seasonality. Both populations remained in diapause and displayed a pattern of up- and then down-regulation (or vice versa) of growth-related transcripts following warming, consistent with transcriptional repression. The ability to repress growth stimulated by permissive temperatures is likely critical to avoid mismatched phenology and excessive metabolic demand. Compared to diapause studies in other insects, our results suggest some overlap in candidate genes/pathways, though the timing and direction of changes in transcription are likely species-specific.

休眠时长调控多数生物的季节节律，并可受日照长度与温度的调控。尽管光周期调控的相关研究已较为充分，但温度对休眠的调控却较少受到关注。本研究以苹果实蝇（Rhagoletis pomonella）的滞育（diapause）遗传变异为研究模型，旨在探究冬季或春季升温过程中的基因表达是否调控滞育时长。我们采用RNAseq技术，比较了苹果寄主种群与山楂寄主种群在模拟冬季期间及模拟冬季结束后的转录本丰度；其中苹果寄主种群的蛹滞育（pupal diapause）终止时间早于山楂寄主种群。冬季期间两个种群的转录组差异显著，表明春季升温前，“早熟”的苹果寄主种群发育进度优于“晚熟”的山楂寄主种群：在冬季低温阶段，苹果蛹中参与生长与发育过程的转录本表达量相对上调。因此，冬季的调控差异最终催生了物候差异，该差异将在次年夏季显现。本研究通过表达分析与多态性分析，筛选出Wnt信号通路（Wnt signaling pathway）与胰岛素信号通路（insulin signaling pathway）中参与调控不同种群间物候差异的候选基因。两个种群均维持滞育状态，升温后生长相关转录本呈现先上调后下调（或反之）的表达模式，这与转录抑制的理论预期相符。抑制适宜温度诱导的生长的能力，对于避免物候错配与过度代谢消耗至关重要。与其他昆虫的滞育研究相比，本研究结果显示候选基因与通路存在一定重叠，但转录变化的时序与方向可能具有物种特异性。