Changes in gene regulation at multiple levels may comprise an important share of the molecular changes underlying adaptive evolution in nature. However, few studies have assayed within- and between-population variation in gene regulatory traits at a transcriptomic scale, and therefore inferences about the characteristics of adaptive regulatory changes have been elusive. Here, we assess quantitative trait differentiation in gene expression levels and alternative splicing (intron usage) between three closely-related pairs of natural populations of Drosophila melanogaster from contrasting thermal environments that reflect three separate instances of cold tolerance evolution. The cold-adapted populations were known to show population genetic evidence for parallel evolution at the SNP level, and here we find evidence for parallel expression evolution between them, with stronger parallelism at larval and adult stages than for pupae. We also implement a flexible method to estimate cis- versus trans-encoded contributions to expression or splicing differences at the adult stage. The apparent contributions of cis- versus trans-regulation to adaptive evolution vary substantially among population pairs. While two of three population pairs show a greater enrichment of cis-regulatory differences among adaptation candidates, trans-regulatory differences are more likely to be implicated in parallel expression changes between population pairs. Genes with significant cis-effects are enriched for signals of elevated genetic differentiation between cold- and warm-adapted populations, suggesting that they are potential targets of local adaptation. These findings expand our knowledge of adaptive gene regulatory evolution and our ability to make inferences about this important and widespread process.

中文翻译：

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冷适应蝇种群中的平行和种群特异性基因调控进化。

多层次的基因调控变化可能是自然界适应性进化的分子变化的重要组成部分。然而，很少有研究在转录组规模上分析基因调控特征的群体内和群体间变异，因此对适应性调控变化特征的推断一直难以捉摸。在这里，我们评估了三对密切相关的黑腹果蝇自然种群之间基因表达水平和选择性剪接（内含子使用）的数量性状差异，这些差异热环境反映了三个不同的耐冷进化实例。众所周知，冷适应的种群在 SNP 水平上显示出平行进化的种群遗传证据，在这里，我们发现了它们之间平行表达进化的证据，在幼虫和成虫阶段的平行性比蛹更强。我们还实施了一种灵活的方法来估计顺式编码与反式编码对成人阶段表达或剪接差异的贡献。顺式与反式调节对适应性进化的明显贡献在种群对之间差异很大。虽然三个种群对中的两个显示出适应候选者之间的顺式调节差异更大，反式调节差异更可能与种群对之间的平行表达变化有关。具有显着顺式效应的基因富含冷适应和暖适应人群之间遗传分化升高的信号，表明它们是局部适应的潜在目标。