Regulation of gene expression is a critical link between genotype and phenotype explaining substantial heritable variation within species. However, we are only beginning to understand the ways that specific gene regulatory mechanisms contribute to adaptive divergence of populations. In plants, the post-transcriptional regulatory mechanism of alternative splicing (AS) plays an important role in both development and abiotic stress response, making it a compelling potential target of natural selection. AS allows organisms to generate multiple different transcripts/proteins from a single gene and thus may provide a source of evolutionary novelty. Here, we examine whether variation in alternative splicing and gene expression levels might contribute to adaptation and incipient speciation of dune-adapted prairie sunflowers in Great Sand Dunes National Park, Colorado, USA. We conducted a common garden experiment to assess transcriptomic variation among ecotypes and analyzed differential expression, differential splicing, and gene coexpression. We show that individual genes are strongly differentiated for both transcript level and alternative isoform proportions, even when grown in a common environment, and that gene coexpression networks are disrupted between ecotypes. Furthermore, we examined how genome-wide patterns of sequence divergence correspond to divergence in transcript levels and isoform proportions and find evidence for both cis and trans-regulation. Together, our results emphasize that alternative splicing has been an underappreciated mechanism providing source material for natural selection at short evolutionary time scales.

基因表达的调控是基因型和表型之间的关键联系，解释了物种内的重大遗传变异。然而，我们才刚刚开始了解特定基因调控机制如何促进种群的适应性分化。在植物中，选择性剪接（AS）的转录后调控机制在发育和非生物胁迫反应中发挥着重要作用，使其成为自然选择引人注目的潜在目标。AS 允许生物体从单个基因产生多种不同的转录本/蛋白质，因此可能提供进化新颖性的来源。在这里，我们研究了选择性剪接和基因表达水平的变化是否可能有助于美国科罗拉多州大沙丘国家公园沙丘适应草原向日葵的适应和早期物种形成。我们进行了一项常见的花园实验来评估生态型之间的转录组变异，并分析差异表达、差异剪接和基因共表达。我们表明，即使在共同的环境中生长，单个基因在转录水平和替代亚型比例方面也存在强烈差异，并且基因共表达网络在生态型之间被破坏。此外，我们研究了全基因组序列分歧模式如何对应于转录水平和亚型比例的分歧，并找到顺式和反式调节的证据。总之，我们的结果强调，选择性剪接一直是一种未被充分重视的机制，为短进化时间尺度的自然选择提供了源材料。