Gene expression and alternative splicing contribute to adaptive divergence of ecotypes

Abstract

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. Alternative splicing (AS) is a post-transcriptional regulatory mechanism in eukaryotes that generates multiple different transcripts (isoforms) from a single gene and thus may provide a source of evolutionary novelty. In plants, AS a compelling potential target of natural selection because it plays important roles in both development and abiotic stress response. We investigated 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 between 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, 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 a substantial contribution of trans-regulation. Genes that show significant differential expression and/or differential splicing are enriched for functions involving seed development, abiotic stress response, nutrient acquisition, and photosynthesis, some of which relate to known adaptive traits. Our results emphasize that alternative splicing has been underappreciated as a mechanism providing variation for natural selection to act upon at short time scales.