Parallelism in gene expression between foothill and alpine ecotypes in Arabidopsis arenosa

Abstract

Parallel adaptation results from the independent evolution of similar traits between closely related lineages and allows us to test to what extent evolution is repeatable. Similar gene expression changes are often detected but the identity of genes shaped by parallel selection and the causes of expression parallelism remain largely unknown. By comparing genomes and transcriptomes of four distinct foothill-alpine population pairs across four treatments, we addressed the genetic underpinnings, plasticity and functional consequences of gene expression parallelism in alpine adaptation. Seeds of eight populations of Arabidopsis arenosa were raised under four treatments that differed in temperature and irradiance, factors varying strongly with elevation. Parallelism in differential gene expression between the foothill and alpine ecotypes was quantified by RNA-seq in leaves of young plants. By manipulating temperature and irradiance, we also tested for parallelism in plasticity (i.e., gene-environment interaction, GEI). In spite of global non-parallel patterns transcriptome wide, we found significant parallelism in gene expression at the level of individual loci with an over-representation of genes involved in biotic stress response. In addition, we demonstrated significant parallelism in GEI, indicating a shared differential response of the originally foothill versus alpine populations to environmental variation across mountain regions. A fraction of genes showing expression parallelism also encompassed parallel outliers for genomic differentiation, with greater enrichment of such variants in cis-regulatory elements in some mountain regions. In summary, our results suggest frequent evolutionary repeatability in gene expression changes associated with the colonization of a challenging environment that combines constitutive expression differences and plastic interaction with the surrounding environment.

Keywords: Arabidopsis arenosa; alpine adaptation; common garden experiment; gene expression; gene-environment interaction; parallel evolution; plasticity.