Genomic Divergence during Speciation Driven by Adaptation to Altitude

Even though Darwin’s “On the Origin of Species” implied selection being the main driver of species formation, the role of natural selection in speciation remains poorly understood. In particular, it remains unclear how selection at a few genes can lead to genomewide divergence and the formation of distinct species. We used a particularly attractive clear-cut case of recent plant ecological speciation to investigate the demography and genomic bases of species formation driven by adaptation to contrasting conditions. High-altitude Senecio aethnensis and low-altitude S. chrysanthemifolius live at the extremes of a mountain slope on Mt. Etna, Sicily, and form a hybrid zone at intermediate altitudes but remain morphologically distinct. Genetic differentiation of these species was analyzed at the DNA polymorphism and gene expression levels by high-throughput sequencing of transcriptomes from multiple individuals. Out of ∼18,000 genes analyzed, only a small number (90) displayed differential expression between the two species. These genes showed significantly elevated species differentiation (F(ST) and D(xy)), consistent with diversifying selection acting on these genes. Genomewide genetic differentiation of the species is surprisingly low (F(ST) = 0.19), while ∼200 genes showed significantly higher (false discovery rate < 1%; mean outlier F(ST) > 0.6) interspecific differentiation and evidence for local adaptation. Diversifying selection at only a handful of loci may be enough for the formation and maintenance of taxonomically well-defined species, despite ongoing gene flow. This provides an explanation of why many closely related species (in plants, in particular) remain phenotypically and ecologically distinct despite ongoing hybridization, a question that has long puzzled naturalists and geneticists alike.