The genomic basis of adaptive divergence and speciation in Senecio (Asteraceae)

Cases of ecological speciation, such as divergence between high altitude Senecio aethnensis and low altitude Senecio chrysanthemifolius(Asteraceae) on Mount Etna (Sicily), provide an attractive opportunity to study the formation of distinct species driven by adaptation to contrasting environments. Here we use transcriptome sequencing, a genome scan, and linkage mapping to investigate how genetic divergence builds up between the genomes of these two species.

Out of ca. 18,000 genes analysed, only a small number (90) displayed differential expression between the two species, consistent with diversifying selection at only a handful of loci maintaining taxonomically well-defined species, despite on-going gene flow. A high-density genetic map of the Senecio genome, demonstrates that loci under diversifying selection cluster in three 5 cM regions characterised by the greatest marker density, possibly corresponding to ‘cold-spots’ of recombination, such as centromeres or chromosomal inversions. Loci in these regions show significantly higher species genetic differentiation (F_ST) than the remainder of the genome, but this is likely due to locally reduced polymorphism in these clusters and not due to higher species divergence; average sequence divergence between the species, d_XY, is not significantly elevated in the clusters.

We also detected three genomic regions with significant transmission ratio distortion (TRD), possibly indicating accumulation of intrinsic genetic incompatibilities between these recently diverged species. One of the TRD regions overlapped with a cluster of high species differentiation, indicating that divergence of these species may have occurred due to a complex interplay of ecological divergence and accumulation of intrinsic genetic incompatibilities.