Rapid Speciation with Gene Flow Following the Formation of Mt. Etna

Environmental or geological changes can create new niches that drive ecological species divergence without the immediate cessation of gene flow. However, few such cases have been characterized. On a recently formed volcano, Mt. Etna, Senecio aethnensis and S. chrysanthemifolius inhabit contrasting environments of high and low altitude, respectively. They have very distinct phenotypes, despite hybridizing promiscuously, and thus may represent an important example of ecological speciation “in action,” possibly as a response to the rapid geological changes that Mt. Etna has recently undergone. To elucidate the species’ evolutionary history, and help establish the species as a study system for speciation genomics, we sequenced the transcriptomes of the two Etnean species, and the outgroup, S. vernalis, using Illumina sequencing. Despite the species’ substantial phenotypic divergence, synonymous divergence between the high- and low-altitude species was low (dS = 0.016 ± 0.017 [SD]). A comparison of species divergence models with and without gene flow provided unequivocal support in favor of the former and demonstrated a recent time of species divergence (153,080 ya ± 11,470 [SE]) that coincides with the growth of Mt. Etna to the altitudes that separate the species today. Analysis of dN/dS revealed wide variation in selective constraint between genes, and evidence that highly expressed genes, more “multifunctional” genes, and those with more paralogs were under elevated purifying selection. Taken together, these results are consistent with a model of ecological speciation, potentially as a response to the emergence of a new, high-altitude niche as the volcano grew.