Significance: Speciation is the basis of the origin of biodiversity in nature. Sympatric speciation (SS) is still a controversial model of the origin of new species, since first proposed by Darwin in 1859. Here, we complement earlier genomic evidence with new analyses of transcriptome profiling, DNA editing, and microRNA, examined in the blind subterranean rodent, Spalax galili , in the Galilee Mountains, Israel, all substantiating SS with gene flow. Gene ontology enrichment of differentially expressed genes, in the abutting soil populations, highlights evolving reproductive isolation, despite a few interpopulation recombinants. Because sharply divergent geological, edaphic, climatic, and biotic interfaces abound in nature, we conclude that SS may be a common model of the origin of new species, as envisaged by Darwin.

Significance: Sympatric speciation (SS) has always been controversial since it was proposed by Darwin. Recently, we showed SS empirically in Spalax by amplified fragment-length polymorphism (AFLP), mitochondrial, and nuclear genomes. Similarly, SS in spiny mice, Acomys , from Evolution Canyon I (EC I), was earlier proposed by mtDNA and AFLP. Here, we show that full transcriptome data substantiates SS under sharp microclimatic and ecological divergence with gene flow, displaying extensive adaptive complexes to slope-specific stresses coupled with habitat choice and signals of reproductive isolation. Remarkably, strong natural selection across a sharply divergent ecological microsite overrules gene flow and advances SS, which is common at EC I. Because microsite ecological, geological, edaphic, and climatic divergences are widespread in nature, we conclude that SS might be a common mode of speciation.