Speciation mechanisms remain controversial. Two speciation models occur in Israeli subterranean mole rats, genus Spalax: a regional speciation cline southward of four peripatric climatic chromosomal species and a local, geologic-edaphic, genic, and sympatric speciation. Here we highlight their genome evolution. The five species were separated into five genetic clusters by single nucleotide polymorphisms, copy number variations (CNVs), repeatome, and methylome in sympatry. The regional interspecific divergence correspond to Pleistocene climatic cycles. Climate warmings caused chromosomal speciation. Triple effective population size, Ne , declines match glacial cold cycles. Adaptive genes evolved under positive selection to underground stresses and to divergent climates, involving interspecies reproductive isolation. Genomic islands evolved mainly due to adaptive evolution involving ancient polymorphisms. Repeatome, including both CNV and LINE1 repetitive elements, separated the five species. Methylation in sympatry identified geologically chalk-basalt species that differentially affect thermoregulation, hypoxia, DNA repair, P53, and other pathways. Genome adaptive evolution highlights climatic and geologic-edaphic stress evolution and the two speciation models, peripatric and sympatric.

Department of Gastroenterology The 305 Hospital of PLA 100017 Beijing China

Faculty of Science University of South Bohemia 370 05 České Budejovice Czech Republic

Institute of Evolution University of Haifa 3498838 Haifa Israel

Institute of Evolution University of Haifa 3498838 Haifa Israel;

Leibniz Institute for Zoo and Wildlife Research 10315 Berlin Germany

Sagol Department of Neurobiology University of Haifa Haifa 3498838 Israel

School of Public Health Lanzhou University Lanzhou 730000 China

State Key Laboratory of Grassland Agro Ecosystem Institute of Innovation Ecology Lanzhou University 730000 Lanzhou China

State Key Laboratory of Grassland Agro Ecosystem Institute of Innovation Ecology Lanzhou University 730000 Lanzhou China;

Tauber Bioinformatics Research Center Haifa 3498838 Israel

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