Incipient sympatric speciation in blind mole rat, Spalax galili, in Israel, caused by sharp ecological divergence of abutting chalk-basalt ecologies, has been proposed previously based on mitochondrial and whole-genome nuclear DNA. Here, we present new evidence, including transcriptome, DNA editing, microRNA, and codon usage, substantiating earlier evidence for adaptive divergence in the abutting chalk and basalt populations. Genetic divergence, based on the previous and new evidence, is ongoing despite restricted gene flow between the two populations. The principal component analysis, neighbor-joining tree, and genetic structure analysis of the transcriptome clearly show the clustered divergent two mole rat populations. Gene-expression level analysis indicates that the population transcriptome divergence is displayed not only by soil divergence but also by sex. Gene ontology enrichment of the differentially expressed genes from the two abutting soil populations highlights reproductive isolation. Alternative splicing variation of the two abutting soil populations displays two distinct splicing patterns. L-shaped FST distribution indicates that the two populations have undergone divergence with gene flow. Transcriptome divergent genes highlight neurogenetics and nutrition characterizing the chalk population, and energetics, metabolism, musculature, and sensory perception characterizing the abutting basalt population. Remarkably, microRNAs also display divergence between the two populations. The GC content is significantly higher in chalk than in basalt, and stress-response genes mostly prefer nonoptimal codons. The multiple lines of evidence of ecological-genomic and genetic divergence highlight that natural selection overrules the gene flow between the two abutting populations, substantiating the sharp ecological chalk-basalt divergence driving sympatric speciation.

Beijing Genomics Institute BGI Shenzhen Shenzhen 518083 China;

College of Chemistry and Life Science Zhejiang Normal University Jinhua Zhejiang 321004 China;

Department of Molecular Genetics and Microbiology School of Medicine Duke University Durham NC 27708;

Department of Zoology Faculty of Science University of South Bohemia 37005 Ceske Budejovice Czech Republic;

Faculty of Medicine Bar Ilan University Safed 13195 Israel;

Institute of Apicultural Research Chinese Academy of Agricultural Sciences Beijing 100093 China;

Institute of Apicultural Research Chinese Academy of Agricultural Sciences Beijing 100093 China; Institute of Evolution University of Haifa Haifa 3498838 Israel;

Institute of Evolution University of Haifa Haifa 3498838 Israel;

School of Life Sciences Zhengzhou University Zhengzhou 450001 Henan China

The Mina and Everard Goodman Faculty of Life Sciences Bar Ilan University Ramat Gan 52900 Israel;

The People's Hospital of Qinghai Province Xining 810007 China;

University of Chinese Academy of Sciences Beijing 100049 China;

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