Spiny mice, Acomys cahirinus, colonized Israel 30,000 y ago from dry tropical Africa and inhabited rocky habitats across Israel. Earlier, we had shown by mtDNA that A. cahirinus incipiently sympatrically speciates at Evolution Canyon I (EC I) in Mount Carmel, Israel because of microclimatic interslope divergence. The EC I microsite consists of a dry and hot savannoid "African" slope (AS) and an abutting humid and cool-forested "European" slope (ES). Here, we substantiate incipient SS in A. cahirinus at EC I based on the entire transcriptome, showing that multiple slope-specific adaptive complexes across the transcriptome result in two divergent clusters. Tajima's D distribution of the abutting Acomys interslope populations shows that the ES population is under stronger positive selection, whereas the AS population is under balancing selection, harboring higher genetic polymorphisms. Considerable sites of the two populations were differentiated with a coefficient of FST = 0.25-0.75. Remarkably, 24 and 37 putatively adaptively selected genes were detected in the AS and ES populations, respectively. The AS genes involved DNA repair, growth arrest, neural cell differentiation, and heat-shock proteins adapting to the local AS stresses of high solar radiation, drought, and high temperature. In contrast, the ES genes involved high ATP associated with energetics stress. The sharp ecological interslope divergence led to strong slope-specific selection overruling the interslope gene flow. Earlier tests suggested slope-specific mate choice. Habitat interslope-adaptive selection across the transcriptome and mate choice substantiate sympatric speciation (SS), suggesting its prevalence at EC I and commonality in nature.

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

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;

Institute of Evolution University of Haifa Haifa 3498838 Israel; Department of Zoology Faculty of Science University of South Bohemia 37005 Ceske Budejovice Czech Republic;

Key Laboratory of Adaptation and Evolution of Plateau Biota Northwest Institute of Plateau Biology Chinese Academy of Sciences Xining 810001 China;

School of Life Sciences Zhengzhou University Zhengzhou 450001 China

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

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