title: Sympatric speciation of spiny mice, Acomys, unfolded transcriptomically at Evolution Canyon, Israel.
abstract: 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.
authors.affiliation: Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, China; Institute of Evolution, University of Haifa, Haifa 3498838, Israel; nevo@research.haifa.ac.il likexin323@gmail.com wzl@zzu.edu.cn.
authors.forename: Kexin
authors.initials: K
authors.lastname: Li
authors.affiliation: Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, China;
authors.forename: Huihua
authors.initials: H
authors.lastname: Wang
authors.affiliation: Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810001, China;
authors.forename: Zhenyuan
authors.initials: Z
authors.lastname: Cai
authors.affiliation: Department of Molecular Genetics and Microbiology, School of Medicine, Duke University, Durham, NC 27708;
authors.forename: Liuyang
authors.initials: L
authors.lastname: Wang
authors.affiliation: The People's Hospital of Qinghai Province, Xining 810007, China;
authors.forename: Qinqin
authors.initials: Q
authors.lastname: Xu
authors.affiliation: Institute of Evolution, University of Haifa, Haifa 3498838, Israel; Department of Zoology, Faculty of Science, University of South Bohemia, 37005 Ceske Budejovice, Czech Republic;
authors.forename: Matěj
authors.initials: M
authors.lastname: Lövy
authors.affiliation: School of Life Sciences, Zhengzhou University, Zhengzhou 450001, China nevo@research.haifa.ac.il likexin323@gmail.com wzl@zzu.edu.cn.
authors.forename: Zhenlong
authors.initials: Z
authors.lastname: Wang
authors.affiliation: Institute of Evolution, University of Haifa, Haifa 3498838, Israel; nevo@research.haifa.ac.il likexin323@gmail.com wzl@zzu.edu.cn.
authors.forename: Eviatar
authors.initials: E
authors.lastname: Nevo
mesh_terms: D000818:Animals; D005075:Biological Evolution; D001921:Brain / Q000378:metabolism; D051456:Gene Flow; D049810:Genetic Speciation; D007557:Israel; D008834:Microclimate; D051189:Murinae / Q000235:genetics*; D020641:Polymorphism, Single Nucleotide; D059467:Transcriptome
keywords: RNA-seq; adaptive ecological speciation; microclimate; natural selection