Sympatric speciation of spiny mice, Acomys, unfolded transcriptomically at Evolution Canyon, Israel

Kexin Li, Huihua Wang, Zhenyuan Cai, Liuyang Wang, Qinqin Xu, Matej Lövy, Zhenlong Wang, Eviatar Nevo

Research output: Contribution to journalArticlepeer-review

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.

Original languageEnglish
Pages (from-to)8254-8259
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number29
DOIs
StatePublished - 19 Jul 2016

Bibliographical note

Funding Information:
We thank Robin Permut and Avigdor Beiles (University of Haifa) for commenting on the manuscript and Xiaoying Song for her technical assistance. The following foundations supported this work financially: Agricultural Science and Technology Innovation Program Grant CAAS-ASTIP-2016-IAR, the Ancell-Teicher Research Foundation for Genetics and Molecular Evolution, National Natural Science Foundation of China Grant 31372193, Foundation of Henan Educational Committee Grant 13A180717, and Czech Science Foundation Project 14-31670P.

Keywords

  • Adaptive ecological speciation
  • Microclimate
  • Natural selection
  • RNA-seq

ASJC Scopus subject areas

  • General

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