Sympatric speciation of wild emmer wheat driven by ecology and chromosomal rearrangements

Hongwei Wang, Huayan Yin, Chengzhi Jiao, Xiaojian Fang, Guiping Wang, Guangrong Li, Fei Ni, Penghuan Li, Peisen Su, Wenyang Ge, Zhongfan Lyu, Shoushen Xu, Yanhong Yang, Yongchao Hao, Xinxin Cheng, Jinxiao Zhao, Cheng Liu, Fengfeng Xu, Xin Ma, Silong SunYan Zhao, Yinguang Bao, Cheng Liu, Jingjing Zhang, Tomas Pavlicek, Anfei Li, Zujun Yang, Eviatar Nevo, Lingrang Kong

Research output: Contribution to journalArticlepeer-review

Abstract

In plants, the mechanism for ecological sympatric speciation (SS) is little known. Here, after ruling out the possibility of secondary contact, we show that wild emmer wheat, at the microclimatically divergent microsite of “Evolution Canyon” (EC), Mt. Carmel, Israel, underwent triple SS. Initially, it split following a bottleneck of an ancestral population, and further diversified to three isolated populations driven by disruptive ecological selection. Remarkably, two postzygotically isolated populations (SFS1 and SFS2) sympatrically branched within an area less than 30 m at the tropical hot and dry savannoid south-facing slope (SFS). A series of homozygous chromosomal rearrangements in the SFS1 population caused hybrid sterility with the SFS2 population. We demonstrate that these two populations developed divergent adaptive mechanisms against severe abiotic stresses on the tropical SFS. The SFS2 population evolved very early flowering, while the SFS1 population alternatively evolved a direct tolerance to irradiance by improved ROS scavenging activity that potentially accounts for its evolutionary fate with unstable chromosome status. Moreover, a third prezygotically isolated sympatric population adapted on the abutting temperate, humid, cool, and forested north-facing slope (NFS), separated by 250 m from the SFS wild emmer wheat populations. The NFS population evolved multiple resistant loci to fungal diseases, including powdery mildew and stripe rust. Our study illustrates how plants sympatrically adapt and speciate under disruptive ecological selection of abiotic and biotic stresses.

Original languageEnglish
Pages (from-to)5955-5963
Number of pages9
JournalProceedings of the National Academy of Sciences of the United States of America
Volume117
Issue number11
DOIs
StatePublished - 17 Mar 2020

Bibliographical note

Publisher Copyright:
© 2020 National Academy of Sciences. All rights reserved.

Keywords

  • Abiotic stress
  • Biotic stress
  • Robertsonian translocation
  • Sympatric speciation
  • Wild emmer wheat

ASJC Scopus subject areas

  • General

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