Sympatric speciation of the spiny mouse from Evolution Canyon in Israel substantiated genomically and methylomically

Yinjia Wang, Zhenglei Qiao, Leyan Mao, Fang Li, Xiaolong Liang, Xuan An, Shangzhe Zhang, Xi Liu, Zhuoran Kuang, Na Wan, Eviatar Nevo, Kexin Li

Research output: Contribution to journalArticlepeer-review

Abstract

Speciation with ongoing homogenizing gene flow, later dubbed sympatric speciation, has been a fascinating and debated topic since Darwin proposed it. Here, we analyzed sympatric speciation of the spiny mouse, Acomys cahirinus, from Evolution Canyon I, Mount Carmel, Israel, revealed by whole-genome, methylome, and behavior comparisons. Mitochondrial phylogeny indicated that the tropical African Slope (AS) and temperate European Slope (ES) populations were sister taxa and shared a common ancestor. Based on the de novo chromosomal-level genome, we compared the genome and methylome of the two populations from EC I. We found clear-cut divergences between them based on both single nucleotide polymorphisms (SNPs) and structure variations (SVs). We identified 440 highly diverged regions and found olfactory receptors significantly divergent between slopes, suggesting prezygotic reproductive isolation. Furthermore, genes related to adaptation were enriched in immunity, temperature homeostasis in AS and energy, and cell cycle in ES. Population demographic modeling showed that the AS and ES populations split from the same ancestor with decreasing gene flow, implying sympatric speciation. Epigenetic methylation divergence preceded genetic differentiation and facilitated slope adaptation and sympatric speciation. We found a significant difference in activity onset in laboratory between the two populations, associated with the methylation divergence of circadian genes. We concluded that behavioral, genomic, and methylomic divergence substantiated sympatric speciation of Acomys from EC I in Israel, shown earlier transcriptomically.

Original languageEnglish
Article numbere2121822119
JournalProceedings of the National Academy of Sciences of the United States of America
Volume119
Issue number13
DOIs
StatePublished - 29 Mar 2022

Bibliographical note

Funding Information:
ACKNOWLEDGMENTS. This project was supported by the National Natural Science Foundation of China (32071487), National Key Research and Development Programs (2021YFD1200900), Science Fund for Creative Research Groups of Gansu Province (21JR7RA533), Lanzhou University’s “Double First-Class” Guided Project-Team Building Funding-Research Startup Fee for Kexin Li, Chang Jiang Scholars Program, The Fundamental Research Funds for Excellent Youth from the Central Universities, LZU (lzujbky-2021-ey17, lzujbky-2020-ct02), a grant from State Key Laboratory of Grassland Agro-Ecosystems (Lanzhou University) (Grant Numbers: SKLGAE-202001, 202009, and 202010). We are also grateful to the Ancell-Teicher Research Foundation for Genetic and Molecular Evolution for its constant financial support for the Spalax research program. We received support for computational work from the Big Data Computing Platform for Western Ecological Environment and Regional Development and Supercomputing Center of Lanzhou University.

Publisher Copyright:
© 2022 the Author(s).

Keywords

  • adaptation j population genetics j methylation j genome divergence j sympatric speciation

ASJC Scopus subject areas

  • General

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