Ancient polymorphisms and divergence hitchhiking contribute to genomic islands of divergence within a poplar species complex

Tao Ma, Kun Wang, Quanjun Hu, Zhenxiang Xi, Dongshi Wan, Qian Wang, Jianju Feng, Dechun Jiang, Hamid Ahani, Richard J. Abbott, Martin Lascoux, Eviatar Nevo, Jianquan Liu

Research output: Contribution to journalArticlepeer-review

Abstract

How genome divergence eventually leads to speciation is a topic of prime evolutionary interest. Genomic islands of elevated divergence are frequently reported between diverging lineages, and their size is expected to increase with time and gene flow under the speciation-with-gene-flow model. However, such islands can also result from divergent sorting of ancient polymorphisms, recent ecological selection regardless of gene flow, and/or recurrent background selection and selective sweeps in low-recombination regions. It is challenging to disentangle these nonexclusive alternatives, but here we attempt to do this in an analysis of what drove genomic divergence between four lineages comprising a species complex of desert poplar trees. Within this complex we found that two morphologically delimited species, Populus euphratica and Populus pruinosa, were paraphyletic while the four lineages exhibited contrasting levels of gene flow and divergence times, providing a good system for testing hypotheses on the origin of divergence islands. We show that the size and number of genomic islands that distinguish lineages are not associated with either rate of recent gene flow or time of divergence. Instead, they are most likely derived from divergent sorting of ancient polymorphisms and divergence hitchhiking. We found that highly diverged genes under lineage-specific selection and putatively involved in ecological and morphological divergence occur both within and outside these islands. Our results highlight the need to incorporate demography, absolute divergence measurement, and gene flow rate to explain the formation of genomic islands and to identify potential genomic regions involved in speciation.

Original languageEnglish
Pages (from-to)E236-E243
JournalProceedings of the National Academy of Sciences of the United States of America
Volume115
Issue number2
DOIs
StatePublished - 9 Jan 2017

Bibliographical note

Funding Information:
We thank Drs. Lakhdar Khelifi and Abdelkader Morsli (Laboratoire des Ressources G?n?tiques et Biotechnologies, Ecole Nationale Sup?rieure Agronomique, Algiers) for helping collect materials from Algeria. Financial support was provided by National Natural Science Foundation of China (91731301, 31590821, 31500502, and 31561123001), National Key Research and Development Program of China (2016YFD0600101), National High Technology Research and Development Program of China (863 Program, No. 2013AA100605), Youth Science and Technology Innovation Team of Province (2014TD003), National Key Project for Basic Research (2012CB114504), Ministry of Science and Technology of the People's Republic of China (2010DFA34610), International Collaboration 111 Projects of China, and the 985 and 211 Projects of Sichuan University.

Funding Information:
Supérieure Agronomique, Algiers) for helping collect materials from Algeria. Financial support was provided by National Natural Science Foundation of China (91731301, 31590821, 31500502, and 31561123001), National Key Research and Development Program of China (2016YFD0600101), National High Technology Research and Development Program of China (863 Program, No.

Funding Information:
2013AA100605), Youth Science and Technology Innovation Team of Province (2014TD003), National Key Project for Basic Research (2012CB114504), Ministry of Science and Technology of the People’s Republic of China (2010DFA34610), International Collaboration 111 Projects of China, and the 985 and 211 Projects of Sichuan University.

Keywords

  • Gene flow
  • Genome divergence
  • Natural selection
  • Paraphyletic
  • Speciation

ASJC Scopus subject areas

  • General

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