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Proc Natl Acad Sci U S A. 2018 Jan 9;115(2):E236-E243. doi: 10.1073/pnas.1713288114. Epub 2017 Dec 26.

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

Author information

1
Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, People's Republic of China.
2
State Key Laboratory of Grassland Agro-ecosystem, College of Life Sciences, Lanzhou University, Lanzhou 730000, People's Republic of China.
3
Natural Resources and Watershed Management Administration of Khorasan Razavi, Khorasan 9177948974, Iran.
4
School of Biology, University of St. Andrews, St. Andrews, Fife KY16 9TH, United Kingdom.
5
Department of Ecology and Genetics, Evolutionary Biology Center and Science for Life Laboratory, Uppsala University, Uppsala 75236, Sweden.
6
Institute of Evolution, University of Haifa, Mount Carmel, Haifa 3498838, Israel liujq@nwipb.cas.cn nevo@research.haifa.ac.il.
7
Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, People's Republic of China; liujq@nwipb.cas.cn nevo@research.haifa.ac.il.

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.

KEYWORDS:

gene flow; genome divergence; natural selection; paraphyletic; speciation

PMID:
29279400
PMCID:
PMC5777044
DOI:
10.1073/pnas.1713288114
[Indexed for MEDLINE]
Free PMC Article

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