OpenLB
Open Library of Bioscience
Advanced Search
Proceedings of the National Academy of Sciences of the United States of America
01 09, 2018;115 (2): E236-E243.

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
Author Information
  1. Tao Ma: 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. Kun Wang: 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.
  3. Quanjun Hu: 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.
  4. Zhenxiang Xi: 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.
  5. Dongshi Wan: State Key Laboratory of Grassland Agro-ecosystem, College of Life Sciences, Lanzhou University, Lanzhou 730000, People's Republic of China.
  6. Qian Wang: 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.
  7. Jianju Feng: State Key Laboratory of Grassland Agro-ecosystem, College of Life Sciences, Lanzhou University, Lanzhou 730000, People's Republic of China.
  8. Dechun Jiang: State Key Laboratory of Grassland Agro-ecosystem, College of Life Sciences, Lanzhou University, Lanzhou 730000, People's Republic of China.
  9. Hamid Ahani: Natural Resources and Watershed Management Administration of Khorasan Razavi, Khorasan 9177948974, Iran.
  10. Richard J Abbott: School of Biology, University of St. Andrews, St. Andrews, Fife KY16 9TH, United Kingdom.
  11. Martin Lascoux: Department of Ecology and Genetics, Evolutionary Biology Center and Science for Life Laboratory, Uppsala University, Uppsala 75236, Sweden. ORCID
  12. Eviatar Nevo: Institute of Evolution, University of Haifa, Mount Carmel, Haifa 3498838, Israel liujq@nwipb.cas.cn nevo@research.haifa.ac.il.
  13. Jianquan Liu: 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.
PMID: 29279400 DOI: 10.1073/pnas.1713288114

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, and , 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

References

Genome Res. 2015 Nov;25(11):1656-65 [PMID: 26355005]
Nature. 2011 Jul 13;475(7357):493-6 [PMID: 21753753]
BMC Bioinformatics. 2014 Nov 25;15:356 [PMID: 25420514]
Mol Ecol. 2016 Jun;25(11):2337-60 [PMID: 26836441]
Science. 2014 May 16;344(6185):738-42 [PMID: 24833390]
Mol Ecol. 2016 Jun;25(11):2542-58 [PMID: 27206531]
Genome Res. 2013 Nov;23(11):1817-28 [PMID: 24045163]
BMC Plant Biol. 2013 Dec 11;13:210 [PMID: 24330668]
PLoS One. 2012;7(7):e37558 [PMID: 22911679]
Science. 2010 Jul 2;329(5987):75-8 [PMID: 20595611]
Nat Ecol Evol. 2017 Feb 17;1(4):82 [PMID: 28812654]
Nature. 1992 Apr 9;356(6369):519-20 [PMID: 1560824]
Nat Rev Genet. 2017 Feb;18(2):87-100 [PMID: 27840429]
Nat Commun. 2014 Jun 25;5:4248 [PMID: 24963649]
Philos Trans R Soc Lond B Biol Sci. 2012 Feb 5;367(1587):343-53 [PMID: 22201164]
Mol Biol Evol. 2016 Jul;33(7):1754-67 [PMID: 26983554]
PLoS Genet. 2012;8(11):e1002967 [PMID: 23166502]
Philos Trans R Soc Lond B Biol Sci. 2012 Feb 5;367(1587):451-60 [PMID: 22201174]
Mol Ecol. 2014 Feb;23(2):311-24 [PMID: 26010734]
Mol Ecol. 2009 Feb;18(3):375-402 [PMID: 19143936]
PLoS Biol. 2005 Sep;3(9):e285 [PMID: 16076241]
Genome Res. 2006 Jun;16(6):730-7 [PMID: 16687734]
J Evol Biol. 2017 Aug;30(8):1450-1477 [PMID: 28786193]
Nature. 2012 Nov 29;491(7426):756-60 [PMID: 23103876]
Genetics. 2013 Jun;194(2):459-71 [PMID: 23535385]
Nat Rev Genet. 2014 Mar;15(3):176-92 [PMID: 24535286]
Nat Commun. 2016 May 31;7:11693 [PMID: 27243207]
PLoS Genet. 2015 Feb 13;11(2):e1004966 [PMID: 25679225]
Front Plant Sci. 2017 Jan 04;7:2022 [PMID: 28101098]
Heredity (Edinb). 2009 Dec;103(6):439-44 [PMID: 19920849]
Mol Ecol. 2015 Aug;24(16):4238-51 [PMID: 26175196]
Plant Cell. 2007 Feb;19(2):473-84 [PMID: 17307931]
Plant Cell Physiol. 2012 Jul;53(7):1283-94 [PMID: 22619471]
Mol Ecol. 2014 Jul;23 (13):3133-57 [PMID: 24845075]
Genome Res. 2017 Jun;27(6):1004-1015 [PMID: 28442558]
Cell. 2017 Jun 15;169(7):1177-1186 [PMID: 28622505]
Am J Hum Genet. 2007 Nov;81(5):1084-97 [PMID: 17924348]
Mol Ecol. 2010 Mar;19(5):848-50 [PMID: 20456221]
PLoS Genet. 2013 Oct;9(10):e1003905 [PMID: 24204310]
Science. 2010 Oct 22;330(6003):512-4 [PMID: 20966253]
Genetics. 2013 Nov;195(3):693-702 [PMID: 24026093]
Bioinformatics. 2010 Aug 15;26(16):2064-5 [PMID: 20591904]
Nat Commun. 2013;4:1827 [PMID: 23652015]
PLoS Genet. 2014 Aug 28;10(8):e1003519 [PMID: 25166595]
Science. 2014 Jun 20;344(6190):1410-4 [PMID: 24948738]
Nat Rev Genet. 2003 Dec;4(12 ):981-94 [PMID: 14631358]
Evolution. 2010 Jun;64(6):1729-47 [PMID: 20624183]
Heredity (Edinb). 2014 Feb;112(2):156-64 [PMID: 24065180]
Nature. 2014 Sep 18;513(7518):375-381 [PMID: 25186727]
Nat Commun. 2015 Aug 13;6:7960 [PMID: 26268845]
PLoS Genet. 2016 Feb 29;12(2):e1005887 [PMID: 26925837]
Plant Cell. 2006 Jun;18(6):1383-95 [PMID: 16679458]
Plant Cell. 2010 Nov;22(11):3574-88 [PMID: 21119060]
Genetics. 1987 May;116(1):153-9 [PMID: 3110004]
Science. 2015 Dec 18;350(6267):1493-1498 [PMID: 26680190]
Nat Commun. 2016 Oct 31;7:13195 [PMID: 27796282]
Nat Commun. 2013;4:2797 [PMID: 24256998]
Mol Ecol. 2016 Sep;25(18):4488-507 [PMID: 27484941]

MeSH Term

Biological Evolution
Chromosome Mapping
Chromosomes, Plant
Genetic Speciation
Genome, Plant
Genomic Islands
Polymorphism, Genetic
Populus
Journal Article Research Support, Non-U.S. Gov't

Word Cloud

Similar Articles

Cited By