title: Genome-wide evidence for speciation with gene flow in Heliconius butterflies.
abstract: Most speciation events probably occur gradually, without complete and immediate reproductive isolation, but the full extent of gene flow between diverging species has rarely been characterized on a genome-wide scale. Documenting the extent and timing of admixture between diverging species can clarify the role of geographic isolation in speciation. Here we use new methodology to quantify admixture at different stages of divergence in Heliconius butterflies, based on whole-genome sequences of 31 individuals. Comparisons between sympatric and allopatric populations of H. melpomene, H. cydno, and H. timareta revealed a genome-wide trend of increased shared variation in sympatry, indicative of pervasive interspecific gene flow. Up to 40% of 100-kb genomic windows clustered by geography rather than by species, demonstrating that a very substantial fraction of the genome has been shared between sympatric species. Analyses of genetic variation shared over different time intervals suggested that admixture between these species has continued since early in speciation. Alleles shared between species during recent time intervals displayed higher levels of linkage disequilibrium than those shared over longer time intervals, suggesting that this admixture took place at multiple points during divergence and is probably ongoing. The signal of admixture was significantly reduced around loci controlling divergent wing patterns, as well as throughout the Z chromosome, consistent with strong selection for Müllerian mimicry and with known Z-linked hybrid incompatibility. Overall these results show that species divergence can occur in the face of persistent and genome-wide admixture over long periods of time.
authors.affiliation: Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom;
authors.forename: Simon H
authors.initials: SH
authors.lastname: Martin
authors.forename: Kanchon K
authors.initials: KK
authors.lastname: Dasmahapatra
authors.forename: Nicola J
authors.initials: NJ
authors.lastname: Nadeau
authors.forename: Camilo
authors.initials: C
authors.lastname: Salazar
authors.forename: James R
authors.initials: JR
authors.lastname: Walters
authors.forename: Fraser
authors.initials: F
authors.lastname: Simpson
authors.forename: Mark
authors.initials: M
authors.lastname: Blaxter
authors.forename: Andrea
authors.initials: A
authors.lastname: Manica
authors.forename: James
authors.initials: J
authors.lastname: Mallet
authors.forename: Chris D
authors.initials: CD
authors.lastname: Jiggins
mesh_terms: D000483:Alleles; D000818:Animals; D002080:Butterflies / Q000145:classification / Q000235:genetics*; D019143:Evolution, Molecular; D051456:Gene Flow; D017344:Genes, Insect; D049810:Genetic Speciation; D014644:Genetic Variation; D016678:Genome; D049750:Genome, Insect; D015810:Linkage Disequilibrium; D010641:Phenotype; D010802:Phylogeny; D012730:Sex Chromosomes / Q000235:genetics; D061350:Sympatry
references.citation: Evolution. 2011 May;65(5):1489-500
references.pmid: 21521198
references.citation: Evolution. 2001 Aug;55(8):1631-8
references.pmid: 11580022
references.citation: Evol Dev. 2003 May-Jun;5(3):269-80
references.pmid: 12752766
references.citation: PLoS Genet. 2010 Feb 26;6(2):e1000862
references.pmid: 20195501
references.citation: Mol Biol Evol. 1998 May;15(5):538-43
references.pmid: 9580982
references.citation: Genome Res. 2012 Aug;22(8):1499-511
references.pmid: 22534282
references.citation: Science. 2010 May 7;328(5979):710-722
references.pmid: 20448178
references.citation: PLoS Genet. 2009 Jul;5(7):e1000550
references.pmid: 19578407
references.citation: Mol Biol Evol. 2011 Aug;28(8):2239-52
references.pmid: 21325092
references.citation: Trends Ecol Evol. 2005 May;20(5):229-37
references.pmid: 16701374
references.citation: Genome Res. 2013 Aug;23(8):1248-57
references.pmid: 23674305
references.citation: Syst Biol. 2008 Oct;57(5):758-71
references.pmid: 18853362
references.citation: PLoS Genet. 2012;8(6):e1002752
references.pmid: 22737081
references.citation: Trends Ecol Evol. 2011 Aug;26(8):389-97
references.pmid: 21592615
references.citation: Am Nat. 2005 Jul;166(1):56-67
references.pmid: 15937789
references.citation: Genetics. 2002 Aug;161(4):1517-26
references.pmid: 12196397
references.citation: Nature. 2009 Sep 24;461(7263):489-94
references.pmid: 19779445
references.citation: Mol Ecol. 2010 Mar;19(5):848-50
references.pmid: 20456221
references.citation: Mol Ecol. 2009 Feb;18(3):375-402
references.pmid: 19143936
references.citation: PLoS Biol. 2005 Sep;3(9):e285
references.pmid: 16076241
references.citation: Mol Biol Evol. 2002 Apr;19(4):472-88
references.pmid: 11919289
references.citation: PLoS Genet. 2012;8(10):e1002947
references.pmid: 23055938
references.citation: PLoS Genet. 2010 Feb 05;6(2):e1000794
references.pmid: 20140188
references.citation: Trends Genet. 2012 Jul;28(7):342-50
references.pmid: 22520730
references.citation: Philos Trans R Soc Lond B Biol Sci. 2012 Feb 5;367(1587):395-408
references.pmid: 22201169
references.citation: BMC Biol. 2006 Apr 21;4:11
references.pmid: 16630334
references.citation: BMC Evol Biol. 2008 May 02;8:132
references.pmid: 18454858
references.citation: Nature. 2012 Aug 16;488(7411):370-4
references.pmid: 22801491
references.citation: Am Nat. 2002 Mar;159 Suppl 3:S22-35
references.pmid: 18707367
references.citation: Curr Biol. 2009 Feb 10;19(3):R119-22
references.pmid: 19211049
references.citation: Mol Ecol Resour. 2010 Mar;10(2):378-84
references.pmid: 21565033
references.citation: Science. 2009 Dec 18;326(5960):1704-7
references.pmid: 19965377
references.citation: Proc Biol Sci. 2012 Dec 22;279(1749):4907-13
references.pmid: 23075843
references.citation: BMC Evol Biol. 2008 Nov 28;8:324
references.pmid: 19040737
references.citation: Nat Genet. 2011 May;43(5):491-8
references.pmid: 21478889
references.citation: BMC Genet. 2012 Apr 11;13:27
references.pmid: 22494792
references.citation: BMC Evol Biol. 2007 Feb 23;7:28
references.pmid: 17319954
references.citation: Evolution. 2006 Jun;60(6):1254-68
references.pmid: 16892975
references.citation: Evolution. 2013 Sep;67(9):2483-97
references.pmid: 24033162
references.citation: Heredity (Edinb). 2009 Dec;103(6):439-44
references.pmid: 19920849
references.citation: Philos Trans R Soc Lond B Biol Sci. 2012 Feb 5;367(1587):343-53
references.pmid: 22201164
references.citation: Proc Natl Acad Sci U S A. 2010 May 25;107(21):9724-9
references.pmid: 20457907
references.citation: Science. 2010 Oct 22;330(6003):512-4
references.pmid: 20966253
references.citation: Mol Ecol. 2011 Dec;20(24):5123-40
references.pmid: 22066935
references.citation: Proc Biol Sci. 2011 Feb 22;278(1705):511-8
references.pmid: 20810445
references.citation: Bioinformatics. 2006 Nov 1;22(21):2688-90
references.pmid: 16928733
references.citation: Science. 2009 Nov 6;326(5954):847-50
references.pmid: 19892982
references.citation: Bioinformatics. 2010 May 15;26(10):1372-3
references.pmid: 20228129
references.citation: Genome Res. 2011 Jun;21(6):936-9
references.pmid: 20980556
references.citation: Bioinformatics. 2009 Aug 15;25(16):2078-9
references.pmid: 19505943
references.citation: Proc Biol Sci. 2012 Dec 22;279(1749):5058-65
references.pmid: 22696527
references.citation: Heredity (Edinb). 2009 Jan;102(1):4-15
references.pmid: 18781167
references.citation: Nature. 2012 Jul 5;487(7405):94-8
references.pmid: 22722851
references.citation: Proc Natl Acad Sci U S A. 2012 Aug 28;109(35):13956-60
references.pmid: 22893688
references.citation: Nature. 2012 Nov 29;491(7426):756-60
references.pmid: 23103876
references.citation: Hum Hered. 2007;64(1):45-51
references.pmid: 17483596
references.citation: Mol Ecol. 2013 Feb;22(3):814-26
references.pmid: 22924870