title: Multilocus species trees show the recent adaptive radiation of the mimetic heliconius butterflies.
abstract: Müllerian mimicry among Neotropical Heliconiini butterflies is an excellent example of natural selection, associated with the diversification of a large continental-scale radiation. Some of the processes driving the evolution of mimicry rings are likely to generate incongruent phylogenetic signals across the assemblage, and thus pose a challenge for systematics. We use a data set of 22 mitochondrial and nuclear markers from 92% of species in the tribe, obtained by Sanger sequencing and de novo assembly of short read data, to re-examine the phylogeny of Heliconiini with both supermatrix and multispecies coalescent approaches, characterize the patterns of conflicting signal, and compare the performance of various methodological approaches to reflect the heterogeneity across the data. Despite the large extent of reticulate signal and strong conflict between markers, nearly identical topologies are consistently recovered by most of the analyses, although the supermatrix approach failed to reflect the underlying variation in the history of individual loci. However, the supermatrix represents a useful approximation where multiple rare species represented by short sequences can be incorporated easily. The first comprehensive, time-calibrated phylogeny of this group is used to test the hypotheses of a diversification rate increase driven by the dramatic environmental changes in the Neotropics over the past 23 myr, or changes caused by diversity-dependent effects on the rate of diversification. We find that the rate of diversification has increased on the branch leading to the presently most species-rich genus Heliconius, but the change occurred gradually and cannot be unequivocally attributed to a specific environmental driver. Our study provides comprehensive comparison of philosophically distinct species tree reconstruction methods and provides insights into the diversification of an important insect radiation in the most biodiverse region of the planet.
authors: Butterfly Genetics Group, Department of Zoology, University of Cambridge, CB2 3EJ Cambridge, UK; Laboratory of Genetics, Department of Biology, University of Turku, 20014 Turku, Finland; Department of Entomology, The Natural History Museum, London SW7 5BD, UK; Department of Biology, University of York, YO10 5DD Heslington, York, UK; and Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA kk443@cam.ac.uk.
authors: Krzysztof M
authors: KM
authors: Kozak
authors: Butterfly Genetics Group, Department of Zoology, University of Cambridge, CB2 3EJ Cambridge, UK; Laboratory of Genetics, Department of Biology, University of Turku, 20014 Turku, Finland; Department of Entomology, The Natural History Museum, London SW7 5BD, UK; Department of Biology, University of York, YO10 5DD Heslington, York, UK; and Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA.
authors: Niklas
authors: N
authors: Wahlberg
authors: Butterfly Genetics Group, Department of Zoology, University of Cambridge, CB2 3EJ Cambridge, UK; Laboratory of Genetics, Department of Biology, University of Turku, 20014 Turku, Finland; Department of Entomology, The Natural History Museum, London SW7 5BD, UK; Department of Biology, University of York, YO10 5DD Heslington, York, UK; and Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA.
authors: Andrew F E
authors: AF
authors: Neild
authors: Butterfly Genetics Group, Department of Zoology, University of Cambridge, CB2 3EJ Cambridge, UK; Laboratory of Genetics, Department of Biology, University of Turku, 20014 Turku, Finland; Department of Entomology, The Natural History Museum, London SW7 5BD, UK; Department of Biology, University of York, YO10 5DD Heslington, York, UK; and Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA.
authors: Kanchon K
authors: KK
authors: Dasmahapatra
authors: Butterfly Genetics Group, Department of Zoology, University of Cambridge, CB2 3EJ Cambridge, UK; Laboratory of Genetics, Department of Biology, University of Turku, 20014 Turku, Finland; Department of Entomology, The Natural History Museum, London SW7 5BD, UK; Department of Biology, University of York, YO10 5DD Heslington, York, UK; and Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA.
authors: James
authors: J
authors: Mallet
authors: Butterfly Genetics Group, Department of Zoology, University of Cambridge, CB2 3EJ Cambridge, UK; Laboratory of Genetics, Department of Biology, University of Turku, 20014 Turku, Finland; Department of Entomology, The Natural History Museum, London SW7 5BD, UK; Department of Biology, University of York, YO10 5DD Heslington, York, UK; and Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA.
authors: Chris D
authors: CD
authors: Jiggins
mesh_terms: D000818:Animals; D002080:Butterflies / Q000145:classification* / Q000235:genetics*; D005819:Genetic Markers / Q000235:genetics; D049810:Genetic Speciation; D010802:Phylogeny; D013995:Time
chemical_list: D005819:Genetic Markers
keywords: Amazonia; Lepidoptera; Miocene; diversification rate; incongruence; mimicry; multispecies coalescent
references: Evolution. 2011 May;65(5):1489-500
references: 21521198
references: Nucleic Acids Res. 2002 Jul 15;30(14):3059-66
references: 12136088
references: Evolution. 2004 Dec;58(12):2783-7
references: 15696755
references: BMC Evol Biol. 2007 Feb 23;7:28
references: 17319954
references: Am Nat. 2012 Jan;179(1):38-51
references: 22173459
references: J Evol Biol. 2013 Jun;26(6):1203-19
references: 23662978
references: Proc Natl Acad Sci U S A. 2013 Mar 26;110(13):E1179
references: 23460702
references: Mol Phylogenet Evol. 2015 Jan;82 Pt A:156-65
references: 25300455
references: Mol Ecol. 2014 Aug;23(16):4137-52
references: 24962067
references: Insect Mol Biol. 2013 Oct;22(5):532-40
references: 23834845
references: Genome Res. 2013 Aug;23(8):1248-57
references: 23674305
references: Mol Biol Evol. 2002 Dec;19(12):2051-9
references: 12446797
references: Proc Natl Acad Sci U S A. 2010 Apr 20;107(16):7365-70
references: 20368448
references: PLoS Genet. 2012;8(6):e1002752
references: 22737081
references: Oecologia. 1981 Mar;48(2):284-289
references: 28309814
references: Trends Ecol Evol. 2011 Oct;26(10):508-13
references: 21703715
references: Evolution. 1975 Dec;29(4):659-680
references: 28563089
references: Proc Natl Acad Sci U S A. 2004 Jun 29;101(26):9704-9
references: 15210977
references: Syst Biol. 2014 Jul;63(4):610-27
references: 24682412
references: Genome Res. 2013 Nov;23(11):1817-28
references: 24045163
references: Syst Biol. 2011 Mar;60(2):138-49
references: 21248369
references: Evolution. 2009 Jan;63(1):1-19
references: 19146594
references: Syst Biol. 2013 Mar;62(2):298-320
references: 23229025
references: Syst Biol. 2013 Sep;62(5):660-73
references: 23628960
references: PLoS Genet. 2010 Apr 29;6(4):e1000930
references: 20442862
references: Proc Biol Sci. 2000 Nov 22;267(1459):2267-72
references: 11413642
references: Nature. 2012 Mar 21;483(7390):461-4
references: 22437614
references: Naturwissenschaften. 2008 Aug;95(8):681-95
references: 18542902
references: Mol Ecol. 2008 Nov;17(21):4699-712
references: 18828780
references: Mol Biol Evol. 2013 Jan;30(1):197-214
references: 22930702
references: Bioinformatics. 2014 May 1;30(9):1312-3
references: 24451623
references: Am Nat. 2012 Oct;180(4):E75-89
references: 22976017
references: Nature. 2006 Jun 15;441(7095):868-71
references: 16778888
references: Proc Natl Acad Sci U S A. 2012 Sep 11;109(37):14942-7
references: 22930817
references: Proc Biol Sci. 2009 Dec 22;276(1677):4295-302
references: 19793750
references: Syst Biol. 2005 Jun;54(3):483-92
references: 16012113
references: Syst Biol. 2011 Mar;60(2):126-37
references: 21088009
references: J Evol Biol. 2013 Sep;26(9):1959-67
references: 23961921
references: Proc Natl Acad Sci U S A. 2011 Dec 6;108(49):19666-71
references: 22084094
references: Mol Phylogenet Evol. 2010 Oct;57(1):314-26
references: 20637292
references: Syst Biol. 2014 Jan 1;63(1):17-30
references: 23945075
references: Nature. 2001 May 17;411(6835):302-5
references: 11357131
references: Syst Biol. 2014 May;63(3):322-33
references: 23985785
references: Mol Biol Evol. 2012 Aug;29(8):1969-73
references: 22367748
references: Mol Ecol. 2010 Oct;19(19):4283-301
references: 20819158
references: Science. 1972 May 26;176(4037):936-9
references: 17829303
references: BMC Evol Biol. 2008 Jan 24;8:22
references: 18218099
references: Mol Biol Evol. 2002 Dec;19(12):2176-90
references: 12446809
references: Bioinformatics. 2010 Nov 15;26(22):2910-1
references: 20861028
references: Proc Natl Acad Sci U S A. 2007 Apr 3;104(14):5936-41
references: 17392434
references: Syst Biol. 2014 Sep;63(5):772-8
references: 24951558
references: PLoS One. 2008 Jul 23;3(7):e2738
references: 18648512
references: Syst Biol. 2008 Dec;57(6):876-90
references: 19085330
references: Syst Biol. 2008 Feb;57(1):104-15
references: 18288620
references: Proc Biol Sci. 2012 Dec 22;279(1749):4907-13
references: 23075843
references: Syst Biol. 2012 Mar;61(2):289-313
references: 22201158
references: Evolution. 2013 Aug;67(8):2323-34
references: 23888854
references: Evolution. 2011 Oct;65(10):2973-86
references: 21967436
references: Syst Biol. 2012 Mar;61(2):253-71
references: 21978990
references: Syst Biol. 2008 Apr;57(2):294-310
references: 18432550
references: J Evol Biol. 2013 Jun;26(6):1254-60
references: 23662837
references: Evolution. 2013 Aug;67(8):2166-79
references: 23888843
references: Philos Trans R Soc Lond B Biol Sci. 2008 Sep 27;363(1506):3047-54
references: 18579480
references: BMC Evol Biol. 2011 Oct 06;11:291
references: 21978073
references: Bioinformatics. 1998;14(9):817-8
references: 9918953
references: PLoS Genet. 2011 Sep;7(9):e1002274
references: 21931567
references: Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6491-5
references: 8022810
references: Syst Biol. 2005 Jun;54(3):471-82
references: 16012112
references: Syst Biol. 2013 Sep;62(5):689-706
references: 23652346
references: PLoS Biol. 2014 May 06;12(5):e1001854
references: 24802950
references: Proc Biol Sci. 2011 Jun 22;278(1713):1777-85
references: 21106589
references: Syst Biol. 2011 Jan;60(1):3-15
references: 20952756
references: Proc Biol Sci. 2009 Jul 22;276(1667):2557-65
references: 19369265
references: Evolution. 2011 Jul;65(7):1851-61
references: 21729043
references: Bioinformatics. 2013 Nov 15;29(22):2869-76
references: 23990417
references: Cell Rep. 2013 Nov 14;5(3):666-77
references: 24183670
references: PLoS Genet. 2013;9(7):e1003620
references: 23950722
references: Proc Natl Acad Sci U S A. 2012 Jul 31;109(31):12632-7
references: 22802635
references: Bioinformatics. 2003 Aug 12;19(12):1572-4
references: 12912839
references: Proc Biol Sci. 2002 Jan 22;269(1487):137-42
references: 11798428
references: Proc Biol Sci. 2012 Apr 7;279(1732):1300-9
references: 21993508
references: Mol Ecol. 2013 Mar;22(5):1193-213
references: 23279129
references: PLoS Biol. 2008 Dec 2;6(12):2642-9
references: 19055316
references: Proc Biol Sci. 2007 Nov 22;274(1627):2881-9
references: 17785265
references: Mol Phylogenet Evol. 2013 Dec;69(3):1172-85
references: 23800835
references: Evolution. 1989 Mar;43(2):421-431
references: 28568556
references: Syst Biol. 2011 Oct;60(5):719-31
references: 21447483
references: Bioinformatics. 2010 May 15;26(10):1372-3
references: 20228129
references: PLoS One. 2014 Feb 26;9(2):e89543
references: 24586858
references: Bioinformatics. 2006 Nov 1;22(21):2688-90
references: 16928733
references: Evolution. 2011 Feb;65(2):395-407
references: 20964683
references: Mol Phylogenet Evol. 1994 Jun;3(2):159-74
references: 8075834
references: Science. 2010 Nov 12;330(6006):927-31
references: 21071659
references: BMC Bioinformatics. 2008 Jul 28;9:322
references: 18662388
references: Syst Biol. 2006 Feb;55(1):21-30
references: 16507521
references: Genome Res. 2012 Mar;22(3):557-67
references: 22147368
references: Mol Biol Evol. 2012 Jun;29(6):1695-701
references: 22319168
references: PLoS One. 2012;7(5):e36464
references: 22586474
references: Mol Biol Evol. 2010 Mar;27(3):570-80
references: 19906793
references: Syst Biol. 2008 Apr;57(2):231-42
references: 18398768
references: Genome Res. 2009 Jun;19(6):1117-23
references: 19251739
references: Methods Mol Biol. 2012;856:3-28
references: 22399453
references: Evolution. 2009 Oct;63(10):2611-26
references: 19545268
references: Genome Biol Evol. 2013;5(6):1233-45
references: 23737327
references: Evolution. 2002 Jul;56(7):1489-97
references: 12206248
references: PLoS Genet. 2006 May;2(5):e68
references: 16733550
references: Bioinformatics. 2004 Jan 22;20(2):289-90
references: 14734327
references: Mol Biol Evol. 2007 Feb;24(2):412-26
references: 17095535
references: Proc Biol Sci. 2010 Apr 7;277(1684):1065-70
references: 19939841
references: Syst Biol. 2013 May 1;62(3):351-65
references: 23302956
references: Mol Ecol. 2013 Feb;22(3):814-26
references: 22924870
references: BMC Bioinformatics. 2009 Dec 15;10:421
references: 20003500
references: Proc Natl Acad Sci U S A. 1979 Apr;76(4):1924-8
references: 287032
references: Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
references: 15034147
references: J Hered. 2001 Jul-Aug;92(4):371-3
references: 11535656
references: Evolution. 2007 Feb;61(2):346-67
references: 17348945
references: Syst Biol. 2014 Jan 1;63(1):83-95
references: 24021724
references: BMC Evol Biol. 2009 May 13;9:99
references: 19439087
references: J Evol Biol. 2007 Jan;20(1):286-95
references: 17210021
references: Mol Biol Evol. 2012 Sep;29(9):2157-67
references: 22403239