Hybridization Reveals the Evolving Genomic Architecture of Speciation

Abstract

The rate at which genomes diverge during speciation is unknown, as are the physical dynamics of the process. Here, we compare full genome sequences of 32 butterflies, representing five species from a hybridizing Heliconius butterfly community, to examine genome-wide patterns of introgression and infer how divergence evolves during the speciation process. Our analyses reveal that initial divergence is restricted to a small fraction of the genome, largely clustered around known wing-patterning genes. Over time, divergence evolves rapidly, due primarily to the origin of new divergent regions. Furthermore, divergent genomic regions display signatures of both selection and adaptive introgression, demonstrating the link between microevolutionary processes acting within species and the origin of species across macroevolutionary timescales. Our results provide a uniquely comprehensive portrait of the evolving species boundary due to the role that hybridization plays in reducing the background accumulation of divergence at neutral sites.

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References 86

1. 1.

   Baxter SW, Nadeau NJ, Maroja LS, Wilkinson P, Counterman BA, Dawson A, Beltran M, Perez-Espona S, Chamberlain N, Ferguson L, et al. Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene clade. PLoS Genet. 2010;6:e1000794.

   Not in our library10.1371/journal.pgen.1000794

2. 2.

   Beltrán M, Jiggins CD, Bull V, Linares M, Mallet J, McMillan WO, Bermingham E. Phylogenetic discordance at the species boundary: comparative gene genealogies among rapidly radiating Heliconius butterflies. Mol Biol Evol. 2002;19:2176-2190.

   Not in our library10.1093/oxfordjournals.molbev.a004042

3. 3.

   Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B. 1995;57:289-300.

   Not in our library

4. 4.

   Benson WW. Resource partitioning in passion vine butterflies. Evolution. 1978;32:493-518.

   Not in our library10.1111/j.1558-5646.1978.tb04593.x

5. 5.

   Brown KS. The biology of Heliconius and related genera. Annu Rev Entomol. 1981;26:427-456.

   Not in our library

6. 6.

   Browning SR, Browning BL. Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet. 2007;81:1084-1097.

   Not in our library10.1086/521987

7. 7.

   Bull V, Beltrán M, Jiggins CD, McMillan WO, Bermingham E, Mallet J. Polyphyly and gene flow between non-sibling Heliconius species. BMC Biol. 2006;4:11.

   Not in our library10.1186/1741-7007-4-11

8. 8.

   Chamberlain NL, Hill RI, Kapan DD, Gilbert LE, Kronforst MR. Polymorphic butterfly reveals the missing link in ecological speciation. Science. 2009;326:847-850.

   Not in our library10.1126/science.1179141

9. 9.

   Chamberlain NL, Hill RI, Baxter SW, Jiggins CD, Kronforst MR. Comparative population genetics of a mimicry locus among hybridizing Heliconius butterfly species. Heredity (Edinb). 2011;107:200-204.

   Not in our library10.1038/hdy.2011.3

10. 10.

    Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, et al. The variant call format and VCFtools. Bioinformatics. 2011;27:2156-2158.

    Not in our library10.1093/bioinformatics/btr330

11. 11.

    Dasmahapatra KK, Silva-Vásquez A, Chung JW, Mallet J. Genetic analysis of a wild-caught hybrid between non-sister Heliconius butterfly species. Biol Lett. 2007;3:660-663.

    Not in our library10.1098/rsbl.2007.0401

12. 12.

    DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet. 2011;43:491-498.

    Not in our library10.1038/ng.806

13. 13.

    Durand EY, Patterson N, Reich D, Slatkin M. Testing for ancient admixture between closely related populations. Mol Biol Evol. 2011;28:2239-2252.

    Not in our library10.1093/molbev/msr048

14. 14.

    Ellegren H, Smeds L, Burri R, Olason PI, Backström N, Kawakami T, Künstner A, Mäkinen H, Nadachowska-Brzyska K, Qvarnström A, et al. The genomic landscape of species divergence in Ficedula flycatchers. Nature. 2012;491:756-760.

    Not in our library10.1038/nature11584

15. 15.

    Estrada C, Jiggins CD. Patterns of pollen feeding and habitat preference among Heliconius species. Ecol Entomol. 2002;27:448-456.

    Not in our library

16. 16.

    Excoffier L, Lischer HEL. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010;10:564-567.

    Not in our library10.1111/j.1755-0998.2010.02847.x

17. 17.

    Excoffier L, Smouse PE, Quattro JM. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics. 1992;131:479-491.

    Not in our library10.1093/genetics/131.2.479

18. 18.

    Feder JL, Nosil P. The efficacy of divergence hitchhiking in generating genomic islands during ecological speciation. Evolution. 2010;64:1729-1747.

    Not in our library10.1111/j.1558-5646.2010.00943.x

19. 19.

    Feder JL, Egan SP, Nosil P. The genomics of speciation-with-gene-flow. Trends Genet. 2012a;28:342-350.

    Not in our library10.1016/j.tig.2012.03.009

20. 20.

    Feder JL, Gejji R, Yeaman S, Nosil P. Establishment of new mutations under divergence and genome hitchhiking. Philos Trans R Soc Lond B Biol Sci. 2012b;367:461-474.

    Not in our library10.1098/rstb.2011.0256

21. 21.

    Flaxman SM, Feder JL, Nosil P. Genetic hitchhiking and the dynamic buildup of genomic divergence during speciation with gene flow. Evolution. 2013;67:2577-2591.

    Not in our library10.1111/evo.12055

22. 22.

    Gilbert LE, Boggs CL, Watt WB, Ehrlich PR. Adaptive novelty through introgression in Heliconius wing patterns: evidence for shared genetic “tool box” from synthetic hybrid zones and a theory of diversification. Ecology and Evolution Taking Flight: Butterflies as Model Systems. 2003;281-318.

    Not in our library

23. 23.
    Patterns of intron sequence evolution in Drosophila are dependent upon length and GC content · 2005

    No notice
24. 24.

    Halligan DL, Keightley PD. Ubiquitous selective constraints in the Drosophila genome revealed by a genome-wide interspecies comparison. Genome Res. 2006;16:875-884.

    Not in our library10.1101/gr.5022906

25. 25.

    Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature. 2012;487:94-98.

    Not in our library10.1038/nature11041

26. 26.

    Hendry AP, Bolnick DI, Berner D, Peichel CL. Along the speciation continuum in sticklebacks. J Fish Biol. 2009;75:2000-2036.

    Not in our library10.1111/j.1095-8649.2009.02419.x

27. 27.

    Hey J. Isolation with migration models for more than two populations. Mol Biol Evol. 2010;27:905-920.

    Not in our library10.1093/molbev/msp296

28. 28.

    Hudson RR. Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics. 2002;18:337-338.

    Not in our library10.1093/bioinformatics/18.2.337

29. 29.

    Jiggins CD, Naisbit RE, Coe RL, Mallet J. Reproductive isolation caused by colour pattern mimicry. Nature. 2001;411:302-305.

    Not in our library10.1038/35077075

30. 30.

    Jiggins CD, Salazar C, Linares M, Mavarez J. Review. Hybrid trait speciation and Heliconius butterflies. Philos Trans R Soc Lond B Biol Sci. 2008;363:3047-3054.

    Not in our library10.1098/rstb.2008.0065

31. 31.

    Joron M, Jiggins CD, Papanicolaou A, McMillan WO. Heliconius wing patterns: an evo-devo model for understanding phenotypic diversity. Heredity (Edinb). 2006a;97:157-167.

    Not in our library10.1038/sj.hdy.6800873

32. 32.
    A Conserved Supergene Locus Controls Colour Pattern Diversity in Heliconius Butterflies · 2006

    No notice
33. 33.

    Kapan DD. Three-butterfly system provides a field test of müllerian mimicry. Nature. 2001;409:338-340.

    Not in our library10.1038/35053066

34. 34.

    Kitano J, Ross JA, Mori S, Kume M, Jones FC, Chan YF, Absher DM, Grimwood J, Schmutz J, Myers RM, et al. A role for a neo-sex chromosome in stickleback speciation. Nature. 2009;461:1079-1083.

    Not in our library10.1038/nature08441

35. 35.
    Gene flow persists millions of years after speciation in <it>Heliconius </it>butterflies · 2008

    Not checked
36. 36.

    Kronforst MR, Gilbert LE. The population genetics of mimetic diversity in Heliconius butterflies. Proc Biol Sci. 2008;275:493-500.

    Not in our library10.1098/rspb.2007.1378

37. 37.

    Kronforst MR, Kapan DD, Gilbert LE. Parallel genetic architecture of parallel adaptive radiations in mimetic Heliconius butterflies. Genetics. 2006a;174:535-539.

    Not in our library10.1534/genetics.106.059527

38. 38.

    Kronforst MR, Young LG, Blume LM, Gilbert LE. Multilocus analyses of admixture and introgression among hybridizing Heliconius butterflies. Evolution. 2006b;60:1254-1268.

    Not in our library

39. 39.

    Kronforst MR, Young LG, Kapan DD, McNeely C, O’Neill RJ, Gilbert LE. Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless. Proc Natl Acad Sci USA. 2006c;103:6575-6580.

    Not in our library10.1073/pnas.0509685103

40. 40.

    Kronforst MR, Salazar C, Linares M, Gilbert LE. No genomic mosaicism in a putative hybrid butterfly species. Proc Biol Sci. 2007a;274:1255-1264.

    Not in our library10.1098/rspb.2006.0207

Cited by papers we hold 6

• Phylogenomic approaches to detecting and characterizing introgression · 2021
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• Recombination rate variation shapes barriers to introgression across butterfly genomes · 2019
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• Widespread selection and gene flow shape the genomic landscape during a radiation of monkeyflowers · 2019
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• Evolution of heterogeneous genome differentiation across multiple contact zones in a crow species complex · 2016
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• Multilocus Species Trees Show the Recent Adaptive Radiation of the Mimetic Heliconius Butterflies · 2015
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• Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci · 2014
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