Genomic Hotspots for Adaptation: The Population Genetics of Müllerian Mimicry in the Clade

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Wing patterning in Heliconius butterflies is a longstanding example of both Müllerian mimicry and phenotypic radiation under strong natural selection. The loci controlling such patterns are “hotspots” for adaptive evolution with great allelic diversity across different species in the genus. We characterise nucleotide variation, genotype-by-phenotype associations, linkage disequilibrium, and candidate gene expression at two loci and across multiple hybrid zones in Heliconius melpomene and relatives. Alleles at HmB control the presence or absence of the red forewing band, while alleles at HmYb control the yellow hindwing bar. Across HmYb two regions, separated by ∼100 kb, show significant genotype-by-phenotype associations that are replicated across independent hybrid zones. In contrast, at HmB a single peak of association indicates the likely position of functional sites at three genes, encoding a kinesin, a G-protein coupled receptor, and an mRNA splicing factor. At both HmYb and HmB there is evidence for enhanced linkage disequilibrium (LD) between associated sites separated by up to 14 kb, suggesting that multiple sites are under selection. However, there was no evidence for reduced variation or deviations from neutrality that might indicate a recent selective sweep, consistent with these alleles being relatively old. Of the three genes showing an association with the HmB locus, the kinesin shows differences in wing disc expression between races that are replicated in the co-mimic, Heliconius erato, providing striking evidence for parallel changes in gene expression between Müllerian co-mimics. Wing patterning loci in Heliconius melpomene therefore show a haplotype structure maintained by selection, but no evidence for a recent selective sweep. The complex genetic pattern contrasts with the simple genetic basis of many adaptive traits studied previously, but may provide a better model for most adaptation in natural populations that has arisen over millions rather than tens of years.

Vyšlo v časopise: Genomic Hotspots for Adaptation: The Population Genetics of Müllerian Mimicry in the Clade. PLoS Genet 6(2): e32767. doi:10.1371/journal.pgen.1000794
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000794

Souhrn

Zdroje

1. OnumaY

TakahashiS

AsashimaM

KurataS

GehringWJ

2002 Conservation of Pax 6 function and upstream activation by Notch signaling in eye development of frogs and flies. Proceedings of the National Academy of Sciences of the United States of America 99 2020 2025 doi:10.1073/pnas.022626999

2. MundyNI

2005 A window on the genetics of evolution: MC1R and plumage colouration in birds. Proceedings of the Royal Society B: Biological Sciences 272 1633 1640 doi:10.1098/rspb.2005.3107

3. HoekstraHE

HirschmannRJ

BundeyRA

InselPA

CrosslandJP

2006 A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313 101 4 doi:10.1126/science.1126121

4. NachmanMW

HoekstraHE

D'AgostinoSL

2003 The genetic basis of adaptive melanism in pocket mice. Proc Natl Acad Sci U S A 100 5268 5273 doi:10.1073/pnas.0431157100

5. ColosimoPF

HosemannKE

BalabhadraS

VillarrealG

DicksonM

2005 Widespread Parallel Evolution in Sticklebacks by Repeated Fixation of Ectodysplasin Alleles. Science 307 1928 1933 doi:10.1126/science.1107239

6. ShapiroMD

MarksME

PeichelCL

BlackmanBK

NerengKS

2004 Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428 717 723 doi:10.1038/nature02415

7. SternDL

OrgogozoV

2008 The loci of evolution: How predictable is genetic evolution? Evolution 62 2155 2177 doi:10.1111/j.1558-5646.2008.00450.x

8. JoronM

JigginsCD

PapanicolaouA

McMillanWO

2006 Heliconius wing patterns: an evo-devo model for understanding phenotypic diversity. Heredity 97 157 67 doi:10.1038/sj.hdy.6800873

9. LanghamGM

2004 Specialized avian predators repeatedly attack novel color morphs of Heliconius butterflies. Evolution 58 2783 7 doi:15696755

10. PapaR

MartinA

ReedRD

2008 Genomic hotspots of adaptation in butterfly wing pattern evolution. Curr Opin Genet Dev 18 559 64 doi:10.1016/j.gde.2008.11.007

11. JoronM

PapaR

BeltránM

ChamberlainN

MavárezJ

2006 A conserved supergene locus controls colour pattern diversity in Heliconius butterflies. PLoS Biol 4 e303 doi:10.1371/journal.pbio.0040303

12. CountermanBA

Araujo-PerezF

HinesHM

BaxterSW

MorrisonC

2010 Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in Heliconius erato. PLoS Genet 6 e796 doi:10.1371/journal.pgen.1000796

13. HirschhornJN

DalyMJ

2005 Genome-wide association studies for common diseases and complex traits. Nat Rev Genet 6 95 108 doi:nrg1521

14. SavolainenV

AnstettM

LexerC

HuttonI

ClarksonJJ

2006 Sympatric speciation in palms on an oceanic island. Nature 441 210 3 doi:nature04566

15. SchlöttererC

2003 Hitchhiking mapping–functional genomics from the population genetics perspective. Trends Genet 19 32 8 doi:12493246

16. WildingCS

ButlinRK

GrahameJ

2001 Differential gene exchange between parapatric morphs of Littorina saxatilis detected using AFLP markers. Journal of Evolutionary Biology 14 611 619 doi:10.1046/j.1420-9101.2001.00304.x

17. BartonNH

2000 Genetic hitchhiking. Philos Trans R Soc Lond B Biol Sci 355 1553 62 doi:PMC1692896

18. DabornPJ

YenJL

BogwitzMR

Le GoffG

FeilE

2002 A Single P450 Allele Associated with Insecticide Resistance in Drosophila. Science 297 2253 2256 doi:10.1126/science.1074170

19. SchlenkeTA

BegunDJ

2004 Strong selective sweep associated with a transposon insertion in Drosophila simulans. Proceedings of the National Academy of Sciences of the United States of America 101 1626 1631 doi:10.1073/pnas.0303793101

20. MalletJ

BartonNH

1989 Strong natural selection in a warning-color hybrid zone. Evolution 43 421 431

21. MalletJ

1989 The Genetics of Warning Colour in Peruvian Hybrid Zones of Heliconius erato and H. melpomene. Proceedings of the Royal Society of London. Series B, Biological Sciences (1934–1990) 236 163 185

22. BartonNH

GaleKS

1993 Genetic analysis of hybrid zones.

HarrisonRG,

Hybrid Zones and the Evolutionary Process New York Oxford University Press 13 45

23. HarrisonRG

BogdanowiczSM

1997 Patterns of Variation and Linkage Disequilibrium in a Field Cricket Hybrid Zone. Evolution 51 493 505 doi:10.2307/2411122

24. HowardDJ

WaringGL

1991 Topographic diversity, zone width, and the strength of reproductive isolation in a zone of overlap and hybridization. Evolution (USA) 45 1120 1135

25. RaufasteN

OrthA

BelkhirK

SenetD

SmadjaC

2005 Inferences of selection and migration in the Danish house mouse hybrid zone. Biological Journal of the Linnean Society 84 593 616 doi:10.1111/j.1095-8312.2005.00457.x

26. JigginsC

McMillanW

KingP

MalletJ

1997 The maintenance of species differences across a Heliconius hybrid zone. Heredity 79 495 505

27. MalletJ

McMillanWO

JigginsCD

1998 Mimicry and warning colour at the boundary between races and species.

HowardDJ

BerlocherSH

BerlocherDJHSH,

Endless Forms New York Oxford University Press 470 p

28. MalletJ

1986 Dispersal and gene flow in a butterfly with home range behavior: Heliconius erato (Lepidoptera: Nymphalidae). Oecologia 68 210 217 doi:10.1007/BF00384789

29. MalletJ

BartonN

GerardoLM

JoseSC

ManuelMM

1990 Estimates of Selection and Gene Flow from Measures of Cline Width and Linkage Disequilibrium in Heliconius Hybrid Zones. Genetics 124 921

30. KronforstMR

GilbertLE

2008 The population genetics of mimetic diversity in Heliconius butterflies. Proc Biol Sci 275 493 500 doi:10.1098/rspb.2007.1378

31. BaxterSW

PapaR

ChamberlainN

HumphraySJ

JoronM

2008 Convergent evolution in the genetic basis of Müllerian mimicry in heliconius butterflies. Genetics 180 1567 77 doi:10.1534/genetics.107.082982

32. CantarelBL

KorfI

RobbSMC

ParraG

RossE

2008 MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res 18 188 96 doi:10.1101/gr.6743907

33. FergusonL

Siu FaiLee

ChamberlainN

NadeaN

JoronM

2009 Characterization of a hotspot for mimicry: Assembly of a butterfly wing transcriptome to genomic sequence at the HmYb/Sb locus. Molecular Ecology In press xx xx

34. KronforstMR

YoungLG

BlumeLM

GilbertLE

2006 Multilocus analyses of admixture and introgression among hybridizing Heliconius butterflies. Evolution 60 1254 1268

35. JigginsCD

NaisbitRE

CoeRL

MalletJ

2001 Reproductive isolation caused by colour pattern mimicry. Nature 411 302 5 doi:10.1038/35077075

36. ViaS

WestJ

2008 The genetic mosaic suggests a new role for hitchhiking in ecological speciation. Mol Ecol 17 4334 4345 doi:10.1111/j.1365-294X.2008.03921.x

37. WoodHM

GrahameJW

HumphrayS

RogersJ

ButlinRK

2008 Sequence differentiation in regions identified by a genome scan for local adaptation. Mol Ecol 17 3123 3135 doi:10.1111/j.1365-294X.2008.03755.x

38. FlanaganNS

ToblerA

DavisonA

PybusOG

KapanDD

2004 Historical demography of Müllerian mimicry in the neotropical Heliconius butterflies. Proc Natl Acad Sci U S A 101 9704 9709 doi:10.1073/pnas.0306243101

39. BarretR

SchluterD

n.d. Adaptation from standing genetic variation. Trends in Ecology and Evolution 23 38 44

40. MalletJ

2010 Shift happens! Evolution of warning colour and mimetic diversity in tropical butterflies. Ecological Entomology 35 xxx xxx

41. MalletJ

SingerMC

1987 Individual selection, kin selection, and the shifting balance in the evolution of warning colours: the evidence from butterflies. Biological Journal of the Linnean Society 32 337 350 doi:10.1111/j.1095-8312.1987.tb00435.x

42. BrownKS

SheppardPM

TurnerJRG

1974 Quaternary Refugia in Tropical America: Evidence from Race Formation in Heliconius Butterflies. Proceedings of the Royal Society of London. Series B, Biological Sciences 187 369 378 doi:10.2307/76410

43. KeysDN

LewisDL

SelegueJE

PearsonBJ

GoodrichLV

1999 Recruitment of a hedgehog Regulatory Circuit in Butterfly Eyespot Evolution. Science 283 532 534 doi:10.1126/science.283.5401.532

44. BrunettiCR

SelegueJE

MonteiroA

FrenchV

BrakefieldPM

2001 The generation and diversification of butterfly eyespot color patterns. Curr Biol 11 1578 85 doi:11676917

45. CarrollS

GatesJ

KeysD

PaddockS

PanganibanG

1994 Pattern formation and eyespot determination in butterfly wings. Science 265 109 114 doi:10.1126/science.7912449

46. GompelN

Prud'hommeB

WittkoppPJ

KassnerVA

CarrollSB

2005 Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433 481 7 doi:10.1038/nature03235

47. JeongS

RebeizM

AndolfattoP

WernerT

TrueJ

2008 The evolution of gene regulation underlies a morphological difference between two Drosophila sister species. Cell 132 783 93 doi:10.1016/j.cell.2008.01.014

48. BeldadeP

SaenkoSV

PulN

LongAD

2009 A gene-based linkage map for Bicyclus anynana butterflies allows for a comprehensive analysis of synteny with the lepidopteran reference genome. PLoS Genet 5 e1000366 doi:10.1371/journal.pgen.1000366

49. GoldsteinLS

PhilpAV

1999 The road less traveled: emerging principles of kinesin motor utilization. Annu Rev Cell Dev Biol 15 141 83 doi:10.1146/annurev.cellbio.15.1.141

50. TekotteH

DavisI

2002 Intracellular mRNA localization: motors move messages. Trends Genet 18 636 42

51. AspengrenS

HedbergD

SköldHN

WallinM

2009 New insights into melanosome transport in vertebrate pigment cells. Int Rev Cell Mol Biol 272 245 302 doi:10.1016/S1937-6448(08)01606-7

52. BoyleRT

McNamaraJC

2008 A Spring-Matrix Model for Pigment Translocation in the Red Ovarian Chromatophores of the Freshwater Shrimp Macrobrachium olfersi (Crustacea, Decapoda). Biol Bull 214 111 121

53. KronforstMR

YoungLG

KapanDD

McNeelyC

O'NeillRJ

2006 Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless. Proc Natl Acad Sci U S A 103 6575 80 doi:10.1073/pnas.0509685103

54. GilbertLE

2003 Adaptive novelty through introgression in Heliconius wing patterns: Evidence for shared genetic ‘tool box’ from synthetic hybrid zones and a theory of diversification.

BoggsCL

WattWB

EhrlichPR,

Ecology and Evolution Taking Flight: Butterflies as Model Systems Chicago Univ. of Chicago Press

55. OttoTD

GomesLHF

Alves-FerreiraM

de MirandaAB

DegraveWM

2008 ReRep: Computational detection of repetitive sequences in genome survey sequences(GSS). BMC Bioinformatics 9 366

56. KorfI

2004 Gene finding in novel genomes. BMC Bioinformatics 5 59 doi:10.1186/1471-2105-5-59

57. LewisSE

SearleSMJ

HarrisN

GibsonM

IyerV

2002 Apollo: a sequence annotation editor. Genome Biol 3 1 14

58. RozasJ

Sánchez-DelBarrioJC

MesseguerX

RozasR

2003 DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19 2496 7 doi:14668244

59. NeiM

1987 Molecular Evolutionary Genetics. 1st ed Columbia University Press. 512

60. TajimaF

1989 Statistical Method for Testing the Neutral Mutation Hypothesis by DNA Polymorphism. Genetics 123 585 595

61. HudsonRR

SlatkinM

MaddisonWP

1992 Estimation of Levels of Gene Flow From DNA Sequence Data. Genetics 132 583 589

62. WeirBS

1996 Genetic Data Analysis 2: Methods for Discrete Population Genetic Data. 2nd ed Sinauer Associates

63. ArmitageP

1955 Tests for Linear Trends in Proportions and Frequencies. Biometrics 11 375 386 doi:10.2307/3001775

64. ShinJH

BlayS

McNeneyB

GrahamJ

2006 LDheatmap: An R Function for Graphical Display of Pairwise Linkage Disequilibria between Single Nucleotide Polymorphisms. Journal of Statistical Software 16 Code Snippet 3

65. FergusonLC

JigginsCD

2009 Shared and divergent expression domains on mimetic Heliconius wings. Evolution & Development 11 498 512 doi:10.1111/j.1525-142X.2009.00358.x