Demographic Divergence History of Pied Flycatcher and Collared Flycatcher Inferred from Whole-Genome Re-sequencing Data

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Profound knowledge of demographic history is a prerequisite for the understanding and inference of processes involved in the evolution of population differentiation and speciation. Together with new coalescent-based methods, the recent availability of genome-wide data enables investigation of differentiation and divergence processes at unprecedented depth. We combined two powerful approaches, full Approximate Bayesian Computation analysis (ABC) and pairwise sequentially Markovian coalescent modeling (PSMC), to reconstruct the demographic history of the split between two avian speciation model species, the pied flycatcher and collared flycatcher. Using whole-genome re-sequencing data from 20 individuals, we investigated 15 demographic models including different levels and patterns of gene flow, and changes in effective population size over time. ABC provided high support for recent (mode 0.3 my, range <0.7 my) species divergence, declines in effective population size of both species since their initial divergence, and unidirectional recent gene flow from pied flycatcher into collared flycatcher. The estimated divergence time and population size changes, supported by PSMC results, suggest that the ancestral species persisted through one of the glacial periods of middle Pleistocene and then split into two large populations that first increased in size before going through severe bottlenecks and expanding into their current ranges. Secondary contact appears to have been established after the last glacial maximum. The severity of the bottlenecks at the last glacial maximum is indicated by the discrepancy between current effective population sizes (20,000–80,000) and census sizes (5–50 million birds) of the two species. The recent divergence time challenges the supposition that avian speciation is a relatively slow process with extended times for intrinsic postzygotic reproductive barriers to evolve. Our study emphasizes the importance of using genome-wide data to unravel tangled demographic histories. Moreover, it constitutes one of the first examples of the inference of divergence history from genome-wide data in non-model species.

Vyšlo v časopise: Demographic Divergence History of Pied Flycatcher and Collared Flycatcher Inferred from Whole-Genome Re-sequencing Data. PLoS Genet 9(11): e32767. doi:10.1371/journal.pgen.1003942
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003942

Souhrn

Zdroje

1. NosilP, FederJL (2011) Genomic divergence during speciation: causes and consequences. Philos Trans R Soc Lond B Biol Sci 367: 332–342.

2. SmadjaCM, ButlinRK (2011) A framework for comparing processes of speciation in the presence of gene flow. Mol Ecol 20: 5123–5140.

3. FederJL, EganSP, NosilP (2012) The genomics of speciation-with-gene-flow. Trends Genet 28: 342–350.

4. ViaS (2012) Divergence hitchhiking and the spread of genomic isolation during ecological speciation-with-gene-flow. Philos Trans R Soc Lond B Biol Sci 367: 451–460.

5. VonlanthenP, BittnerD, Hudson aG, Young Ka, MüllerR, et al. (2012) Eutrophication causes speciation reversal in whitefish adaptive radiations. Nature 482: 357–362.

6. SeehausenO (2006) Losing biodiversity by reverse speciation. Curr Biol 16: R333–4.

7. SeehausenO, van AlphenJ, WitteF (1997) Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277: 1808–1811.

8. TaylorEB, BoughmanJW, GroenenboomM, SniatynskiM, SchluterD, et al. (2006) Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Mol Ecol 15: 343–355.

9. GrantBR, GrantPR (2008) Fission and fusion of Darwin's finches populations. Philos Trans R Soc Lond B Biol Sci 363: 2821–2829.

10. GilmanRT, BehmJE (2011) Hybridization, species collapse, and species reemergence after disturbance to premating mechanisms of reproductive isolation. Evolution 65: 2592–2605.

11. WuC-I, TingC-T (2004) Genes and speciation. Nat Rev Genet 5: 114–122.

12. TurnerTL, HahnMW, NuzhdinSV (2005) Genomic islands of speciation in Anopheles gambiae. PloS Biol 3: e285.

13. NosilP, FunkDJ, Ortiz-BarrientosD (2009) Divergent selection and heterogeneous genomic divergence. Mol Ecol 18: 375–402.

14. ViaS, WestJ (2008) The genetic mosaic suggests a new role for hitchhiking in ecological speciation. Mol Ecol 17: 4334–4345.

15. LiH, DurbinR (2011) Inference of human population history from individual whole-genome sequences. Nature 475: 493–496.

16. GronauI, HubiszMJ, GulkoB, DankoCG, SiepelA (2011) Bayesian inference of ancient human demography from individual genome sequences. Nat Genet 43: 1031–1035.

17. HobolthA, ChristensenOF, MailundT, SchierupMH (2007) Genomic relationships and speciation times of human, chimpanzee, and gorilla inferred from a coalescent hidden Markov model. PLoS Genet 3: e7.

18. WegmannD, LeuenbergerC, ExcoffierL (2009) Efficient approximate Bayesian computation coupled with Markov chain Monte Carlo without likelihood. Genetics 182: 1207–1218.

19. NielsenR, WakeleyJ (2001) Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158: 885–896.

20. WakeleyJ, HeyJ (1997) Estimating ancestral population parameters. Genetics 145: 847–855.

21. Wakeley J (2008) Coalescent theory: an introduction. Greenwood Village, Colorado: Roberts & Company Publishers.

22. BecquetC, PrzeworskiM (2007) A new approach to estimate parameters of speciation models with application to apes. Genome Res 17: 1505–1519.

23. HeyJ, NielsenR (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc Natl Acad Sci U S A 104: 2785–2790.

24. HeyJ, NielsenR (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167: 747–760.

25. ZhuT, YangZ (2012) Maximum likelihood implementation of an isolation-with-migration model with three species for testing speciation with gene flow. Mol Biol Evol 29: 3131–3142.

26. PinhoC, HeyJ (2010) Divergence with gene flow: models and data. Annu Rev Ecol Evol Syst 41: 215–230.

27. CsilléryK, BlumMGB, GaggiottiOE, FrançoisO (2010) Approximate Bayesian Computation (ABC) in practice. Trends Ecol Evol 25: 410–418.

28. BackströmN, SætreG-P, EllegrenH (2013) Inferring the demographic history of European Ficedula flycatcher populations. BMC Evol Biol 13: 2.

29. NadachowskaK, BabikW (2009) Divergence in the face of gene flow: the case of two newts (Amphibia: Salamandridae). Mol Biol Evol 26: 829–841.

30. GeraldesA, BassetP, GibsonB, SmithKL, HarrB, et al. (2008) Inferring the history of speciation in house mice from autosomal, X-linked, Y-linked and mitochondrial genes. Mol Ecol 17: 5349–5363.

31. CarlingMD, LovetteIJ, BrumfieldRT (2010) Historical divergence and gene flow: coalescent analyses of mitochondrial, autosomal and sex-linked loci in Passerina buntings. Evolution 64: 1762–1772.

32. BeaumontM, ZhangW, BaldingDJ (2002) Approximate Bayesian computation in population genetics. Genetics 162: 2025–2035.

33. CornilleA, GiraudT, BellardC, TellierA, Le CamB, et al. (2013) Postglacial recolonization history of the European crabapple (Malus sylvestris Mill.), a wild contributor to the domesticated apple. Mol Ecol 22: 2249–2263.

34. FontaineMC, AusterlitzF, GiraudT, LabbéF, PapuraD, et al. (2013) Genetic signature of a range expansion and leap-frog event after the recent invasion of Europe by the grapevine downy mildew pathogen Plasmopara viticola. Mol Ecol 22: 2771–2786.

35. FagundesNJR, RayN, BeaumontM, NeuenschwanderS, SalzanoFM, et al. (2007) Statistical evaluation of alternative models of human evolution. Proc Natl Acad Sci USA 104: 17614–17619.

36. SousaVC, BeaumontM, FernandesP, CoelhoMM, ChikhiL (2011) Population divergence with or without admixture: selecting models using an ABC approach. Heredity 1–10.

37. RobinsonJD, HallDW, WaresJP (2013) Approximate Bayesian estimation of extinction rate in the Finnish Daphnia magna metapopulation. Mol Ecol 22: 2627–2639.

38. LeuenbergerC, WegmannD (2010) Bayesian computation and model selection without likelihoods. Genetics 184: 243–252.

39. BeaumontM (2010) Approximate Bayesian Computation in evolution and ecology. Annu Rev Ecol Evol Syst 41: 379–406.

40. BertorelleG, BenazzoA, MonaS (2010) ABC as a flexible framework to estimate demography over space and time: some cons, many pros. Mol Ecol 19: 2609–2625.

41. VeeramahKR, WegmannD, WoernerA, MendezFL, WatkinsJC, et al. (2011) An early divergence of KhoeSan ancestors from those of other modern humans is supported by an ABC-based analysis of autosomal re-sequencing data. Mol Biol Evol 29: 617–630.

42. WegmannD, ExcoffierL (2010) Bayesian inference of the demographic history of chimpanzees. Mol Biol Evol 27: 1425–1435.

43. YeungCKL, TsaiP-W, ChesserRT, LinR-C, YaoC-T, et al. (2011) Testing founder effect speciation: divergence population genetics of the spoonbills Platalea regia and Pl. minor (Threskiornithidae, Aves). Mol Biol Evol 28: 473–482.

44. RayN, WegmannD, FagundesNJR, WangS, Ruiz-LinaresA, et al. (2010) A statistical evaluation of models for the initial settlement of the american continent emphasizes the importance of gene flow with Asia. Mol Biol Evol 27: 337–345.

45. LaurentSJY, WerznerA, ExcoffierL, StephanW (2011) Approximate Bayesian analysis of Drosophila melanogaster polymorphism data reveals a recent colonization of Southeast Asia. Mol Biol Evol 28: 2041–2051.

46. TellierA, LaurentS (2011) Inference of seed bank parameters in two wild tomato species using ecological and genetic data. Proc Natl Acad Sci USA 108: 17052–17057.

47. DuchenP, ZivkovicD, HutterS, StephanW, LaurentS (2013) Demographic inference reveals African and European admixture in the North American Drosophila melanogaster population. Genetics 193: 291–301.

48. HoffmanJI, GrantSM, ForcadaJ, PhillipsCD (2011) Bayesian inference of a historical bottleneck in a heavily exploited marine mammal. Mol Ecol 0049: 3989–4008.

49. AscunceMS, YangC-C, OakeyJ, CalcaterraL, WuW-J, et al. (2011) Global invasion history of the fire ant Solenopsis invicta. Science 331: 1066–1068.

50. LanderTA, Oddou-MuratorioS, Prouillet-LeplatH, KleinEK (2011) Reconstruction of a beech population bottleneck using archival demographic information and Bayesian analysis of genetic data. Mol Ecol 20: 5182–5196.

51. HaraY, ImanishiT, SattaY (2012) Reconstructing the demographic history of the human lineage using whole-genome sequences from human and three great apes. Genome Biol Evol 4: 1133–1145.

52. HeyJ (2010) The divergence of chimpanzee species and subspecies as revealed in multipopulation isolation-with-migration analyses. Mol Biol Evol 27: 921–933.

53. BlumMGB, JakobssonM (2011) Deep divergences of human gene trees and models of human origins. Mol Biol Evol 28: 889–898.

54. GutenkunstRN, HernandezRD, WilliamsonSH, BustamanteCD (2009) Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet 5: e1000695.

55. WonY-J, HeyJ (2005) Divergence population genetics of chimpanzees. Mol Biol Evol 22: 297–307.

56. EllegrenH (2014) Genome sequencing and population genomics of non-model organisms. Trends Ecol Evol in press.

57. EllegrenH, SmedsL, BurriR, OlasonPI, BackströmN, et al. (2012) The genomic landscape of species divergence in Ficedula flycatchers. Nature 491: 756–760.

58. GustafssonL, PärtT (1990) Acceleration of senescence in the collared flycatcher Ficedula albicollis by reproductive costs. Nature 347: 279–281.

59. EllegrenH, GustafssonL, SheldonBC (1996) Sex ratio adjustment in relation to paternal attractiveness in a wild bird population. Proc Natl Acad Sci USA 93: 11723–11728.

60. Qvarnströma, PärtT, SheldonBC (2000) Adaptive plasticity in mate preference linked to differences in reproductive effort. Nature 405: 344–347.

61. MeriläJ, KruukLE, SheldonBC (2001) Cryptic evolution in a wild bird population. Nature 412: 76–79.

62. QvarnströmA, RiceAM, EllegrenH (2010) Speciation in Ficedula flycatchers. Philos Trans R Soc Lond B Biol Sci 365: 1841–1852.

63. SaetreG-P, SaetherSA (2010) Ecology and genetics of speciation in Ficedula flycatchers. Mol Ecol 19: 1091–1106.

64. SaetreGP, BorgeT, LindellJ, MoumT, PrimmerCR, et al. (2001) Speciation, introgressive hybridization and nonlinear rate of molecular evolution in flycatchers. Mol Ecol 10: 737–749.

65. BorgeT, LindroosK, NádvorníkP, SyvänenA-C, SaetreG-P (2005) Amount of introgression in flycatcher hybrid zones reflects regional differences in pre and post-zygotic barriers to gene exchange. J Evol Biol 18: 1416–1424.

66. BackströmN, KaraiskouN, LederEH, GustafssonL, PrimmerCR, et al. (2008) A gene-based genetic linkage map of the collared flycatcher (Ficedula albicollis) reveals extensive synteny and gene-order conservation during 100 million years of avian evolution. Genetics 179: 1479–1495.

67. BackströmN, BrandströmM, GustafssonL, QvarnströmA, ChengH, et al. (2006) Genetic mapping in a natural population of collared flycatchers (Ficedula albicollis): conserved synteny but gene order rearrangements on the avian Z chromosome. Genetics 174: 377–386.

68. BackströmN, QvarnströmA, GustafssonL, EllegrenH (2006) Levels of linkage disequilibrium in a wild bird population. Biol Lett 2: 435–438.

69. BackströmN, PalkopoulouE, QvarnströmA, EllegrenH (2010) No evidence for Z-chromosome rearrangements between the pied flycatcher and the collared flycatcher as judged by gene-based comparative genetic maps. Mol Ecol 19: 3394–3405.

70. BackströmN, LindellJ, ZhangY, PalkopoulouE, QvarnströmA, et al. (2010) A high-density scan of the Z chromosome in Ficedula flycatchers reveals candidate loci for diversifying selection. Evolution 64: 3461–3475.

71. TegelstromH, GelterH (1990) Haldane's rule and sex biassed gene flow between two hybridizing flycatcher species (Ficedula albicollis and F . hypoleuca, Aves: Muscicapidae). Evolution 44: 2012–2021.

72. WileyC, QvarnströmA, AnderssonG, BorgeT, SaetreG-P (2009) Postzygotic isolation over multiple generations of hybrid descendents in a natural hybrid zone: how well do single-generation estimates reflect reproductive isolation? Evolution 63: 1731–1739.

73. VeenT, BorgeT, GriffithSC, SaetreGP, BuresS, et al. (2001) Hybridization and adaptive mate choice in flycatchers. Nature 411: 45–50.

74. SvedinN, WileyC, VeenT, GustafssonL, QvarnströmA (2008) Natural and sexual selection against hybrid flycatchers. Philos Trans R Soc Lond B Biol Sci 275: 735–744.

75. AlataloR, GustafssonL, LundbergA (1982) Hybridization and breeding success of collared and pied flycatchers on the island of Gotland. Auk 99: 285–291.

76. SætreG, KrálK, BuresS, ImsR (1999) Dynamics of a clinal hybrid zone and a comparison with island hybrid zones of flycatchers (Ficedula hypoleuca and F. albicollis). J Zool 247: 53–64.

77. HognerS, Sæther Sa, BorgeT, BruvikT, JohnsenA, et al. (2012) Increased divergence but reduced variation on the Z chromosome relative to autosomes in Ficedula flycatchers: differential introgression or the faster-Z effect? Ecol Evol 2: 379–396.

78. SaetreG-P, BorgeT, LindroosK, HaavieJ, SheldonBC, et al. (2003) Sex chromosome evolution and speciation in Ficedula flycatchers. Philos Trans R Soc Lond B Biol Sci 270: 53–59.

79. NeuenschwanderS, LargiadèrCR, RayN, CurratM, VonlanthenP, et al. (2008) Colonization history of the Swiss Rhine basin by the bullhead (Cottus gobio): inference under a Bayesian spatially explicit framework. Mol Ecol 17: 757–772.

80. CurratM, RuediM, PetitRJ, ExcoffierL (2008) The hidden side of invasions: massive introgression by local genes. Evolution 62: 1908–1920.

81. PetitRJ, ExcoffierL (2009) Gene flow and species delimitation. Trends Ecol Evol 24: 386–393.

82. Lundberg A, Alatalo R (1992) The pied flycatcher. London, UK: Poyser.

83. PriceTD, BouvierMM (2002) The evolution of F1 postzygotic incompatibilities in birds. Evolution 56: 2083–2089.

84. EdwardsSV, BeerliP (2000) Perspective: gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies. Evolution 54: 1839–1854.

85. ArbogastBS, EdwardsSV, WakeleyJ, BeerliP, SlowinskiJB (2002) Estimating divergence times from molecular data on phylogenetic and population genetic timescales. Annu Rev Ecol Evol Syst 33: 707–740.

86. Lijtmaer Da, MahlerB, TubaroPL (2003) Hybridization and postzygotic isolation patterns in pigeons and doves. Evolution 57: 1411–1418.

87. StorchováR, ReifJ, NachmanMW (2010) Female heterogamety and speciation: reduced introgression of the Z chromosome between two species of nightingales. Evolution 64: 456–471.

88. LiJ-W, YeungCKL, TsaiP-W, LinR-C, YehC-F, et al. (2010) Rejecting strictly allopatric speciation on a continental island: prolonged postdivergence gene flow between Taiwan (Leucodioptron taewanus, Passeriformes Timaliidae) and Chinese (L. canorum canorum) hwameis. Mol Ecol 19: 494–507.

89. LiS, JakobssonM (2012) Estimating demographic parameters from large-scale population genomic data using Approximate Bayesian Computation. BMC Genet 13: 22.

90. NosilP, HarmonLJ, SeehausenO (2009) Ecological explanations for (incomplete) speciation. Trends Ecol Evol 24: 145–156.

91. BackströmN, ForstmeierW, SchielzethH, MelleniusH, NamK, et al. (2010) The recombination landscape of the zebra finch Taeniopygia guttata genome. Genome Res 20: 485–495.

92. WegmannD, LeuenbergerC, NeuenschwanderS, ExcoffierL (2010) ABCtoolbox: a versatile toolkit for approximate Bayesian computations. BMC Bioinformatics 11: 116.

93. PavlidisP, LaurentS, StephanW (2010) msABC: a modification of Hudson's ms to facilitate multi-locus ABC analysis. Mol Ecol Resour 10: 723–727.

94. HudsonR (2002) Generating samples under a Wright–Fisher neutral model of genetic variation. Bioinformatics 18: 337–338.

95. EllegrenH (2007) Molecular evolutionary genomics of birds. Cytogenet Genome Res 117: 120–130.

96. BoulesteixA-L, StrimmerK (2007) Partial least squares: a versatile tool for the analysis of high-dimensional genomic data. Brief Bioinformatics 8: 32–44.

97. MevikB, WehrensR (2007) The pls package: Principal component and partial least squares regression in R. J Stat Softw 18.

98. FagundesNJR, RayN, BeaumontM, NeuenschwanderS, SalzanoFM, et al. (2007) Statistical evaluation of alternative models of human evolution. Proc Natl Acad Sci USA 104: 17614–17619.

99. PritchardJK (2011) Whole-genome sequencing data offer insights into human demography. Nat Genet 43: 923–925.