The Genomic Architecture of Population Divergence between Subspecies of the European Rabbit

English version České info

A number of laboratory studies of speciation have uncovered individual genes that confer lower fitness when in a divergent genetic background. It is, however, unclear whether these genes were ever relevant to restricting gene flow in nature, or whether they are indirect consequences of functional divergence between species that in most cases can no longer hybridize in natural conditions. Analysis of introgression across the genome of divergent populations provides an alternative approach to determine the genetic basis of reproductive isolation. Using two subspecies of rabbits as a model for the early stages of speciation, we provide a genome-wide map of genetic differentiation. Our study revealed important aspects of the genetic architecture of differentiation in the early stages of divergence and allowed the identification of genomic regions that resist introgression and are likely to confer reproductive barriers in natural conditions. The gene content of these regions, which in several cases reached gene-level resolution, suggests an important role for epigenetic and transcription regulation in the maintenance of reproductive barriers. Some of the genes identified here in a natural system are similar in function to the hybrid male sterility genes identified in laboratory studies of speciation.

Vyšlo v časopise: The Genomic Architecture of Population Divergence between Subspecies of the European Rabbit. PLoS Genet 10(8): e32767. doi:10.1371/journal.pgen.1003519
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003519

Souhrn

Zdroje

1. PresgravesDC (2010) The molecular evolutionary basis of species formation. Nat Rev Genet 11 : 175–180.

2. Coyne JA, Orr HA (2004) Speciation. Sunderland: Sinauer Associates, Inc. 545 p.

3. BarbashDA, SiinoDF, TaroneAM, RooteJ (2003) A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc Natl Acad Sci U S A 100 : 5302–5307.

4. BayesJJ, MalikHS (2009) Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species. Science 326 : 1538–41.

5. MiholaO, TrachtulecZ, VlcekC, SchimentiJC, ForejtJ (2009) A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science 323 : 373–375.

6. PhadnisN, OrrHA (2009) A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 323 : 376–9.

7. MalletJ (2006) What does Drosophila genetics tell us about speciation? Trends Ecol Evol 21 : 386–393.

8. RiesebergLH, BairdSJ, GardnerKA (2000) Hybridization, introgression, and linkage evolution. Plant Mol Biol 42 : 205–224.

9. HarrisonRG (1990) Hybrid Zones: windows on evolutionary process. Oxford Surveys in Evolutionary Biology 7 : 69–128.

10. PayseurBA (2010) Using differential introgression in hybrid zones to identify genomic regions involved in speciation. Mol Ecol Resour 10 : 806–820.

11. PinhoC, HeyJ (2010) Divergence with Gene Flow: Models and Data. Annu Rev Ecol Evol S 41 : 215–230.

12. Endler JA (1977) Geographic variation, speciation, and clines. Princeton: Princeton Univ. Press. 262 p.

13. BartonNH, BengtssonBO (1986) The barrier to genetic exchange between hybridizing populations. Heredity 57 : 357–376.

14. WuC-I (2001) The genic view of the process of speciation. J Evol Biol 14 : 851–865.

15. KulathinalRJ, StevisonLS, NoorMA (2009) The genomics of speciation in Drosophila: diversity, divergence, and introgression estimated using low-coverage genome sequencing. PLoS Genet 5: e1000550 doi:10.1371/journal.pgen.1000550

16. NeafseyDE, LawniczakMK, ParkDJ, RedmondSN, CoulibalyMB, et al. (2010) SNP genotyping defines complex gene-flow boundaries among African malaria vector mosquitoes. Science 330 : 514–517.

17. MichelAP, SimS, PowellTH, TaylorMS, NosilP, et al. (2010) Widespread genomic divergence during sympatric speciation. Proc Natl Acad Sci U S A 107 : 9724–9729.

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

19. AndresJA, LarsonEL, BogdanowiczSM, HarrisonRG (2013) Patterns of transcriptome divergence in the male accessory gland of two closely related species of field crickets. Genetics 193 : 501–513.

20. BrancoM, FerrandN, MonnerotM (2000) Phylogeography of the European rabbit (Oryctolagus cuniculus) in the Iberian Peninsula inferred from RFLP analysis of the cytochrome b gene. Heredity 85 : 307–317.

21. CarneiroM, FerrandN, NachmanMW (2009) Recombination and speciation: loci near centromeres are more differentiated than loci near telomeres between subspecies of the European rabbit (Oryctolagus cuniculus). Genetics 181 : 593–606.

22. SharplesCM, FaJE, BellDJ (1996) Geographic variation in size in the European rabbit Oryctolagus cuniculus (Lagomorpha: LEPORIDAE) in western Europe and North Africa. Zool J Linn Soc-London 117 : 141–158.

23. Villafuerte R (2002) Oryctolagus cuniculus, pp. 464–466 in Atlas de los Mamíferos Terrestres de España, edited by L. J. Palomo and J. Gisbert. Dirección General de Conservación de la Naturaleza-SECEM-SECEMU, Madrid. [ In Spanish]

24. GeraldesA, CarneiroM, Delibes-MateosM, VillafuerteR, NachmanMW, et al. (2008) Reduced introgression of the Y chromosome between subspecies of the European rabbit (Oryctolagus cuniculus) in the Iberian Peninsula. Mol Ecol 17 : 4489–4499.

25. GeraldesA, FerrandN, NachmanMW (2006) Contrasting patterns of introgression at X-linked loci across the hybrid zone between subspecies of the European rabbit (Oryctolagus cuniculus). Genetics 173 : 919–933.

26. CarneiroM, Blanco-AguiarJA, VillafuerteR, FerrandN, NachmanMW (2010) Speciation in the European rabbit (Oryctolagus cuniculus): islands of differentiation on the X chromosome and autosomes. Evolution 64 : 3443–3460.

27. CarneiroM, BairdSJE, AfonsoS, RamirezE, VillafuerteR, et al. (in press) Steep clines within a highly permeable genome between two subspecies of the European rabbit. Mol Ecol

28. AlbertFW, SomelM, CarneiroM, Aximu-PetriA, HalbwaxM, et al. (2012) A Comparison of Brain Gene Expression Levels in Domesticated and Wild Animals. PLoS Genet 8: e1002962 doi:10.1371/journal.pgen.1002962

29. CarneiroM, AlbertFW, Melo-FerreiraJ, GaltierN, GayralP, et al. (2012) Evidence for widespread positive and purifying selection across the European rabbit (Oryctolagus cuniculus) genome. Mol Biol Evol 29 : 1837–49.

30. RoestiM, SalzburgerW, BernerD (2012) Uninformative polymorphisms bias genome scans for signatures of selection. BMC Evol Biol 12

31. The International HapMap Consortium (2005) A haplotype map of the human genome. Nature 437 : 1299–1320.

32. ReidenbachKR, NeafseyDE, CostantiniC, SagnonN, SimardF, et al. (2012) Patterns of Genomic Differentiation between Ecologically Differentiated M and S Forms of Anopheles gambiae in West and Central Africa. Genome Biol Evol 4 : 1202–12.31.

33. LawniczakMK, EmrichSJ, HollowayAK, RegierAP, OlsonM, et al. (2010) Widespread divergence between incipient Anopheles gambiae species revealed by whole genome sequences. Science 330 : 512–514.

34. YatabeY, KaneNC, Scotti-SaintagneC, RiesebergLH (2007) Rampant gene exchange across a strong reproductive barrier between the annual sunflowers, Helianthus annuus and H. petiolaris. Genetics 175 : 1883–1893.

35. StrasburgJL, RiesebergLH (2008) Molecular demographic history of the annual sunflowers Helianthus annuus and H. petiolaris: Large effective population sizes and rates of long-term gene flow. Evolution 62 : 1936–1950.

36. 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.

37. 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.

38. Soriguer RC (1983) El conejo: papel ecológico y estrategia de vida en los ecosistemas mediterrâneos. In Proc.: XV Congreso Internacional de Fauna Cinegética y Silvestre, Trujillo, Spain, pp 517–542.

39. Maynard SmithJ, HaighJ (1974) The hitch-hiking effect of a favourable gene. Genet Res 23 : 23–35.

40. CharlesworthB, MorganMT, CharlesworthD (1993) The Effect of Deleterious Mutations on Neutral Molecular Variation. Genetics 134 : 1289–1303.

41. FederJL, XieXF, RullJ, VelezS, ForbesA, et al. (2005) Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis. Proceedings of the National Academy of Sciences of the United States of America 102 : 6573–6580.

42. CharlesworthB (1998) Measures of divergence between populations and the effect of forces that reduce variability. Mol Biol Evol 15 : 538–543.

43. NoorMAF, BennettSM (2010) Islands of speciation or mirages in the desert? Examining the role of restricted recombination in maintaining species (vol 103, pg 434, 2009). Heredity 104 : 418–418.

44. FayJC, WuCI (2000) Hitchhiking under positive Darwinian selection. Genetics 155 : 1405–13.

45. LiHP (2011) A New Test for Detecting Recent Positive Selection that is Free from the Confounding Impacts of Demography. Mol Biol Evol 28 : 365–375.

46. GoodJM, DeanMD, NachmanMW (2008) A complex genetic basis to X-linked hybrid male sterility between two species of house mice. Genetics 179 : 2213–2228.

47. PattersonN, RichterDJ, GnerreS, LanderES, ReichD (2006) Genetic evidence for complex speciation of humans and chimpanzees. Nature 441 : 1103–1108.

48. PresgravesDC, YiSV (2009) Doubts about complex speciation between humans and chimpanzees. Trends in Ecology & Evolution 24 : 533–540.

49. KongA, GudbjartssonDF, SainzJ, JonsdottirGM, GudjonssonSA, et al. (2002) A high-resolution recombination map of the human genome. Nat Genet 31 : 241–247.

50. MaslyJP, PresgravesDC (2007) High-resolution genome-wide dissection of the two rules of speciation in Drosophila. PLoS Biol 5: e243 doi:10.1371/journal.pbio.0050243

51. FariaR, NavarroA (2010) Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol Evol 25 : 660–669.

52. VranaPB, FossellaJA, MattesonP, del RioT, O'NeillMJ, et al. (2000) Genetic and epigenetic incompatibilities underlie hybrid dysgenesis in Peromyscus. Nat Genet 25 : 120–124.

53. GoodJM, GigerT, DeanMD, NachmanMW (2010) Widespread over-expression of the X chromosome in sterile F1 hybrid mice. PLoS Genet 6: e1001148 doi:10.1371/journal.pgen.1001148

54. PresgravesDC, BalagopalanL, AbmayrSM, OrrHA (2003) Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423 : 715–719.

55. TingCT, TsaurSC, SunS, BrowneWE, ChenYC, et al. (2004) Gene duplication and speciation in Drosophila: evidence from the Odysseus locus. Proc Natl Acad Sci U S A 101 : 12232–12235.

56. BrideauNJ, FloresHA, WangJ, MaheshwariS, WangX, et al. (2006) Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 314 : 1292–1295.

57. OliverPL, GoodstadtL, BayesJJ, BirtleZ, RoachKC, et al. (2009) Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa. PLoS Genet 5: e1000753 doi:10.1371/journal.pgen.1000753

58. SunF, PalmerK, HandelMA (2010) Mutation of Eif4g3, encoding a eukaryotic translation initiation factor, causes male infertility and meiotic arrest of mouse spermatocytes. Development 137 : 1699–1707.

59. ZindyF, den BestenW, ChenB, RehgJE, LatresE, et al. (2001) Control of spermatogenesis in mice by the cyclin D-dependent kinase inhibitors p18(Ink4c) and p19(Ink4d). Mol Cell Biol 21 : 3244–3255.

60. HodgesE, RooksM, XuanZ, BhattacharjeeA, Benjamin GordonD, et al. (2009) Hybrid selection of discrete genomic intervals on custom-designed microarrays for massively parallel sequencing. Nat Protoc 4 : 960–974.

61. TrapnellC, PachterL, SalzbergSL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25 : 1105–1111.

62. MeyerM, KircherM (2010) Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb Protoc 2010: pdb prot5448.

63. KircherM, StenzelU, KelsoJ (2009) Improved base calling for the Illumina Genome Analyzer using machine learning strategies. Genome Biol 10: R83.

64. LiH, DurbinR (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25 : 1754–1760.

65. LiH, HandsakerB, WysokerA, FennellT, RuanJ, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25 : 2078–2079.

66. HalliganDL, OliverF, Eyre-WalkerA, HarrB, KeightleyPD (2010) Evidence for Pervasive Adaptive Protein Evolution in Wild Mice. PLoS Genet 6: e1000825 doi:10.1371/journal.pgen.1000825

67. WattersonGA (1975) On the number of segregating sites in genetical models without recombination. Theoretical Population Biology 7 : 256–276.

68. Nei M (1987) Molecular Evolutionary Genetics. New York: Columbia University Press. 512 p.

69. TajimaF (1989) Statistical-Method for Testing the Neutral Mutation Hypothesis by DNA Polymorphism. Genetics 123 : 585–595.

70. WeirBS, CockerhamCC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38 : 1358–1370.

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

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

73. Eyre-WalkerA, KeightleyPD (2009) Estimating the rate of adaptive molecular evolution in the presence of slightly deleterious mutations and population size change. Mol Biol Evol 26 : 2097–2108.

74. DurinckS, MoreauY, KasprzykA, DavisS, De MoorB, et al. (2005) BioMart and Bioconductor: a powerful link between biological databases and microarray data analysis. Bioinformatics 21 : 3439–40.

75. DennisGJr, ShermanBT, HosackDA, YangJ, GaoW, et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3.