Genomics of Divergence along a Continuum of Parapatric Population Differentiation

English version České info

A variety of evolutionary forces influence the genomic landscape of divergence during ecological speciation. Here we characterize the evolution of genomic divergence patterns based on 60 fully sequenced three-spined stickleback genomes, contrasting lake and river populations that differ in parasite abundance. Our comparison of the size and abundance of divergent regions in the genomes across a continuum of population differentiation suggests that selection and the hitchhiking effect on neutral sites mainly contributes to the observed heterogeneous patterns of genomic divergence. Additional divergent regions of the genome can be explained by a local reduction of gene flow. Our description of genomic divergence patterns across a continuum of population differentiation combined with an analysis of molecular signatures of evolution highlights how adaptation shapes the differentiation of sticklebacks in freshwater habitats.

Vyšlo v časopise: Genomics of Divergence along a Continuum of Parapatric Population Differentiation. PLoS Genet 11(2): e32767. doi:10.1371/journal.pgen.1004966
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004966

Souhrn

Zdroje

1. Hanikenne M, Kroymann J, Trampczynska A, Bernal M, Motte P, et al. (2013) Hard Selective Sweep and Ectopic Gene Conversion in a Gene Cluster Affording Environmental Adaptation. PLoS Genet 9: e1003707. doi: 10.1371/journal.pgen.1003707 23990800

2. Sadier, A, Viriot, L, Pantalacci, S, Laudet, V The ectodysplasin pathway: from diseases to adaptations. Trends Genet.

3. Soria-Carrasco V, Gompert Z, Comeault AA, Farkas TE, Parchman TL, et al. (2014) Stick insect genomes reveal natural selection’s role in parallel speciation. Science 344: 738–742. doi: 10.1126/science.1252136 24833390

4. Renaut S, Grassa CJ, Yeaman S, Moyers BT, Lai Z, et al. (2013) Genomic islands of divergence are not affected by geography of speciation in sunflowers. Nat Commun 4: 1827. doi: 10.1038/ncomms2833 23652015

5. Via S, Conte G, Mason-Foley C, Mills K (2012) Localizing FST outliers on a QTL map reveals evidence for large genomic regions of reduced gene exchange during speciation-with-gene-flow. Mol Ecol 21: 5546–5560. doi: 10.1111/mec.12021 23057835

6. Turner TL, Hahn MW, Nuzhdin SV (2005) Genomic islands of speciation in Anopheles gambiae. PLoS Biol 3: e285. doi: 10.1371/journal.pbio.0030285 16076241

7. Seehausen O, Butlin RK, Keller I, Wagner CE, Boughman JW, et al. (2014) Genomics and the origin of species. Nat Rev Genet 15: 176–192. doi: 10.1038/nrg3644 24535286

8. Wu CI, Ting CT (2004) Genes and speciation. Nat Rev Genet 5: 114–122. doi: 10.1038/nrg1269 14735122

9. Feder JL, Egan SP, Nosil P (2012) The genomics of speciation-with-gene-flow. Trends Genet 28: 342–350. doi: 10.1016/j.tig.2012.03.009 22520730

10. Noor MAF, Bennett SM (2009) Islands of speciation or mirages in the desert? Examining the role of restricted recombination in maintaining species. Heredity 103: 439–444. doi: 10.1038/hdy.2009.151 19920849

11. White BJ, Cheng C, Simard F, Costantini C, Besansky NJ (2010) Genetic association of physically unlinked islands of genomic divergence in incipient species of Anopheles gambiae. Mol Ecol 19: 925–939. doi: 10.1111/j.1365-294X.2010.04531.x 20149091

12. Nachman MW, Payseur BA (2012) Recombination rate variation and speciation: theoretical predictions and empirical results from rabbits and mice. Philos Trans R Soc Biol Sci 367: 409–421. doi: 10.1098/rstb.2011.0249

13. Berner D, Roesti M, Hendry AP, Salzburger W (2010) Constraints on speciation suggested by comparing lake-stream stickleback divergence across two continents. Mol Ecol 19: 4963–4978. doi: 10.1111/j.1365-294X.2010.04858.x 20964754

14. Kalbe M, Wegner KM, Reusch TBH (2002) Dispersion patterns of parasites in 0+ year three-spined sticklebacks: a cross population comparison. J Fish Biol 60: 1529–1542. doi: 10.1111/j.1095-8649.2002.tb02445.x

15. Eizaguirre C, Lenz TL, Kalbe M, Milinski M (2012) Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations. Nat Commun 3: 621. doi: 10.1038/ncomms1632 22233631

16. Wegner KM, Reusch TBH, Kalbe M (2003) Multiple parasites are driving major histocompatibility complex polymorphism in the wild. J Evol Biol 16: 224–232. doi: 10.1046/j.1420-9101.2003.00519.x 14635861

17. Chain FJJ, Feulner PGD, Panchal M, Eizaguirre C, Samonte IE, et al. (2014) Extensive copy-number variation of young genes across stickleback populations. PLoS Genet 10: e1004830. doi: 10.1371/journal.pgen.1004830 25474574

18. Eizaguirre C, Lenz TL, Traulsen A, Milinski M (2009) Speciation accelerated and stabilized by pleiotropic major histocompatibility complex immunogenes. Ecol Lett 12: 5–12. doi: 10.1111/j.1461-0248.2008.01247.x 19087108

19. Nosil P, Funk DJ, Ortiz-Barrientos D (2009) Divergent selection and heterogeneous genomic divergence. Mol Ecol 18: 375–402. doi: 10.1111/j.1365-294X.2008.03946.x 19143936

20. Deagle BE, Jones FC, Chan YGF, Absher DM, Kingsley DM, et al. (2012) Population genomics of parallel phenotypic evolution in stickleback across stream-lake ecological transitions. Proc R Soc Biol Sci Ser 279: 1277–1286. doi: 10.1098/rspb.2011.1552

21. Roesti M, Hendry AP, Salzburger W, Berner D (2012) Genome divergence during evolutionary diversification as revealed in replicate lake—stream stickleback population pairs. Mol Ecol 21: 2852–2862. doi: 10.1111/j.1365-294X.2012.05509.x 22384978

22. Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E, et al. (2012) The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484: 55–61. doi: 10.1038/nature10944 22481358

23. Hohenlohe PA, Bassham S, Etter PD, Stiffler N, Johnson EA, et al. (2010) Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet 6: e1000862. doi: 10.1371/journal.pgen.1000862 20195501

24. Kaeuffer R, Peichel CL, Bolnick DI, Hendry AP (2012) Parallel and nonparallel aspects of ecological, phenotypic, and genetic divergence across replicate population pairs of lake and stream stickleback Evolution 66: 402–418.

25. Barton N, Bengtsson BO (1986) The barrier to genetic exchange between hybridising populations. Heredity 57: 357–376. doi: 10.1038/hdy.1986.135 3804765

26. Keinan A, Reich D (2010) Human population differentiation is strongly correlated with local recombination rate. PLoS Genet 6: e1000886. doi: 10.1371/journal.pgen.1000886 20361044

27. Feder JL, Gejji R, Yeaman S, Nosil P (2012) Establishment of new mutations under divergence and genome hitchhiking. Philos Trans R Soc Biol Sci 367: 461–474. doi: 10.1098/rstb.2011.0256

28. Feder JL, Nosil P (2010) The efficacy of divergence hitchhiking in generating genomic islands during ecological speciation. Evolution 64: 1729–1747. doi: 10.1111/j.1558-5646.2009.00943.x 20624183

29. Roesti M, Moser D, Berner D (2013) Recombination in the threespine stickleback genome—patterns and consequences. Mol Ecol 22: 3014–3027. doi: 10.1111/mec.12322 23601112

30. Hohenlohe PA, Bassham S, Currey M, Cresko WA (2012) Extensive linkage disequilibrium and parallel adaptive divergence across threespine stickleback genomes. Philos Trans R Soc Biol Sci 367: 395–408. doi: 10.1098/rstb.2011.0245

31. Feulner PGD, Chain FJJ, Panchal M, Eizaguirre C, Kalbe M, et al. (2013) Genome-wide patterns of standing genetic variation in a marine population of three-spined sticklebacks. Mol Ecol 22: 635–649. doi: 10.1111/j.1365-294X.2012.05680.x 22747593

32. Cruickshank TE, Hahn MW (2014) Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol Ecol 23: 3133–3157. doi: 10.1111/mec.12796 24845075

33. Smith JM, Haigh J (1974) The hitch-hiking effect of a favourable gene. Genetics Res 23: 23–35. doi: 10.1017/S0016672300014634

34. Charlesworth B, Morgan MT, Charlesworth D (1993) The effect of deleterious mutations on neutral molecular variation. Genetics 134: 1289–1303. 8375663

35. Cutter AD, Payseur BA (2013) Genomic signatures of selection at linked sites: unifying the disparity among species. Nat Rev Genet 14: 262–274. doi: 10.1038/nrg3425 23478346

36. Hofer T, Ray N, Wegmann D, Excoffier L (2009) Large allele frequency differences between human continental groups are more likely to have occurred by drift during range expansions than by selection. Annals of Human Genetics 73: 95–108. doi: 10.1111/j.1469-1809.2008.00489.x 19040659

37. Flicek P, Amode MR, Barrell D, Beal K, Brent S, et al. (2011) Ensembl 2011. Nucleic Acids Res 39: D800–D806. doi: 10.1093/nar/gkq1064 21045057

38. Li H, Ruan J, Durbin R (2008) Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res 18: 1851–1858. doi: 10.1101/gr.078212.108 18714091

39. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, et al. (2010) The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20: 1297–1303. doi: 10.1101/gr.107524.110 20644199

40. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43: 491–498. doi: 10.1038/ng.806 21478889

41. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943

42. Browning BL, Browning SR (2009) A unified approach to genotype imputation and haplotype-phase inference for large data sets of trios and unrelated individuals. Am J Hum Gen 84: 210–223. doi: 10.1016/j.ajhg.2009.01.005

43. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, et al. (2011) The variant call format and VCFtools. Bioinformatics 27: 2156–2158. doi: 10.1093/bioinformatics/btr330 21653522

44. Abyzov A, Urban AE, Snyder M, Gerstein M (2011) CNVnator: An approach to discover, genotype, and characterize typical and atypical CNVs from family and population genome sequencing. Genome Res 21: 974–984. doi: 10.1101/gr.114876.110 21324876

45. Nei M (1987) Molecular Evolutionary Genetics. New York: Columbia UP.

46. Roesti M, Salzburger W, Berner D (2012) Uninformative polymorphisms bias genome scans for signatures of selection. BMC Evol Biol 12: 94. doi: 10.1186/1471-2148-12-94 22726891

47. R_Development_Core_Team (2011) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

48. Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841–842. doi: 10.1093/bioinformatics/btq033 20110278

49. Waples R (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89: 438–450. doi: 10.1093/jhered/89.5.438

50. McCormick SD (2001) Endocrine control of osmoregulation in teleost fish1. Am Zool 41: 781–794. doi: 10.1668/0003-1569(2001)041%5B0781:ECOOIT%5D2.0.CO;2

51. Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G Jr., Dickson M, et al. (2005) Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307: 1928–1933. doi: 10.1126/science.1107239 15790847

52. Udpa N, Ronen R, Zhou D, Liang J, Stobdan T, et al. (2014) Whole genome sequencing of Ethiopian highlanders reveals conserved hypoxia tolerance genes. Genome Biol 15: R36. doi: 10.1186/gb-2014-15-2-r36 24555826

53. McVean GAT, Myers SR, Hunt S, Deloukas P, Bentley DR, et al. (2004) The fine-scale structure of recombination rate variation in the human genome. Science 304: 581–584. doi: 10.1126/science.1092500 15105499

54. Auton A, McVean G (2007) Recombination rate estimation in the presence of hotspots. Genome Res 17: 1219–1227. doi: 10.1101/gr.6386707 17623807

55. Auton A, Fledel-Alon A, Pfeifer S, Venn O, Ségurel L, et al. (2012) A fine-scale chimpanzee genetic map from population sequencing. Science 336: 193–198. doi: 10.1126/science.1216872 22422862

56. Alexa A, Rahnenführer J, Lengauer T (2006) Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22: 1600–1607. doi: 10.1093/bioinformatics/btl140 16606683