, Volume 138, Issue 4, pp 409–418 | Cite as

Population genomics and speciation

  • Roger K. Butlin


The process of speciation begins with genomically-localised barriers to gene exchange associated with loci for local adaptation, intrinsic incompatibility or assortative mating. The barrier then spreads until reproductive isolation influences the whole genome. The population genomics approach can be used to identify regions of reduced gene flow by detecting loci with greater differentiation than expected from the average across many loci. Recently, this approach has been used in several systems. I review these studies, concentrating on the robustness of the approach and the methods available to go beyond the simple identification of differentiated markers. Population genomics has already contributed significantly to understanding the balance between gene flow and selection during the evolution of reproductive isolation and has great future potential both in genome species and in non-model organisms.


FST Genome scan Reproductive isolation Local adaptation 



I am very grateful to Jacob Hoglund and Gernot Segelbacher for organising, and inviting me to attend, the very stimulating workshop from which these proceedings are derived. The workshop was funded by the European Science Foundation. Discussions with Juan Galindo about population genomics approaches have been important in the development of this paper. My work on Littorina is in collaboration with John Grahame and has been funded by the BBSRC.


  1. Akey JM, Zhang G, Zhang K, Jin L, Shriver MD (2002) Interrogating a high-density SNP map for signatures of natural selection. Genome Res 12:1805–1814. doi: 10.1101/gr.631202 CrossRefPubMedGoogle Scholar
  2. Beaumont MA (2005) Adaptation and speciation: what can FST tell us? Trends Ecol Evol 20:435–440. doi: 10.1016/j.tree.2005.05.017 CrossRefPubMedGoogle Scholar
  3. Beaumont MA, Balding DJ (2004) Identifying adaptive genetic divergence among populations from genome scans. Mol Ecol 13:969–980. doi: 10.1111/j.1365-294X.2004.02125.x CrossRefPubMedGoogle Scholar
  4. Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond B Biol Sci 263:1619–1626. doi: 10.1098/rspb.1996.0237 CrossRefGoogle Scholar
  5. Bonin A, Taberlet P, Miaud C, Pompanon F (2006) Explorative genome scan to detect candidate loci for adaptation along a gradient of altitude in the common frog (Rana temporaria). Mol Biol Evol 23:773–783. doi: 10.1093/molbev/msj087 CrossRefPubMedGoogle Scholar
  6. Boursot P, Belkhir K (2006) Mouse SNPs for evolutionary biology: beware of ascertainment biases. Genome Res 16:1191–1192. doi: 10.1101/gr.5541806 CrossRefPubMedGoogle Scholar
  7. Caballero A, Quesada H, Rolán-Alvarez E (2008) Impact of AFLP fragment size homoplasy on the estimation of population genetic diversity and the detection of selective loci. Genetics 179(1):539–554CrossRefPubMedGoogle Scholar
  8. Campbell D, Bernatchez L (2004) Generic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. Mol Biol Evol 21:945–956. doi: 10.1093/molbev/msh101 CrossRefPubMedGoogle Scholar
  9. Charlesworth B, Nordborg M, Charlesworth D (1997) The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations. Genet Res 70:155–174. doi: 10.1017/S0016672397002954 CrossRefPubMedGoogle Scholar
  10. Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, SunderlandGoogle Scholar
  11. De Kovel CGF (2006) The power of allele frequency comparisons to detect the footprint of selection in natural and experimental situations. Genet Sel Evol 38:3–23. doi: 10.1051/gse:2005024 CrossRefPubMedGoogle Scholar
  12. Egan SR, Nosil P, Funk DJ (2008) Selection and genomic differentiation during ecological speciation: isolating the contributions of host-association via a comparative genome scan of Neochlamisus bebbianae leaf beetles. Evolution (online early)Google Scholar
  13. Emelianov I, Marec F, Mallet J (2004) Genomic evidence for divergence with gene flow in host races of the larch budmoth. Proc R Soc Lond B Biol Sci 271:97–105. doi: 10.1098/rspb.2003.2574 CrossRefGoogle Scholar
  14. Eveno E, Collada C, Guevara MA, Leger V, Soto A, Diaz L et al (2008) Contrasting patterns of selection at Pinus pinaster Ait. drought stress candidate genes as revealed by genetic differentiation analyses. Mol Biol Evol 25:417–437. doi: 10.1093/molbev/msm272 CrossRefPubMedGoogle Scholar
  15. Feder JL, Roethele FB, Filchak K, Niedbalski J, Romero-Severson J (2003) Evidence for inversion polymorphism related to sympatric host race formation in the apple maggot fly, Rhagoletis pomonella. Genetics 163:939–953PubMedGoogle Scholar
  16. Gavrilets S, Vose A (2007) Case studies and mathematical models of ecological speciation. 2. Palms on an oceanic island. Mol Ecol 16:2910–2921. doi: 10.1111/j.1365-294X.2007.03304.x CrossRefPubMedGoogle Scholar
  17. Grahame JW, Wilding CS, Butlin RK (2006) Adaptation to a steep environmental gradient and an associated barrier to gene exchange in Littorina saxatilis. Evolution 60:268–278PubMedGoogle Scholar
  18. Harr B (2006a) Genomic islands of differentiation between house mouse subspecies. Genome Res 16:730–737. doi: 10.1101/gr.5045006 CrossRefPubMedGoogle Scholar
  19. Harr B (2006b) Regions of high differentiation—worth a check. Genome Res 16:1193–1194. doi: 10.1101/gr.5787706 CrossRefPubMedGoogle Scholar
  20. Kelley JL, Madeoy J, Calhoun JC, Swanson W, Akey JM (2006) Genomic signatures of positive selection in humans and the limits of outlier approaches. Genome Res 16:980–989. doi: 10.1101/gr.5157306 CrossRefPubMedGoogle Scholar
  21. Lewontin RC, Krakauer J (1973) Distribution of gene frequency as a test of theory of selective neutrality of polymorphisms. Genetics 74:175–195PubMedGoogle Scholar
  22. Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet 4:981–994. doi: 10.1038/nrg1226 CrossRefPubMedGoogle Scholar
  23. Mäkinen HS, Cano JM, Merilä J (2008) Identifying footprints of directional and balancing selection in marine and freshwater three-spined stickleback (Gasterosteus aculeatus) populations. Mol Ecol 17:3565–3582. doi: 10.1111/j.1365-294X.2008.03714.x CrossRefPubMedGoogle Scholar
  24. Minder AM, Widmer A (2008) A population genomic analysis of species boundaries: neutral processes, adaptive divergence and introgression between two hybridizing plant species. Mol Ecol (online early)Google Scholar
  25. Murray MC, Hare MP (2006) A genomic scan for divergent selection in a secondary contact zone between Atlantic and Gulf of Mexico oysters, Crassostrea virginica. Mol Ecol 15:4229–4242. doi: 10.1111/j.1365-294X.2006.03060.x CrossRefPubMedGoogle Scholar
  26. Nielsen R (2005) Molecular signatures of natural selection. Annu Rev Genet 39:197–218. doi: 10.1146/annurev.genet.39.073003.112420 CrossRefPubMedGoogle Scholar
  27. Nosil P, Vines TH, Funk DJ (2005) Perspective: reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59:705–719PubMedGoogle Scholar
  28. Nosil P, Egan SR, Funk DJ (2008) Heterogeneous genomic differentiation between walking-stick ecotypes: “isolation by adaptation” and multiple roles for divergent selection. Evolution 62:316–336. doi: 10.1111/j.1558-5646.2007.00299.x CrossRefPubMedGoogle Scholar
  29. Ortiz-Barrientos D, Reiland J, Hey J, Noor MAF (2002) Recombination and the divergence of hybridizing species. Genetica 116:167–178. doi: 10.1023/A:1021296829109 CrossRefPubMedGoogle Scholar
  30. Poinar HN, Schwarz C, Qi J, Shapiro B, MacPhee RDE, Buigues B et al (2006) Metagenomics to paleogenomics: large-scale sequencing of mammoth DNA. Science 311:392–394. doi: 10.1126/science.1123360 CrossRefPubMedGoogle Scholar
  31. Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev Genet 6:847–859. doi: 10.1038/nrg1707 CrossRefPubMedGoogle Scholar
  32. Pool JE, DuMont VB, Mueller JL, Aquadro CF (2006) A scan of molecular variation leads to the narrow localization of a selective sweep affecting both afrotropical and cosmopolitan populations of Drosophila melanogaster. Genetics 172:1093–1105. doi: 10.1534/genetics.105.049973 CrossRefPubMedGoogle Scholar
  33. Presgraves DC (2003) A fine-scale genetic analysis of hybrid incompatibilities in Drosophila. Genetics 163:955–972PubMedGoogle Scholar
  34. Price T (2007) Speciation in birds. Roberts and Company, Greenwood VillageGoogle Scholar
  35. Roberge C, Guderley H, Bernatchez L (2007) Genomewide identification of genes under directional selection: gene transcription QST scan in diverging Atlantic salmon subpopulations. Genetics 177:1011–1022. doi: 10.1534/genetics.107.073759 CrossRefPubMedGoogle Scholar
  36. Roelofs W, Glover T, Tang XH, Sreng I, Robbins P, Eckenrode C et al (1987) Sex pheromone production and perception in European corn-borer moths is determined by both autosomal and sex-linked genes. Proc Natl Acad Sci USA 84:7585–7589. doi: 10.1073/pnas.84.21.7585 CrossRefPubMedGoogle Scholar
  37. Rogers SM, Bernatchez L (2005) Integrating QTL mapping and genome scans towards the characterization of candidate loci under parallel selection in the lake whitefish (Coregonus clupeaformis). Mol Ecol 14:351–361. doi: 10.1111/j.1365-294X.2004.02396.x CrossRefPubMedGoogle Scholar
  38. Rogers SM, Bernatchez L (2007) The genetic architecture of ecological speciation and the association with signatures of selection in natural lake whitefish (Coregonas sp., Salmonidae) species pairs. Mol Biol Evol 24:1423–1438. doi: 10.1093/molbev/msm066 CrossRefPubMedGoogle Scholar
  39. Savolainen V, Anstett MC, Lexer C, Hutton I, Clarkson JJ, Norup MV et al (2006) Sympatric speciation in palms on an oceanic island. Nature 441:210–213. doi: 10.1038/nature04566 CrossRefPubMedGoogle Scholar
  40. Servedio MR, Noor MAF (2003) The role of reinforcement in speciation: theory and data. Annu Rev Ecol Evol Syst 34:339–364. doi: 10.1146/annurev.ecolsys.34.011802.132412 CrossRefGoogle Scholar
  41. Singleton DR (2008) Evaluating the reliability of FST-based methods at detecting the signature of selection in microsatellite markers linked to a selection-targeted locus. Ph.D. thesis, University of ReadingGoogle Scholar
  42. Smadja C, Galindo J, Butlin RK (2008) Hitching a lift on the road to speciation. Mol Ecol (in press)Google Scholar
  43. Stinchcombe JR, Hoekstra HE (2007) Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100:158–170. doi: 10.1038/sj.hdy.6800937 CrossRefPubMedGoogle Scholar
  44. Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14:671–688. doi: 10.1111/j.1365-294X.2005.02437.x CrossRefPubMedGoogle Scholar
  45. Teshima KM, Coop G, Przeworski M (2006) How reliable are empirical genomic scans for selective sweeps? Genome Res 16:702–712. doi: 10.1101/gr.5105206 CrossRefPubMedGoogle Scholar
  46. Thornton K, Andolfatto P (2006) Approximate Bayesian inference reveals evidence for a recent, severe bottleneck in a Netherlands population of Drosophila melanogaster. Genetics 172:1607–1619. doi: 10.1534/genetics.105.048223 CrossRefPubMedGoogle Scholar
  47. Ting CT, Tsaur SC, Wu ML, Wu CI (1998) A rapidly evolving homeobox at the site of a hybrid sterility gene. Science 282:1501–1504. doi: 10.1126/science.282.5393.1501 CrossRefPubMedGoogle Scholar
  48. Turner TL, Hahn MW (2007) Locus- and population-specific selection and differentiation between incipient species of Anopheles gambiae. Mol Biol Evol 24:2132–2138. doi: 10.1093/molbev/msm143 CrossRefPubMedGoogle Scholar
  49. Turner TL, Hahn MW, Nuzhdin SV (2005) Genomic islands of speciation in Anopheles gambiae. PLoS Biol 3:1572–1578. doi: 10.1371/journal.pbio.0030285 CrossRefGoogle Scholar
  50. Vasemagi A, Nilsson J, Primmer CR (2005) Expressed sequence tag-linked microsatellites as a source of gene-associated polymorphisms for detecting signatures of divergent selection in Atlantic salmon (Salmo salar L.). Mol Biol Evol 22:1067–1076. doi: 10.1093/molbev/msi093 CrossRefPubMedGoogle Scholar
  51. Vekemans X, Beauwens T, Lemaire M, Roldan-Ruiz I (2002) Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Mol Ecol 11:139–151. doi: 10.1046/j.0962-1083.2001.01415.x CrossRefPubMedGoogle Scholar
  52. Via S, West J (2008) The genetic mosaic suggests a new role for hitchhiking in ecological speciation. Mol Ecol (in press)Google Scholar
  53. Vitalis R, Dawson K, Boursot P, Belkhir K (2003) DetSel 1.0: a computer program to detect markers responding to selection. J Hered 94:429–431. doi: 10.1093/jhered/esg083 CrossRefPubMedGoogle Scholar
  54. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M et al (1995) AFLP—a new technique for DNA-fingerprinting. Nucleic Acids Res 23:4407–4414. doi: 10.1093/nar/23.21.4407 CrossRefPubMedGoogle Scholar
  55. Wakeley J (1999) Nonequilibrium migration in human history. Genetics 153:1863–1871PubMedGoogle Scholar
  56. Wilding CS, Butlin RK, Grahame J (2001) Differential gene exchange between parapatric morphs of Littorina saxatilis detected using AFLP markers. J Evol Biol 14:611–619. doi: 10.1046/j.1420-9101.2001.00304.x CrossRefGoogle Scholar
  57. Wood HM, Grahame JW, Humphray S, Rogers J, Butlin RK (2008) Sequence differentiation in regions identified by a genome scan for local adaptation. Mol Ecol 17(13):3123–3135CrossRefPubMedGoogle Scholar
  58. Wu CI (2001) The genic view of the process of speciation. J Evol Biol 14:851–865. doi: 10.1046/j.1420-9101.2001.00335.x CrossRefGoogle Scholar
  59. Yatabe Y, Kane NC, Scotti-Saintagne C, Rieseberg LH (2007) Rampant gene exchange across a strong reproductive barrier between the annual sunflowers, Helianthus annuus and H. petiolaris. Genetics 175:1883–1893. doi: 10.1534/genetics.106.064469 CrossRefPubMedGoogle Scholar
  60. Zhivotovsky LA (1999) Estimating population structure in diploids with multilocus dominant DNA markers. Mol Ecol 8:907–913. doi: 10.1046/j.1365-294x.1999.00620.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.Department of Animal and Plant SciencesThe University of SheffieldSheffieldUK

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