Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Genomics and the origin of species

Nature Reviews Genetics volume 15, pages 176–192 (2014)Cite this article

Subjects

Key Points

  • Speciation is a central and fundamental process in evolution that concerns the origin of reproductive isolation. The latest generation of genomic approaches provide remarkable opportunities to describe speciation and to learn about its underlying mechanisms.

  • Genome scans, which can now be carried out in a truly genome-wide scale and at base-pair resolution, reveal substantial genomic divergence among incipient species even in the face of gene flow and show that there is extensive genomic heterogeneity in the extent of differentiation, especially at early stages of speciation, both in sympatry and in allopatry.

  • The sources of this heterogeneity remain incompletely understood. The combination of genome scans with sophisticated population genetic modelling, quantitative trait locus mapping, admixture analyses and ecology has the potential to distinguish the influence of selection from demographic, historical and structural effects and to link these sources of genomic divergence to phenotypes and to reproductive isolation.

  • Available empirical data suggest that differentiation between parapatric populations can be restricted to few genomic islands, whereas incipient species that coexist in sympatry show differentiation that is widely distributed across the genome. This suggests that genomically widespread selection is required to permit the maintenance and perhaps the build-up of genetic differentiation in sympatry.

  • Recent genomic studies reveal that the genetic basis of reproductive isolation is often complex. The effects of pleiotropy, genetic correlations and patterns of recombination need to be considered alongside effects of ecological and sexual selection as well as genomic conflict.

  • A surprising recent discovery is the re-use of ancient genetic variants in speciation, which are acquired either from standing genetic variation or by introgressive hybridization.

  • In this Review, we propose a 'roadmap' for the development of speciation genomics towards answering classical and emerging questions in speciation research.

Abstract

Speciation is a fundamental evolutionary process, the knowledge of which is crucial for understanding the origins of biodiversity. Genomic approaches are an increasingly important aspect of this research field. We review current understanding of genome-wide effects of accumulating reproductive isolation and of genomic properties that influence the process of speciation. Building on this work, we identify emergent trends and gaps in our understanding, propose new approaches to more fully integrate genomics into speciation research, translate speciation theory into hypotheses that are testable using genomic tools and provide an integrative definition of the field of speciation genomics.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Genomic patterns of divergence along the 'speciation continuum' of Heliconius spp. butterflies.
Figure 2: Effect sizes of substitutions on phenotype and on reproductive isolation.
Figure 3: Influence of genetic constraints on speciation.

Similar content being viewed by others

References

  1. Coyne, J. & Orr, H. Speciation (Sinauer Associates, 2004). This comprehensive book is a must-read for every student of speciation. It provides excellent background information and reviews of all facets of research on the speciation process.

    Google Scholar 

  2. Nosil, P. Ecological Speciation (Oxford Univ. Press, 2012). This is an in-depth treatment of speciation by divergent natural selection.

    Book  Google Scholar 

  3. Price, T. Speciation in Birds (Roberts & Company, 2008).

    Google Scholar 

  4. Dobzhansky, T. Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 21, 113–135 (1936).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Muller, H. J. & Pontecorvo, G. Recessive genes causing interspecific sterility and other disharmonies between Drosophila melanogaster and simulans. Genetics 27, 157 (1942).

    Google Scholar 

  6. Gavrilets, S. Fitness Landscapes and the Origin of Species (Princeton Univ. Press, 2004).

    Google Scholar 

  7. van Doorn, G. S., Edelaar, P. & Weissing, F. J. On the origin of species by natural and sexual selection. Science 326, 1704–1707 (2009).

    Article  CAS  PubMed  Google Scholar 

  8. M'Gonigle, L. K., Mazzucco, R., Otto, S. P. & Dieckmann, U. Sexual selection enables long-term coexistence despite ecological equivalence. Nature 484, 506–509 (2012).

    Article  CAS  PubMed  Google Scholar 

  9. Gavrilets, S. & Losos, J. B. Adaptive radiation: contrasting theory with data. Science 323, 732–737 (2009).

    Article  CAS  PubMed  Google Scholar 

  10. Dieckmann, U., Doebeli, M., Metz, J. A. J. & Tautz, D. (eds) Adaptive Speciation (Cambridge Univ. Press, 2004).

    Book  Google Scholar 

  11. Coyne, J. A. & Orr, H. A. “Patterns of speciation in Drosophila” revisited. Evolution 51, 295–303 (1997). This is a key comparative study on the rate of evolution of reproductive isolation and was a model for similar studies in other taxa.

    Article  PubMed  Google Scholar 

  12. Nolte, V., Pandey, R. V., Kofler, R. & Schlötterer, C. Genome-wide patterns of natural variation reveal strong selective sweeps and ongoing genomic conflict in Drosophila mauritiana. Genome Res. 23, 99–110 (2013). In this paper, genome-sequence data show how widespread strong selection due to genomic conflict can be, which suggests that such selection may be a potent source of incompatibilities between previously isolated populations.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. van der Sluijs, I. et al. Female mating preference functions predict sexual selection against hybrids between sibling species of cichlid fish. Phil. Trans. R. Soc. B 363, 2871–2877 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Panhuis, T. M., Butlin, R., Zuk, M. & Tregenza, T. Sexual selection and speciation. Trends Ecol. Evol. 16, 364–371 (2001).

    Article  PubMed  Google Scholar 

  15. Boughman, J. W. How sensory drive can promote speciation. Trends Ecol. Evol. 17, 571–577 (2002).

    Article  Google Scholar 

  16. Maan, M. E. & Seehausen, O. Ecology, sexual selection and speciation. Ecol. Lett. 14, 591–602 (2011).

    Article  PubMed  Google Scholar 

  17. Hendry, A. P., Nosil, P. & Rieseberg, L. H. The speed of ecological speciation. Funct. Ecol. 21, 455–464 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  18. Abbott, R. et al. Hybridization and speciation. J. Evol. Biol. 26, 229–246 (2013).

    Article  CAS  PubMed  Google Scholar 

  19. Presgraves, D. C. Speciation genetics: search for the missing snowball. Curr. Biol. 20, R1073–R1074 (2010).

    Article  CAS  PubMed  Google Scholar 

  20. Presgraves, D. C. The molecular evolutionary basis of species formation. Nature Rev. Genet. 11, 175–180 (2010). This review summarizes empirical evidence on the genetic basis of hybrid dysfunction and focuses on work in genetic model organisms in which key genes have been identified.

    Article  CAS  PubMed  Google Scholar 

  21. Rieseberg, L. H. & Blackman, B. K. Speciation genes in plants. Ann. Bot. 106, 439–455 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Rieseberg, L. H. & Burke, J. M. A genic view of species integration — commentary. J. Evol. Biol. 14, 883–886 (2001).

    Article  Google Scholar 

  23. Bikard, D. et al. Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana. Science 323, 623–626 (2009).

    Article  CAS  PubMed  Google Scholar 

  24. Masly, J. P., Jones, C. D., Noor, M. A. F., Locke, J. & Orr, H. A. Gene transposition as a cause of hybrid sterility in Drosophila. Science 313, 1448–1450 (2006).

    Article  CAS  PubMed  Google Scholar 

  25. Ting, C. T. et al. Gene duplication and speciation in Drosophila: evidence from the Odysseus locus. Proc. Natl Acad. Sci. USA 101, 12232–12235 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Matute, D. R., Butler, I. A., Turissini, D. A. & Coyne, J. A. A test of the snowball theory for the rate of evolution of hybrid incompatibilities. Science 329, 1518–1521 (2010).

    Article  CAS  PubMed  Google Scholar 

  27. Moyle, L. C. & Nakazato, T. Hybrid incompatibility “snowballs” between Solanum species. Science 329, 1521–1523 (2010).

    Article  CAS  PubMed  Google Scholar 

  28. Stadler, T., Florez-Rueda, A. M. & Paris, M. Testing for “snowballing” hybrid incompatibilities in Solanum: impact of ancestral polymorphism and divergence estimates. Mol. Biol. Evol. 29, 31–34 (2012).

    Article  CAS  PubMed  Google Scholar 

  29. Lynch, M. & Force, A. G. The origin of interspecific genomic incompatibility via gene duplication. Am. Naturalist 156, 590–605 (2000).

    Article  Google Scholar 

  30. Schluter, D. Evidence for ecological speciation and its alternative. Science 323, 737–741 (2009).

    Article  CAS  PubMed  Google Scholar 

  31. Nei, M., Maruyama, T. & Wu, C. I. Models of evolution of reproductive isolation. Genetics 103, 557–579 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Ting, C. T., Tsaur, S. C., Wu, M. L. & Wu, C. I. A rapidly evolving homeobox at the site of a hybrid sterility gene. Science 282, 1501–1504 (1998).

    Article  CAS  PubMed  Google Scholar 

  33. Crespi, B. & Nosil, P. Conflictual speciation: species formation via genomic conflict. Trends Ecol. Evol. 28, 48–57 (2013).

    Article  PubMed  Google Scholar 

  34. Frank, S. A. Divergence of meiotic drive-suppression systems as an explanation for sex-biased hybrid sterility and inviability. Evolution 45, 262–267 (1991).

    PubMed  Google Scholar 

  35. Hurst, L. D. & Pomiankowski, A. Causes of sex ratio bias may account for unisexual sterility in hybrids: a new explanation of Haldane's rule and related phenomena. Genetics 128, 841–858 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Cocquet, J. et al. A genetic basis for a postmeiotic X versus Y chromosome intragenomic conflict in the mouse. PLoS Genet. 8, e1002900 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Malik, H. S. in Progress in Molecular and Subcellular Biology (ed. Ugarovic, D.) 33–52 (Springer, 2009).

    Google Scholar 

  38. Campbell, P., Good, J. M. & Nachman, M. W. Meiotic sex chromosome inactivation is disrupted in sterile hybrid male house mice. Genetics 193, 819–828 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Rebollo, R., Horard, B., Hubert, B. & Vieira, C. Jumping genes and epigenetics: towards new species. Gene 454, 1–7 (2010).

    Article  CAS  PubMed  Google Scholar 

  40. Watson, E. T. & Demuth, J. P. in Speciation: Natural Processes, Genetics and Biodiversity (ed. Michalak, P.) (Nova Science Publishers, 2013).

    Google Scholar 

  41. Burton, R. S. & Barreto, F. S. A disproportionate role for mtDNA in Dobzhansky–Muller incompatibilities? Mol. Ecol. 21, 4942–4957 (2012).

    Article  CAS  PubMed  Google Scholar 

  42. Sambatti, J. B. M., Ortiz-Barrientos, D., Baack, E. J. & Rieseberg, L. H. Ecological selection maintains cytonuclear incompatibilities in hybridizing sunflowers. Ecol. Lett. 11, 1082–1091 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  43. van Doorn, G. S. & Kirkpatrick, M. Turnover of sex chromosomes induced by sexual conflict. Nature 449, 909–912 (2007).

    Article  CAS  PubMed  Google Scholar 

  44. Charlesworth, D. & Charlesworth, B. Sex differences in fitness and selection for centric fusions between sex-chromosomes and autosomes. Genet. Res. 35, 205–214 (1980).

    Article  CAS  PubMed  Google Scholar 

  45. Kitano, J. et al. A role for a neo-sex chromosome in stickleback speciation. Nature 461, 1079–1083 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Parnell, N. F. & Streelman, J. T. Genetic interactions controlling sex and color establish the potential for sexual conflict in Lake Malawi cichlid fishes. Heredity 110, 239–246 (2013).

    Article  CAS  PubMed  Google Scholar 

  47. Yeaman, S. & Whitlock, M. C. The genetic architecture of adaptation under migration–selection balance. Evolution 65, 1897–1911 (2011).

    Article  PubMed  Google Scholar 

  48. Silver, L. The peculiar journey of a selfish chromosome: mouse t haplotypes and meiotic drive. Trends Genet. 9, 250–254 (1993).

    Article  CAS  PubMed  Google Scholar 

  49. Larracuente, A. M. & Presgraves, D. C. The selfish segregation distorter gene complex of Drosophila melanogaster. Genetics 192, 33–53 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Bull, J. J. Evolution of Sex-determining Mechanisms. (Benjamin/Cumings, 1983).

    Google Scholar 

  51. Phadnis, N. & Orr, H. A. A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 323, 376–379 (2009).

    Article  CAS  PubMed  Google Scholar 

  52. Saether, S. A. et al. Sex chromosome-linked species recognition and evolution of reproductive isolation in flycatchers. Science 318, 95–97 (2007).

    Article  CAS  PubMed  Google Scholar 

  53. Lindholm, A. & Breden, F. Sex chromosomes and sexual selection in poeciliid fishes. Am. Naturalist 160, S214–S224 (2002).

    Article  Google Scholar 

  54. Reeve, H. K. & Pfennig, D. W. Genetic biases for showy males: are some genetic systems especially conducive to sexual selection? Proc. Natl Acad. Sci. USA 100, 1089–1094 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Templeton, A. R. Mechanisms of speciation — a population genetic approach. Annu. Rev. Ecol. Systemat. 12, 23–48 (1981).

    Article  Google Scholar 

  56. Ayala, F. J. & Tracey, M. L. Genetic differentiation within and between species of Drosophila willistoni group. Proc. Natl Acad. Sci. USA 71, 999–1003 (1974).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Coyne, J. A. Genetics and speciation. Nature 355, 511–515 (1992).

    Article  CAS  PubMed  Google Scholar 

  58. Price, T. D. & Bouvier, M. M. The evolution of F1 postzygotic incompatibilities in birds. Evolution 56, 2083–2089 (2002).

    Article  PubMed  Google Scholar 

  59. Stelkens, R. B., Young, K. A. & Seehausen, O. The accumulation of reproductive incompatibilities in African cichlid fish. Evolution 64, 617–632 (2010).

    Article  PubMed  Google Scholar 

  60. Scopece, G., Musacchio, A., Widmer, A. & Cozzolino, S. Patterns of reproductive isolation in Mediterranean deceptive orchids. Evolution 61, 2623–2642 (2007).

    Article  PubMed  Google Scholar 

  61. Orr, H. A. & Turelli, M. The evolution of postzygotic isolation: accumulating Dobzhansky–Muller incompatibilities. Evolution 55, 1085–1094 (2001). This paper provides background on the evolution of reproductive isolation through postzygotic intrinsic barriers. It considers the dynamics of accumulation of Dobzhansky–Muller incompatibilities in diverging lineages.

    Article  CAS  PubMed  Google Scholar 

  62. Strasburg, J. L. & Rieseberg, L. H. Interpreting the estimated timing of migration events between hybridizing species. Mol. Ecol. 20, 2353–2366 (2011).

    Article  PubMed  Google Scholar 

  63. Nosil, P., Funk, D. J. & Ortiz-Barrientos, D. Divergent selection and heterogeneous genomic divergence. Mol. Ecol. 18, 375–402 (2009).

    Article  PubMed  Google Scholar 

  64. Strasburg, J. L. et al. What can patterns of differentiation across plant genomes tell us about adaptation and speciation? Phil. Trans. R. Soc. B 367, 364–373 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  65. Barton, N. Gene flow and speciation. Heredity 50, 213–213 (1983).

    Article  Google Scholar 

  66. Wu, C. I. The genic view of the process of speciation. J. Evol. Biol. 14, 851–865 (2001). This review discusses the process of speciation from a genetic perspective by highlighting the difference between thinking of the evolution of reproductive isolation as a whole-genome process and understanding the influence of specific loci on reproductive isolation and gene exchange. The idea that genes, but not whole genomes, are the unit of species differentiation is a seminal perspective, which is crucial to much of the current work in speciation genetics.

    Article  Google Scholar 

  67. Via, S. & West, J. The genetic mosaic suggests a new role for hitchhiking in ecological speciation. Mol. Ecol. 17, 4334–4345 (2008).

    Article  PubMed  Google Scholar 

  68. Feder, J. L., Egan, S. P. & Nosil, P. The genomics of speciation-with-gene-flow. Trends Genet. 28, 342–350 (2012). This review brings together empirical studies with theory on the effect of divergent selection on gene flow elsewhere in the genome to examine how reproductive isolation might spread through the genome as speciation proceeds.

    Article  CAS  PubMed  Google Scholar 

  69. Nadeau, N. J. et al. Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing. Phil. Trans. R. Soc. B 367, 343–353 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Andrew, R. L. & Rieseberg, L. H. Divergence is focused on few genomic regions early in speciation: incipient speciation of sunflower ecotypes. Evolution 67, 2468–2482 (2013). Applying genomic analysis at different points of the speciation continuum is important for understanding how reproductive isolation develops. This study shows how differentiation can be focused on a small proportion of the genome early in speciation.

    Article  PubMed  Google Scholar 

  71. Stolting, K. N. et al. Genomic scan for single nucleotide polymorphisms reveals patterns of divergence and gene flow between ecologically divergent species. Mol. Ecol. 22, 842–855 (2013).

    Article  CAS  PubMed  Google Scholar 

  72. Hohenlohe, P. A. et al. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet. 6, e100086 (2010).

    Article  CAS  Google Scholar 

  73. Deagle, B. E. et al. Population genomics of parallel phenotypic evolution in stickleback across stream- lake ecological transitions. Proc. R. Soc. B 279, 1277–1286 (2012).

    Article  CAS  PubMed  Google Scholar 

  74. Jones, F. C. et al. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484, 55–61 (2012). This is an example of how genomic data can inform about the genetic basis for repeated adaptation to similar environments. This study shows that stickleback fish populations throughout the northern hemisphere have repeatedly used the same genetic elements to adapt to freshwater environments.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Lawniczak, M. K. N. et al. Widespread divergence between incipient Anopheles gambiae species revealed by whole genome sequences. Science 330, 512–514 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Renaut, S. et al. Genomic islands of divergence are not affected by geography of speciation in sunflowers. Nature Commun. 4, 1827 (2013).

    Article  CAS  Google Scholar 

  77. Keller, I. et al. Population genomic signatures of divergent adaptation, gene flow, and hybrid speciation in the rapid radiation of Lake Victoria cichlid fishes. Mol. Ecol. 22, 2848–2863 (2012).

    Article  CAS  PubMed  Google Scholar 

  78. Jones, F. C. et al. A genome-wide SNP genotyping array reveals patterns of global and repeated species-pair divergence in sticklebacks. Curr. Biol. 22, 83–90 (2012).

    Article  CAS  PubMed  Google Scholar 

  79. Parchman, T. L. et al. The genomic consequences of adaptive divergence and reproductive isolation between species of manakins. Mol. Ecol. 22, 3304–3317 (2013).

    Article  CAS  PubMed  Google Scholar 

  80. Gagnaire, P.-A., Pavey, S. A., Normandeau, E. & Bernatchez, L. The genetic architecture of reproductive isolation during speciation-with-gene-flow in lake whitefish pairs assessed by RAD-sequencing. Evolution 67, 2483–2497 (2013).

    Article  PubMed  Google Scholar 

  81. Michel, A. P. et al. Widespread genomic divergence during sympatric speciation. Proc. Natl Acad. Sci. USA 107, 9724–9729 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  82. Via, S., Conte, G., Mason-Foley, C. & Mills, K. 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 (2012).

    Article  CAS  PubMed  Google Scholar 

  83. Roesti, M., Hendry, A. P., Salzburger, W. & Berner, D. Genome divergence during evolutionary diversification as revealed in replicate lake-stream stickleback population pairs. Mol. Ecol. 21, 2852–2862 (2012).

    Article  PubMed  Google Scholar 

  84. Garrigan, D. et al. Genome sequencing reveals complex speciation in the Drosophila simulans clade. Genome Res. 22, 1499–1511 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Neafsey, D. E. et al. SNP genotyping defines complex gene-flow boundaries among African malaria vector mosquitoes. Science 330, 514–517 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Nosil, P. et al. Genomic consequences of multiple speciation processes in a stick insect. Proc. R. Soc. B 279, 5058–5065 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  87. Martin, S. H. et al. Genome-wide evidence for speciation with gene flow in Heliconius butterflies. Genome Res. 23, 1817–1828 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Noor, M. A. F. & Bennett, S. M. Islands of speciation or mirages in the desert? Examining the role of restricted recombination in maintaining species. Heredity 103, 439–444 (2009).

    Article  CAS  PubMed  Google Scholar 

  89. Hahn, M. W., White, B. J., Muir, C. D. & Besansky, N. J. No evidence for biased co-transmission of speciation islands in Anopheles gambiae. Phil. Trans. R. Soc. B 367, 374–384 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  90. Sousa, V. & Hey, J. Understanding the origin of species with genome-scale data: modelling gene flow. Nature Rev. Genet. 14, 404–414 (2013).

    Article  CAS  PubMed  Google Scholar 

  91. Scally, A. et al. Insights into hominid evolution from the gorilla genome sequence. Nature 483, 169–175 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Charlesworth, B., Morgan, M. T. & Charlesworth, D. The effect of deleterious mutations on neutral molecular variation. Genetics 134, 1289–1303 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Spencer, C. C. A. et al. The influence of recombination on human genetic diversity. PLoS Genet. 2, 1375–1385 (2006).

    Article  CAS  Google Scholar 

  94. Nachman, M. W. & Payseur, B. A. Recombination rate variation and speciation: theoretical predictions and empirical results from rabbits and mice. Phil. Trans. R. Soc. B. 367, 409–421 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  95. Nei, M. Molecular Evolutionary Genetics (Columbia Univ. Press, 1987).

    Book  Google Scholar 

  96. Charlesworth, B. Measures of divergence between populations and the effect of forces that reduce variability. Mol. Biol. Evol. 15, 538–543 (1998).

    Article  CAS  PubMed  Google Scholar 

  97. Renaut, S., Owens, G. L. & Rieseberg, L. H. Shared selective pressure and local genomic landscape lead to repeatable patterns of genomic divergence in sunflowers. Mol. Ecol. 23, 311–324 (2014).

    Article  CAS  PubMed  Google Scholar 

  98. Ellegren, H. et al. The genomic landscape of species divergence in Ficedula flycatchers. Nature 491, 756–760 (2012). This paper presents a truly genome-wide view of differentiation in a system with remarkable ecological and behavioural information available. Strikingly heterogeneous levels of divergence were observed, including major divergence peaks at telomeres that are so far unexplained.

    Article  CAS  PubMed  Google Scholar 

  99. Heliconius Genome Consortium. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487, 94–98 (2012).

  100. Janousek, V. et al. Genome-wide architecture of reproductive isolation in a naturally occurring hybrid zone between Mus musculus musculus and M. m. domesticus. Mol. Ecol. 21, 3032–3047 (2012).

    Article  PubMed  Google Scholar 

  101. Elmer, K. R. & Meyer, A. Adaptation in the age of ecological genomics: insights from parallelism and convergence. Trends Ecol. Evol. 26, 298–306 (2011).

    Article  PubMed  Google Scholar 

  102. Nosil, P., Egan, S. P. & Funk, D. J. Heterogeneous genomic differentiation between walking-stick ecotypes: “isolation by adaptation” and multiple roles for divergent selection. Evolution 62, 316–336 (2008).

    Article  PubMed  Google Scholar 

  103. Campbell, D. & Bernatchez, L. 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 (2004).

    Article  CAS  PubMed  Google Scholar 

  104. Excoffier, L., Hofer, T. & Foll, M. Detecting loci under selection in a hierarchically structured population. Heredity 103, 285–298 (2009).

    Article  CAS  PubMed  Google Scholar 

  105. Gagnaire, P.-A., Normandeau, E., Pavey, S. A. & Bernatchez, L. Mapping phenotypic, expression and transmission ratio distortion QTL using RAD markers in the Lake Whitefish (Coregonus clupeaformis). Mol. Ecol. 22, 3036–3048 (2013).

    Article  CAS  PubMed  Google Scholar 

  106. Nosil, P., Parchman, T. L., Feder, J. L. & Gompert, Z. Do highly divergent loci reside in genomic regions affecting reproductive isolation? A test using next-generation sequence data in Timema stick insects. BMC Evol. Biol. 12, 164 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  107. Lindtke, D., González-Martínez, S. C., Macaya-Sanz, D. & Lexer, C. Admixture mapping of quantitative traits in Populus hybrid zones: power and limitations. Heredity 111, 474–485 (2013). This is one of the first studies to use admixture mapping in a natural hybrid population to examine the genetic basis of traits that contribute to reproductive isolation. Application of this powerful approach is likely to make important contributions to speciation research.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Malek, T. B., Boughman, J. W., Dworkin, I. & Peichel, C. L. Admixture mapping of male nuptial colour and body shape in a recently formed hybrid population of threespine stickleback. Mol. Ecol. 21, 5265–5279 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  109. Schluter, D. & Conte, G. L. Genetics and ecological speciation. Proc. Natl Acad. Sci. USA 106, 9955–9962 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  110. Seehausen, O. et al. Speciation through sensory drive in cichlid fish. Nature 455, 620–626 (2008). This study shows how divergent female preferences that initially have an ecological basis can impose selection on male signal traits and generate reproductive isolation in the face of gene flow given the right balance between intensity of selection and distribution of habitats.

    Article  CAS  PubMed  Google Scholar 

  111. Feder, J. L. et al. Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis. Proc. Natl Acad. Sci. USA 100, 10314–10319 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Nadeau, N. J. et al. Genome-wide patterns of divergence and gene flow across a butterfly radiation. Mol. Ecol. 22, 814–826 (2013).

    Article  CAS  PubMed  Google Scholar 

  113. Seehausen, O. Hybridization and adaptive radiation. Trends Ecol. Evol. 19, 198–207 (2004).

    Article  PubMed  Google Scholar 

  114. Smadja, C. M. & Butlin, R. K. A framework for comparing processes of speciation in the presence of gene flow. Mol. Ecol. 20, 5123–5140 (2011).

    Article  PubMed  Google Scholar 

  115. Bierne, N., Welch, J., Loire, E., Bonhomme, F. & David, P. The coupling hypothesis: why genome scans may fail to map local adaptation genes. Mol. Ecol. 20, 2044–2072 (2011).

    Article  PubMed  Google Scholar 

  116. Hermann, K. et al. Tight genetic linkage of prezygotic barrier loci creates a multifunctional speciation island in Petunia. Curr. Biol. 23, 873–877 (2013).

    Article  CAS  PubMed  Google Scholar 

  117. Bank, C., Burger, R. & Hermisson, J. The limits to parapatric speciation: Dobzhansky–Muller incompatibilities in a continent-island model. Genetics 191, 845–863 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  118. Wright, K. M., Lloyd, D., Lowry, D. B., Macnair, M. R. & Willis, J. H. Indirect evolution of hybrid lethality due to linkage with selected locus in Mimulus guttatus. PLoS Biol. 11, e1001497 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Barton, N. H. Multilocus clines. Evolution 37, 454–471 (1983).

    Article  CAS  PubMed  Google Scholar 

  120. Barton, N. H. & de Cara, M. A. The evolution of strong reproductive isolation. Evolution 63, 1171–1190 (2009). This theoretical paper considers the conditions under which selection can overcome recombination to bring together multiple reproductive barriers and therefore generate strong reproductive isolation.

    Article  PubMed  Google Scholar 

  121. Nosil, P., Harmon, L. J. & Seehausen, O. Ecological explanations for (incomplete) speciation. Trends Ecol. Evol. 24, 145–156 (2009).

    Article  PubMed  Google Scholar 

  122. Doebeli, M. & Dieckmann, U. Speciation along environmental gradients. Nature 421, 259–264 (2003).

    Article  CAS  PubMed  Google Scholar 

  123. Butlin, R. K. & Ritchie, M. G. Pulling together or pulling apart: hybridization in theory and practice. J. Evol. Biol. 26, 294–298 (2013).

    Article  CAS  PubMed  Google Scholar 

  124. Servedio, M. R. & Noor, M. A. F. The role of reinforcement in speciation: theory and data. Annu. Rev. Ecol. Evol. Systemat. 34, 339–364 (2003).

    Article  Google Scholar 

  125. Qvarnström, A. & Bailey, R. I. Speciation through evolution of sex-linked genes. Heredity 102, 4–15 (2009).

    Article  CAS  PubMed  Google Scholar 

  126. Pryke, S. R. & Griffith, S. C. Postzygotic genetic incompatibility between sympatric color morphs. Evolution 63, 793–798 (2009).

    Article  PubMed  Google Scholar 

  127. Pryke, S. R. Sex chromosome linkage of mate preference and color signal maintains assortative mating between interbreeding finch morphs. Evolution 64, 1301–1310 (2010).

    PubMed  Google Scholar 

  128. Kirkpatrick, M. & Barton, N. Chromosome inversions, local adaptation and speciation. Genetics 173, 419–434 (2006). This paper gives a thorough theoretical background and new insights into the role of chromosome inversions in adaptation and speciation.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Felsenstein, J. Skepticism towards Santa Rosalia, or why are there so few kinds of animals. Evolution 35, 124–138 (1981). This key paper introduces the antagonism between recombination and the build-up of linkage disequilibrium that lies at the heart of the speciation process.

    Article  PubMed  Google Scholar 

  130. Hopkins, R. & Rausher, M. D. Pollinator-mediated selection on flower color allele drives reinforcement. Science 335, 1090–1092 (2012).

    Article  CAS  PubMed  Google Scholar 

  131. Hopkins, R. & Rausher, M. D. Identification of two genes causing reinforcement in the Texas wildflower Phlox drummondii. Nature 469, 411–414 (2011).

    Article  CAS  PubMed  Google Scholar 

  132. Servedio, M. R., Van Doorn, G. S., Kopp, M., Frame, A. M. & Nosil, P. Magic traits in speciation: 'magic' but not rare? Trends Ecol. Evol. 26, 389–397 (2011).

    Article  PubMed  Google Scholar 

  133. Lowry, D. B. & Willis, J. H. A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation. PLoS Biol. 8, e1000500 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Joron, M. et al. Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 477, 203–206 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Noor, M. A. F., Grams, K. L., Bertucci, L. A. & Reiland, J. Chromosomal inversions and the reproductive isolation of species Proc. Natl Acad. Sci. USA 98, 12084–12088 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Shaw, K. L. & Lesnick, S. C. Genomic linkage of male song and female acoustic preference QTL underlying a rapid species radiation. Proc. Natl Acad. Sci. USA 106, 9737–9742 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  137. Merrill, R. M., Van Schooten, B., Scott, J. A. & Jiggins, C. D. Pervasive genetic associations between traits causing reproductive isolation in Heliconius butterflies. Proc. R. Soc. B 278, 511–518 (2011).

    Article  PubMed  Google Scholar 

  138. Saetre, G. P. & Saether, S. A. Ecology and genetics of speciation in Ficedula flycatchers. Mol. Ecol. 19, 1091–1106 (2010).

    Article  PubMed  Google Scholar 

  139. Bimova, B. V. et al. Reinforcement selection acting on the European house mouse hybrid zone. Mol. Ecol. 20, 2403–2424 (2011). Using powerful analyses of the exceptionally well-studied mouse hybrid zone, this paper provides clear evidence for the operation of reinforcement and also for the limits on its effectiveness in reducing gene flow.

    Article  PubMed  Google Scholar 

  140. Teeter, K. C. et al. The variable genomic architecture of isolation between hybridizing species of house mice. Evolution 64, 472–485 (2010).

    Article  CAS  PubMed  Google Scholar 

  141. Nielsen, R., Korneliussen, T., Albrechtsen, A., Li, Y. & Wang, J. SNP calling, genotype calling, and sample allele frequency estimation from new-generation sequencing data. PLoS ONE 7, e37558 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Orr, H. A. The genetics of species differences. Trends Ecol. Evol. 16, 343–350 (2001).

    Article  Google Scholar 

  143. Haller, B. C., De Leon, L. F., Rolshausen, G., Gotanda, K. M. & Hendry, A. P. Magic traits: distinguishing the important from the trivial. Trends Ecol. Evol. 27, 4–5 (2012).

    Article  PubMed  Google Scholar 

  144. Fisher, R. A. The Genetical Theory of Natural Selection (Clarendon Press, 1930).

    Book  Google Scholar 

  145. Orr, H. A. The population genetics of adaptation: The distribution of factors fixed during adaptive evolution. Evolution 52, 935–949 (1998).

    Article  PubMed  Google Scholar 

  146. Orr, H. A. The genetic theory of adaptation: a brief history. Nature Rev. Genet. 6, 119–127 (2005).

    Article  CAS  PubMed  Google Scholar 

  147. Rockman, M. V. The QTN program and the alleles that matter for evolution: all that's gold does not glitter. Evolution 66, 1–17 (2012).

    Article  PubMed  Google Scholar 

  148. Gordo, I. & Campos, P. R. Evolution of clonal populations approaching a fitness peak. Biol. Lett. 9, 20120239 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  149. Guillaume, F. & Whitlock, M. C. Effects of migration on the genetic covariance matrix. Evolution 61, 2398–2409 (2007).

    Article  PubMed  Google Scholar 

  150. Bomblies, K. & Weigel, D. Arabidopsis and relatives as models for the study of genetic and genomic incompatibilities. Phil. Trans. R. Soc. B 365, 1815–1823 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  151. Leary, G. P. et al. Single mutation to a sx pheromone receptor provides adaptive specificity between closely related moth species. Proc. Natl Acad. Sci. USA 109, 14081–14086 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  152. Bradshaw, H. D. & Schemske, D. W. Allele substitution at a flower colour locus produces a pollinator shift in monkey flowers. Nature 426, 176–178 (2003).

    Article  CAS  PubMed  Google Scholar 

  153. Feder, J. L. et al. Host fidelity is an effective premating barrier between sympatric races of the apple maggot fly. Proc. Natl Acad. Sci. USA 91, 7990–7994 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Klahre, U. et al. Pollinator choice in Petunia depends on two major genetic loci for floral scent production. Curr. Biol. 21, 730–739 (2011).

    Article  CAS  PubMed  Google Scholar 

  155. Dambroski, H. R. et al. The genetic basis for fruit odor discrimination in Rhagoletis flies and its significance for sympatric host shifts. Evolution 59, 1953–1964 (2005).

    Article  CAS  PubMed  Google Scholar 

  156. Haesler, M. P. & Seehausen, O. Inheritance of female mating preference in a sympatric sibling species pair of Lake Victoria cichlids: implications for speciation. Proc. R. Soc. B 272, 237–245 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  157. Fan, P. et al. Genetic and neural mechanisms that inhibit Drosophila from mating with other species. Cell 154, 89–102 (2013).

    Article  CAS  PubMed  Google Scholar 

  158. Ballerini, E. S. et al. QTL mapping reveals the genetic architecture of loci affecting pre- and post-zygotic isolating barriers in Louisiana Iris. BMC Plant Biol. 12, 91 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Reed, R. D. et al. optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science 333, 1137–1141 (2011).

    Article  CAS  PubMed  Google Scholar 

  160. Barrett, R. D. H., Rogers, S. M. & Schluter, D. Environment specific pleiotropy facilitates divergence at the Ectodysplasin locus in threespine stickleback. Evolution 63, 2831–2837 (2009).

    Article  PubMed  Google Scholar 

  161. Arnold, S. J., Burger, R., Hohenlohe, P. A., Ajie, B. C. & Jones, A. G. Understanding the evolution and stability of the G-matrix. Evolution 62, 2451–2461 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  162. Lande, R. Quantitative genetic-analysis of multivariate evolution, applied to brain — body size allometry. Evolution 33, 402–416 (1979).

    Article  PubMed  Google Scholar 

  163. Schluter, D. Adaptive radiation along genetic lines of least resistance. Evolution 50, 1766–1774 (1996). This key conceptual paper shows how the structure of genetic variances and covariances among quantitative traits can influence the direction of evolution and thus the progress of adaptive radiation.

    Article  PubMed  Google Scholar 

  164. Roff, D. The evolution of the G matrix: selection or drift? Heredity 84, 135–142 (2000).

    Article  PubMed  Google Scholar 

  165. Martin, G., Chapuis, E. & Goudet, J. Multivariate Qst–Fst comparisons: a neutrality test for the evolution of the G matrix in structured populations. Genetics 180, 2135–2149 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  166. Hansen, T. F. & Houle, D. Measuring and comparing evolvability and constraint in multivariate characters. J. Evol. Biol. 21, 1201–1219 (2008).

    Article  CAS  PubMed  Google Scholar 

  167. Chenoweth, S. F., Rundle, H. D. & Blows, M. W. The contribution of selection and genetic constraints to phenotypic divergence. Am. Naturalist 175, 186–196 (2010).

    Article  Google Scholar 

  168. Roff, D. A. & Fairbairn, D. J. A test of the hypothesis that correlational selection generates genetic correlations. Evolution 66, 2953–2960 (2012).

    Article  PubMed  Google Scholar 

  169. Jones, A. G., Arnold, S. J. & Bürger, R. Stability of the G-matrix in a population experiencing pleiotropic mutation, stabilizing selection, and genetic drift. Evolution 57, 1747–1760 (2003).

    Article  PubMed  Google Scholar 

  170. Agrawal, A. F., Brodie, E. D. & Rieseberg, L. H. Possible consequences of genes of major effect: transient changes in the G-matrix. Genetica 112, 33–43 (2001).

    Article  PubMed  Google Scholar 

  171. Jones, A. G., Arnold, S. J., Bürger, R., Hohenlohe, P. A. & Uyeda, J. C. The effects of stochastic and episodic movement of the optimum on the evolution of the G-matrix and the response of the trait mean to selection. J. Evol. Biol. 25, 2210–2231 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  172. Yang, J. et al. Genome partitioning of genetic variation for complex traits using common SNPs. Nature Genet. 43, 519–525 (2011).

    Article  CAS  PubMed  Google Scholar 

  173. Kopp, A. Metamodels and phylogenetic replication: a systematic approach to the evolution of developmental pathways. Evolution 63, 2771–2789 (2009).

    Article  PubMed  Google Scholar 

  174. Eroukhmanoff, F. & Svensson, E. I. Evolution and stability of the G-matrix during the colonization of a novel environment. J. Evol. Biol. 24, 1363–1373 (2011).

    Article  CAS  PubMed  Google Scholar 

  175. Nolte, A. W. & Tautz, D. Understanding the onset of hybrid speciation. Trends Genet. 26, 54–58 (2010).

    Article  CAS  PubMed  Google Scholar 

  176. Selz, O. M., Lucek, K., Young, K. A. & Seehausen, O. Relaxed trait covariance in interspecific cichlid hybrids predicts morphological diversity in adaptive radiations. J. Evol. Biol. 27, 11–24 (2014).

    Article  CAS  PubMed  Google Scholar 

  177. Macaya-Sanz, D. et al. Genetic analysis of post-mating reproductive barriers in hybridizing European Populus species. Heredity 107, 478–486 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Seehausen, O. Conditions when hybridization might predispose populations for adaptive radiation. J. Evol. Biol. 26, 279–281 (2013).

    Article  CAS  PubMed  Google Scholar 

  179. Bolnick, D. I. & Fitzpatrick, B. M. Sympatric speciation: models and empirical evidence. Annu. Rev. Ecol. Evol. Systemat. 38, 459–487 (2007).

    Article  Google Scholar 

  180. Papadopulos, A. S. T. et al. A comparative analysis of the mechanisms underlying speciation on Lord Howe Island. J. Evol. Biol. 26, 733–745 (2013).

    Article  CAS  PubMed  Google Scholar 

  181. Stern, D. L. & Orgogozo, V. The loci of evolution: how predictable is genetic evolution? Evolution 62, 2155–2177 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  182. Hoekstra, H. E. & Coyne, J. A. The locus of evolution: evo devo and the genetics of adaptation. Evolution 61, 995–1016 (2007).

    Article  PubMed  Google Scholar 

  183. Eriksson, A. & Manica, A. Effect of ancient population structure on the degree of polymorphism shared between modern human populations and ancient hominins. Proc. Natl Acad. Sci. USA 109, 13956–13960 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  184. Bazin, E., Dawson, K. J. & Beaumont, M. A. Likelihood-free inference of population structure and local adaptation in a Bayesian hierarchical model. Genetics 185, 587–602 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Lawson, D. J., Hellenthal, G., Myers, S. & Falush, D. Inference of population structure using dense haplotype data. PLoS Genet. 8, e1002453 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Slate, J. Quantitative trait locus mapping in natural populations: progress, caveats and future directions. Mol. Ecol. 14, 363–379 (2005).

    Article  CAS  PubMed  Google Scholar 

  187. Buerkle, C. A. & Lexer, C. Admixture as the basis for genetic mapping. Trends Ecol. Evol. 23, 686–694 (2008).

    Article  PubMed  Google Scholar 

  188. Gompert, Z. & Buerkle, C. A. Bayesian estimation of genomic clines. Mol. Ecol. 20, 2111–2127 (2011).

    Article  PubMed  Google Scholar 

  189. Trier, C. N., Hermansen, J. S., Sætre, G. P. & Bailey, R. I. Evidence for mito-nuclear and sex-linked incompatibilities between the hybrid Italian sparrow and its parent species. PLoS Genet. 10, e1004075 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  190. Barrett, R. D. H., Rogers, S. M. & Schluter, D. Natural selection on a major armor gene in threespine stickleback. Science 322, 255–257 (2008). This study showed unexpected complexity in the response to selection for alleles of the EDA locus, probably because of pleiotropic effects on other fitness-related traits. Such pleiotropic effects may be widespread and have major impacts on the progress of adaptation and speciation.

    Article  CAS  PubMed  Google Scholar 

  191. Cookson, W., Liang, L., Abecasis, G., Moffatt, M. & Lathrop, M. Mapping complex disease traits with global gene expression. Nature Rev. Genet. 10, 184–194 (2009).

    Article  CAS  PubMed  Google Scholar 

  192. Orr, H. A. The population-genetics of speciation — the evolution of hybrid incompatibilities. Genetics 139, 1805–1813 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  193. Vonlanthen, P. et al. Eutrophication causes speciation reversal in whitefish adaptive radiations. Nature 482, 357–362 (2012).

    Article  CAS  PubMed  Google Scholar 

  194. Rosenblum, E. B. et al. Goldilocks meets Santa Rosalia: an ephemeral speciation model explains patterns of diversification across time scales. Evol. Biol. 39, 255–261 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  195. Butlin, R. K., Bridle, J. R. & Schluter, D. Speciation and Patterns of Diversity (Cambridge Univ. Press, 2009).

    Book  Google Scholar 

  196. Sanderson, M. J. & Donoghue, M. J. Reconstructing shifts in diversification rates on phylogenetic trees. Trends Ecol. Evol. 11, 15–20 (1996).

    Article  CAS  PubMed  Google Scholar 

  197. Seehausen, O., van Alphen, J. J. M. & Witte, F. Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277, 1808–1811 (1997).

    Article  CAS  Google Scholar 

  198. Taylor, E. et al. Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Mol. Ecol. 15, 343–355 (2006).

    Article  CAS  PubMed  Google Scholar 

  199. Seehausen, O., Takimoto, G., Roy, D. & Jokela, J. Speciation reversal and biodiversity dynamics with hybridization in changing environments. Mol. Ecol. 17, 30–44 (2008).

    Article  PubMed  Google Scholar 

  200. Etges, W. J., de Oliveira, C. C., Noor, M. A. F. & Ritchie, M. G. Genetics of incipient speciation in Drosophila mojavensis. III. Life-history divergence in allopatry and reproductive isolation. Evolution 64, 3549–3569 (2010).

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank the European Science Foundation networking programme Frontiers in Speciation Research (FroSpects) for funding a workshop on Genetics and Genomics of Speciation and for contributing towards travel expenses for graduate students, and N. Pepe and L. Greuter for help with the organization of the workshop. They thank C. Lexer and two anonymous reviewers for suggestions that improved this Review.

Author information

Author notes

  1. Andrew D. Foote

    Present address: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, DK-1350 Copenhagen, Denmark. Present address: the Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, SE-752 36 Uppsala, Sweden.,

Authors and Affiliations

  1. Department of Fish Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, Kastanienbaum, 6047, Switzerland

    Ole Seehausen

  2. Division of Aquatic Ecology and Evolution, Institute of Ecology and Evolution, University of Bern, Bern, 3012, Switzerland

    Ole Seehausen

  3. Department of Animal and Plant Sciences, the University of Sheffield, Sheffield S10 2TN, UK,

    Roger K. Butlin

  4. and the Sven Lovén Centre — Tjärnö, University of Gothenburg, S-452 96 Strömstad, Sweden.,

    Roger K. Butlin

  5. Department of Fish Ecology and Evolution, Switzerland; the Division of Aquatic Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland; and the Institute of Integrative Biology, ETH Zürich, ETH Zentrum CHN, 8092 Zürich, Switzerland.,

    Irene Keller

  6. the Division of Aquatic Ecology and Evolution, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland,

    Irene Keller

  7. Department of Fish Ecology and Evolution, Switzerland; and the Division of Aquatic Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland.,

    Catherine E. Wagner

  8. and the Division of Aquatic Ecology and Evolution, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland.,

    Catherine E. Wagner

  9. Department of Fish Ecology and Evolution, Switzerland; and the Department of Zoology; Ecology, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Evolutionary Biology and Behavior Program; BEACON Center, Michigan State University, 203 Natural Sciences, East Lansing, Michigan 48824, USA.,

    Janette W. Boughman

  10. and the Department of Zoology,

    Janette W. Boughman

  11. Department of Biological Sciences, Institute of Bioinformatics and Evolutionary Studies, University of Idaho, Moscow, 83844–3051, Idaho, USA

    Paul A. Hohenlohe

  12. Division of Human Biology, Fred Hutchinson Cancer Research Center, Seattle, 98109, Washington, USA

    Catherine L. Peichel

  13. Department of Biosciences, Centre for Ecological and Evolutionary Synthesis, University of Oslo, PO BOX 1066, Blindern, Oslo, N-0316, Norway

    Glenn-Peter Saetre

  14. School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, Lausanne, 1015, Switzerland

    Claudia Bank

  15. Integrated Science Laboratory and the Department of Mathematics and Mathematical Statistics, Umeå University, Umeå, 90187, Sweden

    Åke Brännström

  16. Department of Ecology and Evolution, University of Lausanne, Lausanne, CH-1015, Switzerland

    Alan Brelsford

  17. Liverpool School of Tropical Medicine, Liverpool, L3 5QA, UK

    Chris S. Clarkson

  18. Department of Biosciences, Centre for Ecological and Evolutionary Synthesis, University of Oslo, PO BOX 1066, Blindern, Oslo, N-0316, Norway

    Fabrice Eroukhmanoff

  19. Department of Biological Sciences, University of Notre Dame, Notre Dame, 46556–0369, Indiana, USA

    Jeffrey L. Feder

  20. Institute of Integrative Biology, ETH Zürich, ETH Zentrum CHN, Zürich, 8092, Switzerland

    Martin C. Fischer

  21. Department of Biology, Lehrstuhl für Zoologie und Evolutionsbiologie, University of Konstanz, Konstanz, 78457, Germany

    Paolo Franchini

  22. Department of Zoology, University of Cambridge, Cambridge, CB2 3EJ, UK

    Chris D. Jiggins

  23. Friedrich Miescher Laboratory of the Max Planck Society, Tübingen, 72076, Germany

    Felicity C. Jones

  24. Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, CH-8057, Switzerland

    Anna K. Lindholm

  25. Department of Fish Ecology and Evolution, Switzerland; and the Division of Aquatic Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland.,

    Kay Lucek

  26. and the Division of Aquatic Ecology and Evolution, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland.,

    Kay Lucek

  27. Behavioural Biology Group, Centre for Behaviour and Neurosciences, University of Groningen, PO BOX 11103, Groningen, 9700 CC, The Netherlands

    Martine E. Maan

  28. Department of Fish Ecology and Evolution, Switzerland; the Division of Aquatic Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, and the Computational and Molecular Population Genetics Laboratory, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland.,

    David A. Marques

  29. the Division of Aquatic Ecology and Evolution, and the Computational and Molecular Population Genetics Laboratory, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland.,

    David A. Marques

  30. Department of Zoology, University of Cambridge, Cambridge, CB2 3EJ, UK

    Simon H. Martin

  31. Department of Aquatic Ecology, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, Kastanienbaum, 6047, Switzerland

    Blake Matthews

  32. Department of Fish Ecology and Evolution, Switzerland; the Division of Aquatic Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, and the Computational and Molecular Population Genetics Laboratory, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland.,

    Joana I. Meier

  33. the Division of Aquatic Ecology and Evolution, and the Computational and Molecular Population Genetics Laboratory, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland.,

    Joana I. Meier

  34. Department of Zoology, UK; and the Department of Aquatic Ecology, University of Cambridge, Cambridge CB2 3EJ, Eawag: Swiss Federal Institute of Aquatic Science and Technology, 8600 Dübendorf, Switzerland.,

    Markus Möst

  35. and the Department of Aquatic Ecology, Eawag: Swiss Federal Institute of Aquatic Science and Technology, 8600 Dübendorf, Switzerland.,

    Markus Möst

  36. Museum of Vertebrate Zoology and Department of Integrative Biology, University of California, Berkeley, 94720–3160, California, USA

    Michael W. Nachman

  37. Integrated Science Laboratory and Department of Ecology and Environmental Science, Umeå University, Umeå, 90187, Sweden

    Etsuko Nonaka

  38. Department of Zoology, University of British Columbia, Vancouver, V6T 1Z4, British Columbia, Canada

    Diana J. Rennison

  39. Department of Fish Ecology and Evolution, Switzerland; the Division of Aquatic Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland; and Zoologisches Forschungsmuseum Alexander Koenig, 53113 Bonn, Germany.,

    Julia Schwarzer

  40. the Division of Aquatic Ecology and Evolution, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland,

    Julia Schwarzer

  41. Department of Biology, The University of Texas at Arlington, 76010–0498, Texas, USA

    Eric T. Watson

  42. Department of Animal and Plant Sciences, the University of Sheffield, Sheffield, S10 2TN, UK

    Anja M. Westram

  43. Institute of Integrative Biology, ETH Zürich, ETH Zentrum CHN, Zürich, 8092, Switzerland

    Alex Widmer

Authors
  1. Ole Seehausen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roger K. Butlin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Irene Keller
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Catherine E. Wagner
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Janette W. Boughman
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Paul A. Hohenlohe
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Catherine L. Peichel
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Glenn-Peter Saetre
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Claudia Bank
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Åke Brännström
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Alan Brelsford
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Chris S. Clarkson
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Fabrice Eroukhmanoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Jeffrey L. Feder
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Martin C. Fischer
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Andrew D. Foote
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Paolo Franchini
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Chris D. Jiggins
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Felicity C. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Anna K. Lindholm
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Kay Lucek
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. Martine E. Maan
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. David A. Marques
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. Simon H. Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  25. Blake Matthews
    View author publications

    You can also search for this author in PubMed Google Scholar

  26. Joana I. Meier
    View author publications

    You can also search for this author in PubMed Google Scholar

  27. Markus Möst
    View author publications

    You can also search for this author in PubMed Google Scholar

  28. Michael W. Nachman
    View author publications

    You can also search for this author in PubMed Google Scholar

  29. Etsuko Nonaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  30. Diana J. Rennison
    View author publications

    You can also search for this author in PubMed Google Scholar

  31. Julia Schwarzer
    View author publications

    You can also search for this author in PubMed Google Scholar

  32. Eric T. Watson
    View author publications

    You can also search for this author in PubMed Google Scholar

  33. Anja M. Westram
    View author publications

    You can also search for this author in PubMed Google Scholar

  34. Alex Widmer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ole Seehausen.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

PowerPoint slides

Glossary

Reproductive isolation

The absence or restriction of gene flow between populations beyond that caused by spatial separation.

Gene flow

The movement of alleles between populations. For gene flow to occur, individuals must disperse between populations and successfully reproduce with local individuals. Therefore, gene flow can be reduced not only by dispersal barriers but also by either intrinsic or extrinsic reproductive isolation.

Speciation genomics

The field of speciation research that addresses the influence of genomic properties on the evolution of reproductive barriers and the signatures of speciation processes that are observable in genomic patterns (for example, processes of diversity and divergence). Its aim is a conceptual and methodological integration of genomic approaches with other empirical and theoretical speciation research.

Effect sizes

The magnitude of the influence of a locus or a specific allele on a phenotypic trait. This can be expressed, for example, as the proportion of phenotypic variation due to a specific locus or as the phenotypic difference between genotypes with and without a specific allele.

Pleiotropy

Effect of an allele on more than one trait.

Divergent selection

Selection that favours different phenotypes in different populations.

Extrinsic reproductive isolation

Fitness reduction in hybrids that is dependent on the environment and that is mediated by genotype–environment interactions.

Genomic conflict

Conflict that arises between genes or genetic elements within the same genome either when they are not transmitted by the same rules (for example, biparental versus uniparental inheritance) or when a gene causes its own transmission to the detriment of the rest of the genome. The presence of elements that bias transmission (that is, distorter loci) is expected to lead to the evolution of loci that restore Mendelian segregation (that is, restorer loci).

Intrinsic reproductive isolation

Fitness reduction in hybrids that is independent of the environment.

Ecological speciation

The evolution of reproductive isolation as a consequence of divergent or disruptive natural selection between populations that inhabit different environments or exploit different resources.

Postzygotic isolation

Effects of barriers that act after fertilization, such as hybrid sterility and hybrid inviability. It can be either extrinsic (that is, mediated by the environment) or intrinsic.

Disruptive selection

Selection within a single population that favours extreme phenotypes over intermediate phenotypes.

Sexual isolation

Reproductive isolation due to reduced mating between members of divergent populations, including behavioural assortative mate choice and assortative fertilization in animals, as well as pollinator-mediated assortative mating in plants. It is most often thought of as prezygotic but can also be postzygotic if there is disruptive sexual selection.

FST-outlier analyses

The comparison of the distribution of FST values across loci with the distribution expected in the absence of divergent selection for the same average differentiation. A locus with an FST value that exceeds expectation is likely to be influenced by divergent selection, either on the locus itself or on a linked locus.

Prezygotic isolation

Effect of barriers that act before or after mating but before fertilization, including the isolating effects of divergent mate choice, habitat preference, reproductive timing and gametic incompatibility.

Bateson–Dobzhansky–Muller incompatibilities

(BDMI). Intrinsic postmating barriers that are the result of epistatic interactions between alleles at two or more loci that reduce fitness in hybrids but not in the parental populations.

Underdominance

Heterozygotic inferiority; that is, the phenotype expressed in heterozygotes has lower fitness than that of either homozygote. This can cause disruptive selection.

Meiotic drivers

Factors that distort Mendelian segregation. At a heterozygous site, the driving variant will be found in more than half of the gametes.

Sexual conflict

The evolution of phenotypic characteristics by sexual selection when the trait confers a fitness benefit on one sex but a fitness cost on the other.

Hybridization

Mating between individuals that belong to distinct species or populations. If postmating isolation is incomplete, hybridization leads to the introgression of genes from one population to another.

Linkage disequilibrium

The statistical association of the alleles at two loci within gametes in a population. Although linkage disequilibrium tends to be greater between linked loci, it can also arise between physically unlinked loci (for example, because of selection, nonrandom mating or gene flow).

Distorter loci

Loci that underlie meiotic drive, which is the non-Mendelian segregation of alleles in meiosis. Distorter loci may act on other loci, so-called responder loci.

Responder loci

Loci that show deviations from Mendelian segregation (that is, meiotic drive) owing to the effect of distorter loci.

Speciation continuum

Variation of the strength of reproductive isolation between two incipient species either in different locations or in different species pairs that belong to the same evolutionary lineage and that diverge in similar ways.

Genome scan

Comparison of genome-wide patterns of diversity within populations and/or divergence between populations at hundreds or thousands of markers. Until recently, most studies used amplified fragment length polymorphisms (AFLPs) but this has recently changed, and single-nucleotide polymorphisms (SNPs) generated by next-generation sequencing or SNP chips are being used.

Divergence hitchhiking

When divergent selection on a locus reduces the effective migration rate for physically linked regions, which increases the opportunity for divergence at loci under weaker selection in the surrounding regions. Regions of divergence hitchhiking may remain much larger than those of traditional hitchhiking after a selective sweep within populations because of the persistent reduction in the ability of flanking regions to recombine away from a divergently selected gene.

Parapatric

Pertaining to organisms, populations or species that inhabit either adjacent geographical regions or spatially distinct but adjacent habitats and that may exchange genes.

Sympatric

Pertaining to organisms, populations or species that share the same geographical region and that overlap in their use of space with no spatial barriers to gene exchange.

F ST

(Also known as Wright's fixation index). A measure of population subdivision that compares the correlation between two gene copies that are randomly drawn from the same population to that between two gene copies that are drawn from two different populations. An FST of 1 indicates that two populations are fixed for alternative alleles.

Allopatric

Pertaining to organisms, populations or species that inhabit distinct geographical regions and are therefore not exchanging genes.

Coalescence

The merging of two genetic lineages in a common ancestor.

Incomplete lineage sorting

The situation in which some alleles share a more recent common ancestor with alleles in another species than with other alleles in the same species.

Sweeps

Increases in frequencies of alleles and closely linked chromosomal segments due to positive selection. Sweeps initially reduce variation and subsequently lead to a local excess of rare alleles as new unique mutations accumulate.

D xy

The average number of nucleotide substitutions per site between two populations.

Secondary contact

The meeting of the distribution ranges of two distinct populations or species after a period of evolutionary divergence in geographical isolation (that is, allopatry).

Gene-flow–selection balance

A level of differentiation between subpopulations at which the homogenizing effect of gene flow and the differentiating effect of divergent selection are in equilibrium.

Multifarious

Pertaining to divergent selection that acts on multiple traits.

Cline

Directional variation in phenotype or genotype, or change in frequency (for example, of an allele) across a geographical region.

Coalescent

A statistical framework for the analysis of genetic data, in which the alleles that are shared by populations or species are traced back in time to their most recent common ancestor.

Quantitative trait locus

(QTL). A chromosomal region that has a significant effect on a phenotype.

Admixture mapping

The identification of genetic loci that contribute to phenotypic differences between ancestral populations by investigating genotype–phenotype correlations in a population of mixed ancestry.

Standing genetic variation

Allelic variation that is currently segregating within a population, as opposed to alleles that arise through new mutation events.

Introgressive hybridization

The introduction of genes from one population or species into another through hybridization.

Fixation

The situation in which a mutation or a variant has achieved a frequency of 100% in a population.

Ecotone

A zone in which there is a transition between two distinct biological communities, for example, between forest and grassland or between aquatic and terrestrial habitats. It is typically associated with changes in the physical environment.

Reinforcement

Selection for the strengthening of prezygotic barriers to avoid the production of unfit hybrids between taxa that have previously evolved some postzygotic isolation.

One-allele mechanisms

Mechanisms that produce reproductive barriers through the spread of the same allele in each of two diverging populations, such as alleles for behavioural imprinting or reduced migration.

Two-allele mechanisms

Mechanisms that produce reproductive barriers through the spread of different alleles at the same locus in two diverging populations, such as alleles for different habitat or mating preferences.

Hybrid zones

Spatially restricted regions where the distribution ranges of distinct populations or incipient species come into contact and where hybrids are formed.

G-matrix

The additive genetic variance–covariance matrix that summarizes the variance within and the covariance between multiple phenotypic traits.

Correlational selection

Selection for optimal combinations of characteristics.

Transgressive phenotypes

Phenotypes in hybrids that exceed the range of phenotypes that are observed in the parental taxa.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Seehausen, O., Butlin, R., Keller, I. et al. Genomics and the origin of species. Nat Rev Genet 15, 176–192 (2014). https://doi.org/10.1038/nrg3644

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrg3644

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing