Article series: Study designs

Making sense of genomic islands of differentiation in light of speciation

Journal name:
Nature Reviews Genetics
Volume:
18,
Pages:
87–100
Year published:
DOI:
doi:10.1038/nrg.2016.133
Published online

Abstract

As populations diverge, genetic differences accumulate across the genome. Spurred by rapid developments in sequencing technology, genome-wide population surveys of natural populations promise insights into the evolutionary processes and the genetic basis underlying speciation. Although genomic regions of elevated differentiation are the focus of searches for 'speciation genes', there is an increasing realization that such genomic signatures can also arise by alternative processes that are not related to population divergence, such as linked selection. In this Review, we explore methodological trends in speciation genomic studies, highlight the difficulty in separating processes related to speciation from those emerging from genome-wide properties that are not related to reproductive isolation, and provide a set of suggestions for future work in this area.

At a glance

Figures

  1. A schematic of alternative processes that generate regional genomic islands of elevated differentiation.
    Figure 1: A schematic of alternative processes that generate regional genomic islands of elevated differentiation.

    Red and white circles represent different alleles in a population at the depicted genomic region. The branching schematic indicates the segregation of these alleles between populations that are diverging. a | In regions of gene flow (indicated by the double-headed arrows), differentiation becomes reduced relative to loci where there is selection against gene flow because of reproductive incompatibility, for example. b | In regions where the effective population size (Ne) is reduced by processes that are independent from gene flow (middle panel) the rate of lineage sorting is enhanced relative to background levels, leading to elevated differentiation.

  2. A summary of central aspects of our literature survey on speciation genomic studies.
    Figure 2: A summary of central aspects of our literature survey on speciation genomic studies.

    The figure shows the percentage of studies in our data set that included central aspects of speciation genomic analyses.

References

  1. Darwin, C. & Wallace, A. On the tendency of species to form varieties; and on the perpetuation of varieties and species by natural means of selection. J. Proc. Linn. Soc. Zool. 3, 4562 (1858).
  2. Dobzhansky, T. G. Genetics and the Origin of Species (Columbia Univ. Press, 1937).
  3. Mayr, E. & Provine, W. B. The Evolutionary Synthesis: Perspectives on the Unification of Biology (Harvard Univ. Press, 1998).
  4. Coyne, J. A. & Orr, H. A. Speciation (Sinauer Associates, 2004).
  5. Presgraves, D. C. The molecular evolutionary basis of species formation. Nat. Rev. Genet. 11, 175180 (2010).
  6. Mackay, T. F. C. et al. The Drosophila melanogaster genetic reference panel. Nature 482, 173178 (2012).
  7. Wolf, J. B. W., Lindell, J. & Backstrom, N. Speciation genetics: current status and evolving approaches. Phil. Trans. R. Soc. B Biol. Sci. 365, 17171733 (2010).
  8. Seehausen, O. et al. Genomics and the origin of species. Nat. Rev. Genet. 15, 176192 (2014).
    This Review resulted from a workshop and discusses genomic approaches in speciation at an advanced level.
  9. Foote, A. et al. Genome-culture coevolution promotes rapid divergence in the killer whale. Nat. Commun. 7, 11693 (2016).
  10. Nadachowska-Brzyska, K., Burri, R., Smeds, L. & Ellegren, H. PSMC analysis of effective population sizes in molecular ecology and its application to black-and-white Ficedula flycatchers. Mol. Ecol. 25, 10581072 (2016).
  11. Lawrie, D. S. & Petrov, D. A. Comparative population genomics: power and principles for the inference of functionality. Trends Genet. 30, 133139 (2014).
  12. Comeron, J. M., Ratnappan, R. & Bailin, S. The many landscapes of recombination in Drosophila melanogaster. PLoS Genet. 8, e1002905 (2012).
  13. Singhal, S. et al. Stable recombination hotspots in birds. Science 350, 928932 (2015).
  14. Mugal, C. F., Weber, C. C. & Ellegren, H. GC-biased gene conversion links the recombination landscape and demography to genomic base composition. BioEssays 37, 13171326 (2015).
  15. Romiguier, J. et al. Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature 515, 261263 (2014).
  16. Corbett-Detig, R. B., Hartl, D. L. & Sackton, T. B. Natural selection constrains neutral diversity across a wide range of species. PLoS Biol. 13, e1002112 (2015).
  17. 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, 439444 (2009).
  18. Cutter, A. D. & Payseur, B. A. Genomic signatures of selection at linked sites: unifying the disparity among species. Nat. Rev. Genet. 14, 262274 (2013).
  19. Cruickshank, T. E. & Hahn, M. W. Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol. Ecol. 23, 31333157 (2014).
    This paper provides a good introduction to the processes by which genetic differentiation can be locally elevated.
  20. Haasl, R. J. & Payseur, B. A. Fifteen years of genomewide scans for selection: trends, lessons and unaddressed genetic sources of complication. Mol. Ecol. 25, 523 (2016).
  21. Wu, C. I. The genic view of the process of speciation. J. Evol. Biol. 14, 851865 (2001).
    This influential paper provides a conceptual link between (Darwinian) selection acting on single loci and Mayr's concept of cohesive, genome-wide reproductive isolation under the biological speciation concept.
  22. Feder, J. L., Egan, S. P. & Nosil, P. The genomics of speciation-with-gene-flow. Trends Genet. 28, 342350 (2012).
  23. Nosil, P. & Feder, J. L. Genome evolution and speciation: toward quantitative descriptions of pattern and process. Evolution 67, 24612467 (2013).
  24. Barton, N. & Bengtsson, B. O. The barrier to genetic exchange between hybridising populations. Heredity 57, 357376 (1986).
  25. McDermott, S. R. & Noor, M. A. F. The role of meiotic drive in hybrid male sterility. Phil. Trans. R. Soc. B 365, 12651272 (2010).
  26. Zanders, S. E. et al. Genome rearrangements and pervasive meiotic drive cause hybrid infertility in fission yeast. eLife 3, e02630 (2014).
  27. Harr, B. Genomic islands of differentiation between house mouse subspecies. Genome Res. 16, 730737 (2006).
  28. Turner, T. L., Hahn, M. W. & Nuzhdin, S. V. Genomic islands of speciation in Anopheles gambiae. PLoS Biol. 3, 15721578 (2005).
    This influential paper was the first to interpret islands of differentiation as 'speciation islands'.
  29. Pennisi, E. Disputed islands. Science 345, 611613 (2014).
    This editorial piece provides a historical perspective on the interpretation of genomic regions with elevated differentiation and includes illustrative examples.
  30. Yeaman, S. Genomic rearrangements and the evolution of clusters of locally adaptive loci. Proc. Natl Acad. Sci. USA 110, E1743E1751 (2013).
  31. Feder, J. L., Flaxman, S. M., Egan, S. P., Comeault, A. A. & Nosil, P. Geographic mode of speciation and genomic divergence. Annu. Rev. Ecol. Evol. Syst. 44, 7397 (2013).
  32. Ellegren, H. et al. The genomic landscape of species divergence in Ficedula flycatchers. Nature 491, 756760 (2012).
    This is one of the first genome-wide re-sequencing studies to demonstrate marked heterogeneity in the level of differentiation with few clear peaks per chromosome.
  33. Renaut, S. et al. Genomic islands of divergence are not affected by geography of speciation in sunflowers. Nat. Commun. 4, 1827 (2013).
    This study provides an important empirical demonstration that genomic islands of elevated differentiation emerge between populations in a similar way across a variety of geographical contexts that differ in the presumed amount of gene flow.
  34. Martin, S. H. et al. Genome-wide evidence for speciation with gene flow in Heliconius butterflies. Genome Res. 23, 18171828 (2013).
    This study quantifies the level of gene flow during species divergence.
  35. Poelstra, J. W. et al. The genomic landscape underlying phenotypic integrity in the face of gene flow in crows. Science 344, 14101414 (2014).
    This empirical study provides evidence for highly localized genomic selection against introgression and includes functional analyses.
  36. Soria-Carrasco, V. et al. Stick insect genomes reveal natural selection's role in parallel speciation. Science 344, 738742 (2014).
  37. Marques, D. A. et al. Genomics of rapid incipient speciation in sympatric threespine stickleback. PLoS Genet. 12, e1005887 (2016).
  38. Via, S. Divergence hitchhiking and the spread of genomic isolation during ecological speciation-with-gene-flow. Phil. Trans. R. Soc. B 367, 451460 (2012).
  39. 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, 409421 (2012).
    This empirical study has a solid conceptual introduction and highlights the importance of linked selection in genomic regions of low recombination.
  40. Smith, J. M. & Haigh, J. The hitch-hiking effect of a favourable gene. Genet. Res. 23, 2335 (1974).
  41. Gillespie, J. H. Genetic drift in an infinite population: the pseudohitchhiking model. Genetics 155, 909919 (2000).
  42. Charlesworth, B., Morgan, M. T. & Charlesworth, D. The effect of deleterious mutations on neutral molecular variation. Genetics 134, 12891303 (1993).
  43. Charlesworth, B. Background selection 20 years on: the Wilhelmine E. Key 2012 invitational lecture. J. Hered. 104, 161171 (2013).
  44. Stukenbrock, E. H. in Advances in Botanical Research (ed. Martin, F.) 70, 397423 (Academic Press, 2014).
  45. Dettman, J. R., Sirjusingh, C., Kohn, L. M. & Anderson, J. B. Incipient speciation by divergent adaptation and antagonistic epistasis in yeast. Nature 447, 585588 (2007).
  46. Shaw, K. L. & Mullen, S. P. Speciation continuum. J. Hered. 105, 741742 (2014).
  47. Burri, R. et al. Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers. Genome Res. 25, 16561665 (2015).
  48. Andrew, R. L. & Rieseberg, L. H. Divergence is focused on few genomic regions early in speciation: incipient speciation of sunflower ecotypes. Evolution 67, 24682482 (2013).
  49. Vijay, N. et al. Evolution of heterogeneous genome differentiation across multiple contact zones in a crow species complex. Nat. Commun. (in the press).
  50. Feulner, P. G. D. et al. Genomics of divergence along a continuum of parapatric population differentiation. PLoS Genet. 11, e1004966 (2015).
  51. Malinsky, M. et al. Genomic islands of speciation separate cichlid ecomorphs in an East African crater lake. Science 350, 14931498 (2015).
  52. Via, S. & West, J. The genetic mosaic suggests a new role for hitchhiking in ecological speciation. Mol. Ecol. 17, 43344345 (2008).
  53. Via, S. Natural selection in action during speciation. Proc. Natl Acad. Sci. USA 106, 99399946 (2009).
  54. Nadeau, N. J. et al. Genome-wide patterns of divergence and gene flow across a butterfly radiation. Mol. Ecol. 22, 814826 (2013).
    This empirical study demonstrates the power of study design in the interpretation of outlier genomic regions.
  55. Kronforst, M. R. et al. Hybridization reveals the evolving genomic architecture of speciation. Cell Rep. 5, 666677 (2013).
  56. Nadeau, N. J. et al. Population genomics of parallel hybrid zones in the mimetic butterflies. H. melpomene and H. erato. Genome Res. 24, 13161333 (2014).
  57. Chan, Y. F. et al. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327, 302305 (2009).
  58. Jones, F. C. et al. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484, 5561 (2012).
  59. Roesti, M., Kueng, B., Moser, D. & Berner, D. The genomics of ecological vicariance in threespine stickleback fish. Nat. Commun. 6, 8767 (2015).
  60. Savolainen, O., Lascoux, M. & Merilä, J. Ecological genomics of local adaptation. Nat. Rev. Genet. 14, 807820 (2013).
  61. Mossman, J. A., Biancani, L. M. & Rand, D. M. Mitonuclear epistasis for development time and its modification by diet in Drosophila. Genetics 203, 463484 (2016).
  62. Slatkin, M. Inbreeding coefficients and coalescence times. Genet. Res. 58, 167175 (1991).
  63. Kulathinal, R. J., Stevison, L. S. & Noor, M. A. F. The genomics of speciation in Drosophila: diversity, divergence, and introgression estimated using low-coverage genome sequencing. PLoS Genet. 5, e1000550 (2009).
  64. McGaugh, S. E. & Noor, M. A. F. Genomic impacts of chromosomal inversions in parapatric Drosophila species. Phil. Trans. R. Soc. B 367, 422429 (2012).
  65. Shafer, A. B. A. & Wolf, J. B. W. Widespread evidence for incipient ecological speciation: a meta-analysis of isolation-by-ecology. Ecol. Lett. 16, 940950 (2013).
  66. Shafer, A. B. A., Northrup, J. M., Wikelski, M., Wittemyer, G. & Wolf, J. B. W. Forecasting ecological genomics: high-tech animal instrumentation meets high-throughput sequencing. PLoS Biol. 14, e1002350 (2016).
  67. Payseur, B. A. & Rieseberg, L. H. A genomic perspective on hybridization and speciation. Mol. Ecol. 25, 23372360 (2016).
  68. Hein, J., Schierup, M. H. & Wiuf, C. Gene Genealogies, Variation and Evolution: a Primer in Coalescent Theory (Oxford Univ. Press, 2005).
  69. Gattepaille, L. M., Jakobsson, M. & Blum, M. G. Inferring population size changes with sequence and SNP data: lessons from human bottlenecks. Heredity 110, 409419 (2013).
  70. Pool, J. E. & Nielsen, R. Population size changes reshape genomic patterns of diversity. Evolution 61, 30013006 (2007).
  71. Smeds, L. et al. Evolutionary analysis of the female-specific avian W chromosome. Nat. Commun. 6, 7330 (2015).
  72. Presgraves, D. C. Sex chromosomes and speciation in Drosophila. Trends Genet. 24, 336343 (2008).
  73. Qvarnström, A. & Bailey, R. I. Speciation through evolution of sex-linked genes. Heredity 102, 415 (2009).
  74. Bank, C., Ewing, G. B., Ferrer-Admettla, A., Foll, M. & Jensen, J. D. Thinking too positive? Revisiting current methods of population genetic selection inference. Trends Genet. 30, 540546 (2014).
  75. Schiffels, S. & Durbin, R. Inferring human population size and separation history from multiple genome sequences. Nat. Genet. 46, 919925 (2014).
  76. Liu, X. & Fu, Y.-X. Exploring population size changes using SNP frequency spectra. Nat. Genet. 47, 555559 (2015).
  77. The Heliconius Genome Consortium. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487, 9498 (2012).
  78. Gompert, Z. et al. Experimental evidence for ecological selection on genome variation in the wild. Ecol. Lett. 17, 369379 (2014).
  79. Chaisson, M. J. P., Wilson, R. K. & Eichler, E. E. Genetic variation and the de novo assembly of human genomes. Nat. Rev. Genet. 16, 627640 (2015).
  80. Schlötterer, C., Tobler, R., Kofler, R. & Nolte, V. Sequencing pools of individuals — mining genome-wide polymorphism data without big funding. Nat. Rev. Genet. 15, 749763 (2014).
  81. Bed'hom, B. et al. The lavender plumage colour in Japanese quail is associated with a complex mutation in the region of MLPH that is related to differences in growth, feed consumption and body temperature. BMC Genomics 13, 442 (2012).
  82. Avelar, A. T., Perfeito, L., Gordo, I. & Ferreira, M. G. Genome architecture is a selectable trait that can be maintained by antagonistic pleiotropy. Nat. Commun. 4, 2235 (2013).
  83. Schwander, T., Libbrecht, R. & Keller, L. Supergenes and complex phenotypes. Curr. Biol. 24, R288R294 (2014).
  84. Küpper, C. et al. A supergene determines highly divergent male reproductive morphs in the ruff. Nat. Genet. 48, 7983 (2016).
  85. Lamichhaney, S. et al. Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax). Nat. Genet. 48, 8488 (2016).
  86. Kirubakaran, T. G. et al. Two adjacent inversions maintain genomic differentiation between migratory and stationary ecotypes of Atlantic cod. Mol. Ecol. 25, 21302143 (2016).
  87. Saenko, S. V. et al. Amelanism in the corn snake is associated with the insertion of an LTR-retrotransposon in the OCA2 gene. Sci. Rep. 5, 17118 (2015).
  88. Hoffmann, A. A. & Rieseberg, L. H. Revisiting the impact of inversions in evolution: from population genetic markers to drivers of adaptive shifts and speciation? Annu. Rev. Ecol. Evol. Syst. 39, 2142 (2008).
  89. Rieseberg, L. H. Chromosomal rearrangements and speciation. Trends Ecol. Evol. 16, 351358 (2001).
  90. Kirkpatrick, M. & Barton, N. Chromosome inversions, local adaptation and speciation. Genetics 173, 419434 (2006).
  91. Faria, R. & Navarro, A. Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol. Evol. 25, 660669 (2010).
  92. Navarro, A. & Barton, N. H. Chromosomal speciation and molecular divergence-accelerated evolution in rearranged chromosomes. Science 300, 321324 (2003).
  93. Lohse, K., Clarke, M., Ritchie, M. G. & Etges, W. J. Genome-wide tests for introgression between cactophilic Drosophila implicate a role of inversions during speciation. Evolution 69, 11781190 (2015).
  94. Huang, Y., Wright, S. I. & Agrawal, A. F. Genome-wide patterns of genetic variation within and among alternative selective regimes. PLoS Genet. 10, e1004527 (2014).
  95. Tuttle, E. M. et al. Divergence and functional degradation of a sex chromosome-like supergene. Curr. Biol. 26, 344350 (2016).
  96. Guerrero, R. F., Rousset, F. & Kirkpatrick, M. Coalescent patterns for chromosomal inversions in divergent populations. Phil. Trans. R. Soc. B Biol. Sci. 367, 430438 (2012).
  97. Feder, J. L., Nosil, P. & Flaxman, S. M. Assessing when chromosomal rearrangements affect the dynamics of speciation: implications from computer simulations. Front. Genet. 5, 295 (2014).
  98. Gordon, D. et al. Long-read sequence assembly of the gorilla genome. Science 352, aae0344 (2016).
  99. Felsenstein, J. Skepticism towards Santa Rosalia, or why are there so few kinds of animals. Evolution 35, 124138 (1981).
    This seminal paper illustrates the antagonism between selection and recombination for coupling loci that convey reproductive isolation in a two-allele model with gene flow.
  100. Auton, A. et al. A fine-scale chimpanzee genetic map from population sequencing. Science 336, 193198 (2012).
  101. Gossmann, T. I., Woolfit, M. & Eyre-Walker, A. Quantifying the variation in the effective population size within a genome. Genetics 189, 13891402 (2011).
  102. Charlesworth, B. Measures of divergence between populations and the effect of forces that reduce variability. Mol. Biol. Evol. 15, 538543 (1998).
  103. Roesti, M., Moser, D. & Berner, D. Recombination in the threespine stickleback genome — patterns and consequences. Mol. Ecol. 22, 30143027 (2013).
    This empirical study highlights the dependence of allele frequency shifts between populations on the genome-wide distribution of broad-scale recombination rates and chromosomal features such as centromeres.
  104. Coop, G. Does linked selection explain the narrow range of genetic diversity across species? Preprint at bioRxiv http://dx.doi.org/10.1101/042598 (2016).
  105. Reed, F. A., Akey, J. M. & Aquadro, C. F. Fitting background-selection predictions to levels of nucleotide variation and divergence along the human autosomes. Genome Res. 15, 12111221 (2005).
  106. Rockman, M. V. The QTN program and the alleles that matter for evolution: all that's gold does not glitter. Evolution 66, 117 (2012).
  107. Le Corre, V. & Kremer, A. The genetic differentiation at quantitative trait loci under local adaptation. Mol. Ecol. 21, 15481566 (2012).
    This meta-analyses reviews expectations for allelic differentiation at QTLs and highlights the limitations of FST-based genome scans.
  108. Beaumont, M. A. Adaptation and speciation: what can Fst tell us? Trends Ecol. Evol. 20, 435440 (2005).
  109. Foll, M. & Gaggiotti, O. A. Genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180, 977993 (2008).
  110. Beaumont, M. A. & Nichols, R. A. Evaluating loci for use in the genetic analysis of population structure. Proc. R. Soc. Lond. B Biol. Sci. 263, 16191626 (1996).
  111. 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, 28522862 (2012).
  112. Zeng, K. A coalescent model of background selection with recombination, demography and variation in selection coefficients. Heredity 110, 363371 (2013).
  113. Roesti, M., Gavrilets, S., Hendry, A. P., Salzburger, W. & Berner, D. The genomic signature of parallel adaptation from shared genetic variation. Mol. Ecol. 23, 39443956 (2014).
  114. Berner, D. & Salzburger, W. The genomics of organismal diversification illuminated by adaptive radiations. Trends Genet. 31, 491499 (2015).
  115. Poelstra, J. W., Vijay, N., Hoeppner, M. P. & Wolf, J. B. W. Transcriptomics of colour patterning and coloration shifts in crows. Mol. Ecol. 24, 46174628 (2015).
  116. Laporte, M. et al. RAD-QTL mapping reveals both genome-level parallelism and different genetic architecture underlying the evolution of body shape in lake whitefish (Coregonus clupeaformis) species pairs. G3 (Bethesda) 5, 14811491 (2015).
  117. Winkler, C. A., Nelson, G. W. & Smith, M. W. Admixture mapping comes of age. Annu. Rev. Genom. Hum. Genet. 11, 6589 (2010).
  118. Gompert, Z. & Buerkle, C. A. A powerful regression-based method for admixture mapping of isolation across genome hybrids. Mol. Ecol. 18, 12071224 (2009).
  119. Bono, J. M., Olesnicky, E. C. & Matzkin, L. M. Connecting genotypes, phenotypes and fitness: harnessing the power of CRISPR/Cas9 genome editing. Mol. Ecol. 24, 38103822 (2015).
  120. Hall, A. B. et al. A male-determining factor in the mosquito Aedes aegypti. Science 348, 12681270 (2015).
  121. Markert, M. J. et al. Genomic access to Monarch migration using TALEN and CRISPR/Cas9-mediated targeted mutagenesis. G3 (Bethesda) 6, 905915 (2016).
  122. 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, 364373 (2012).
  123. Earl, D. et al. Assemblathon 1: a competitive assessment of de novo short read assembly methods. Genome Res. 21, 22242241 (2011).
  124. Darwin, C. On the Origin of Species by Means of Natural Selection or the Preservation of Favoured Races in the Struggle for Life (John Murray, 1859).
  125. Kohn, D. in The Cambridge Companion to the “Origin of Species” (eds Ruse, M. & Richards, R. J.) 87108 (Cambridge Univ. Press, 2008).
  126. Mallet, J. Mayr's view of Darwin: was Darwin wrong about speciation? Biol. J. Linn. Soc. 95, 316 (2008).
  127. Mayr, E. Systematics and the Origin of Species (Columbia Univ. Press, 1942).
  128. Orr, H. A. The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139, 18051813 (1995).
  129. Muller, H. J. Isolating mechanisms, evolution and temperature. Biol. Symp. 6, 71125 (1942).
  130. Bateson, W. in Darwin and Modern Science (ed. Seward, A. C.) 85101 (Cambridge Univ. Press, 1909).
  131. Oka, H.-I. Genic analysis for the sterility of hybrids between distantly related varieties of cultivated rice. J. Genet. 55, 397409 (1957).
  132. Smadja, C. M. & Butlin, R. K. A framework for comparing processes of speciation in the presence of gene flow. Mol. Ecol. 20, 51235140 (2011).
  133. Dieckmann, U. & Doebeli, M. On the origin of species by sympatric speciation. Nature 400, 354357 (1999).
  134. Barluenga, M., Stolting, K. N., Salzburger, W., Muschick, M. & Meyer, A. Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439, 719723 (2006).
  135. Papadopulos, A. S. T. et al. Speciation with gene flow on Lord Howe Island. Proc. Natl Acad. Sci. USA 108, 1318813193 (2011).
  136. Roux, C. et al. Shedding light on the grey zone of speciation along a continuum of genomic divergence. Preprint at bioRxiv http://dx.doi.org/10.1101/059790 (2016).
  137. Doebeli, M. & Dieckmann, U. Speciation along environmental gradients. Nature 421, 259264 (2003).
  138. Flaxman, S. M., Wacholder, A. C., Feder, J. L. & Nosil, P. Theoretical models of the influence of genomic architecture on the dynamics of speciation. Mol. Ecol. 40744088 (2014).
  139. Gavrilets, S. Models of speciation: where are we now? J. Hered. 105, 743755 (2014).
  140. Abbott, R. et al. Hybridization and speciation. J. Evol. Biol. 26, 229246 (2013).
    This perspective article summarizes important aspects of speciation with gene flow.
  141. Flaxman, S. M., Feder, J. L. & Nosil, P. Genetic hitchhiking and the dynamic buildup of genomic divergence during speciation with gene flow. Evolution 67, 25772591 (2013).
  142. van Doorn, G. S., Edelaar, P. & Weissing, F. J. On the origin of species by natural and sexual selection. Science 326, 17041707 (2009).
  143. Servedio, M. R., Doorn, G. S. V., Kopp, M., Frame, A. M. & Nosil, P. Magic traits in speciation: 'magic' but not rare? Trends Ecol. Evol. 26, 389397 (2011).
  144. Thompson, M. J. & Jiggins, C. D. Supergenes and their role in evolution. Heredity 113, 18 (2014).
  145. Wright, S. Evolution in Mendelian populations. Genetics 16, 97159 (1931).
  146. Wright, S. The genetical structure of populations. Ann. Eugen. 15, 323354 (1951).
  147. Holsinger, K. E. & Weir, B. S. Genetics in geographically structured populations: defining, estimating and interpreting FST. Nat. Rev. Genet. 10, 639650 (2009).
  148. Nei, M. Analysis of gene diversity in subdivided populations. Proc. Natl Acad. Sci. USA 70, 33213323 (1973).
  149. Hedrick, P. W. A standardized genetic differentiation measure. Evolution 59, 16331638 (2005).
  150. Jost, L. GST and its relatives do not measure differentiation. Mol. Ecol. 17, 40154026 (2008).
  151. Bhatia, G., Patterson, N., Sankararaman, S. & Price, A. L. Estimating and interpreting Fst: the impact of rare variants. Genome Res. 23, 15141521 (2013).
  152. Jakobsson, M., Edge, M. D. & Rosenberg, N. A. The relationship between FST and the frequency of the most frequent allele. Genetics 193, 515528 (2013).
  153. Lamichhaney, S. et al. Evolution of Darwin's finches and their beaks revealed by genome sequencing. Nature 518, 371375 (2015).
  154. Yi, X. et al. Sequencing of fifty human exomes reveals adaptation to high altitude. Science 329, 7578 (2010).
  155. Nei, M. Molecular Evolutionary Genetics. (Columbia Univ. Press, 1987).
  156. Nei, M. & Li, W. H. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc. Natl Acad. Sci. USA 76, 52695273 (1979).
  157. Hey, J. The structure of genealogies and the distribution of fixed differences between DNA sequence samples from natural populations. Genetics 128, 831840 (1991).
  158. Watterson, G. A. On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7, 256276 (1975).
  159. Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585595 (1989).
  160. Fu, Y. X. & Li, W. H. Statistical tests of neutrality of mutations. Genetics 133, 693709 (1993).
  161. Kemppainen, P. et al. Linkage disequilibrium network analysis (LDna) gives a global view of chromosomal inversions, local adaptation and geographic structure. Mol. Ecol. Resour. 15, 10311045 (2015).
  162. Sabeti, P. C. et al. Detecting recent positive selection in the human genome from haplotype structure. Nature 419, 832837 (2002).
  163. Sabeti, P. C. et al. Genome-wide detection and characterization of positive selection in human populations. Nature 449, 913918 (2007).
  164. Mailund, T., Dutheil, J. Y., Hobolth, A., Lunter, G. & Schierup, M. H. Estimating divergence time and ancestral effective population size of Bornean and Sumatran orangutan subspecies using a coalescent hidden Markov model. PLoS Genet. 7, e1001319 (2011).
  165. Zamani, N. et al. Unsupervised genome-wide recognition of local relationship patterns. BMC Genomics 14, 347 (2013).

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Affiliations

  1. Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, SE-752 36 Uppsala, Sweden.

    • Jochen B. W. Wolf &
    • Hans Ellegren
  2. Section of Evolutionary Biology, Department of Biology II, Ludwig Maximilian University of Munich, Grosshaderner Strasse 2, Planegg-Martinsried 82152, Germany.

    • Jochen B. W. Wolf

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The authors declare no competing interests.

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  • Jochen B. W. Wolf

    Jochen B. W. Wolf is a professor in evolutionary biology at the Faculty of Biology, Ludwig-Maximilians University Munich, Germany. He is also guest professor at the Evolutionary Biology Centre, Uppsala University, Sweden. His research group takes an integrative approach to the study of evolutionary processes in a variety of natural and experimental systems, often using large-scale genomic approaches. Jochen B. W. Wolf's homepage

  • Hans Ellegren

    Hans Ellegren is a professor in evolutionary biology at the Evolutionary Biology Centre, Uppsala University, Sweden. His laboratory studies evolutionary genetic questions relating to molecular ecology, molecular evolution, sex chromosome evolution and speciation genetics using bioinformatic and genomic approaches. Hans Ellegren's homepage

Supplementary information

Excel files

  1. Supplementary information S1 (table) (29 KB)

    A Compilation of a literature survey including 67 studies drawn from searching the ISI Web of Knowledge database for terms 'speciation genomics', 'islands of differentiation', 'islands of speciation' and 'speciation with gene flow', and complemented with other references.

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