Genomics and the origin of species (original) (raw)

• 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
• Nosil, P. Ecological Speciation (Oxford Univ. Press, 2012). This is an in-depth treatment of speciation by divergent natural selection.
  Book Google Scholar
• Price, T. Speciation in Birds (Roberts & Company, 2008).
  Google Scholar
• 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
• Muller, H. J. & Pontecorvo, G. Recessive genes causing interspecific sterility and other disharmonies between Drosophila melanogaster and simulans. Genetics 27, 157 (1942).
  Google Scholar
• Gavrilets, S. Fitness Landscapes and the Origin of Species (Princeton Univ. Press, 2004).
  Google Scholar
• 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
• 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
• Gavrilets, S. & Losos, J. B. Adaptive radiation: contrasting theory with data. Science 323, 732–737 (2009).
  Article CAS PubMed Google Scholar
• Dieckmann, U., Doebeli, M., Metz, J. A. J. & Tautz, D. (eds) Adaptive Speciation (Cambridge Univ. Press, 2004).
  Book Google Scholar
• 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
• 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
• 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
• Panhuis, T. M., Butlin, R., Zuk, M. & Tregenza, T. Sexual selection and speciation. Trends Ecol. Evol. 16, 364–371 (2001).
  Article PubMed Google Scholar
• Boughman, J. W. How sensory drive can promote speciation. Trends Ecol. Evol. 17, 571–577 (2002).
  Article Google Scholar
• Maan, M. E. & Seehausen, O. Ecology, sexual selection and speciation. Ecol. Lett. 14, 591–602 (2011).
  Article PubMed Google Scholar
• 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
• Abbott, R. et al. Hybridization and speciation. J. Evol. Biol. 26, 229–246 (2013).
  Article CAS PubMed Google Scholar
• Presgraves, D. C. Speciation genetics: search for the missing snowball. Curr. Biol. 20, R1073–R1074 (2010).
  Article CAS PubMed Google Scholar
• 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
• Rieseberg, L. H. & Blackman, B. K. Speciation genes in plants. Ann. Bot. 106, 439–455 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Rieseberg, L. H. & Burke, J. M. A genic view of species integration — commentary. J. Evol. Biol. 14, 883–886 (2001).
  Article Google Scholar
• 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
• 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
• 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
• 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
• Moyle, L. C. & Nakazato, T. Hybrid incompatibility “snowballs” between Solanum species. Science 329, 1521–1523 (2010).
  Article CAS PubMed Google Scholar
• 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
• Lynch, M. & Force, A. G. The origin of interspecific genomic incompatibility via gene duplication. Am. Naturalist 156, 590–605 (2000).
  Article Google Scholar
• Schluter, D. Evidence for ecological speciation and its alternative. Science 323, 737–741 (2009).
  Article CAS PubMed Google Scholar
• Nei, M., Maruyama, T. & Wu, C. I. Models of evolution of reproductive isolation. Genetics 103, 557–579 (1983).
  CAS PubMed PubMed Central Google Scholar
• 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
• Crespi, B. & Nosil, P. Conflictual speciation: species formation via genomic conflict. Trends Ecol. Evol. 28, 48–57 (2013).
  Article PubMed Google Scholar
• 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
• 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
• 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
• Malik, H. S. in Progress in Molecular and Subcellular Biology (ed. Ugarovic, D.) 33–52 (Springer, 2009).
  Google Scholar
• 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
• 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
• Watson, E. T. & Demuth, J. P. in Speciation: Natural Processes, Genetics and Biodiversity (ed. Michalak, P.) (Nova Science Publishers, 2013).
  Google Scholar
• 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
• 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
• van Doorn, G. S. & Kirkpatrick, M. Turnover of sex chromosomes induced by sexual conflict. Nature 449, 909–912 (2007).
  Article CAS PubMed Google Scholar
• 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
• 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
• 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
• Yeaman, S. & Whitlock, M. C. The genetic architecture of adaptation under migration–selection balance. Evolution 65, 1897–1911 (2011).
  Article PubMed Google Scholar
• 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
• 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
• Bull, J. J. Evolution of Sex-determining Mechanisms. (Benjamin/Cumings, 1983).
  Google Scholar
• 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
• 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
• Lindholm, A. & Breden, F. Sex chromosomes and sexual selection in poeciliid fishes. Am. Naturalist 160, S214–S224 (2002).
  Article Google Scholar
• 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
• Templeton, A. R. Mechanisms of speciation — a population genetic approach. Annu. Rev. Ecol. Systemat. 12, 23–48 (1981).
  Article Google Scholar
• 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
• Coyne, J. A. Genetics and speciation. Nature 355, 511–515 (1992).
  Article CAS PubMed Google Scholar
• Price, T. D. & Bouvier, M. M. The evolution of F1 postzygotic incompatibilities in birds. Evolution 56, 2083–2089 (2002).
  Article PubMed Google Scholar
• 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
• 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
• 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
• 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
• Nosil, P., Funk, D. J. & Ortiz-Barrientos, D. Divergent selection and heterogeneous genomic divergence. Mol. Ecol. 18, 375–402 (2009).
  Article PubMed Google Scholar
• 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
• Barton, N. Gene flow and speciation. Heredity 50, 213–213 (1983).
  Article Google Scholar
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• Via, S., Conte, G., Mason-Foley, C. & Mills, K. Localizing _F_ST 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• Spencer, C. C. A. et al. The influence of recombination on human genetic diversity. PLoS Genet. 2, 1375–1385 (2006).
  Article CAS Google Scholar
• 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
• Nei, M. Molecular Evolutionary Genetics (Columbia Univ. Press, 1987).
  Book Google Scholar
• 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
• 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
• 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
• Heliconius Genome Consortium. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487, 94–98 (2012).
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• Schluter, D. & Conte, G. L. Genetics and ecological speciation. Proc. Natl Acad. Sci. USA 106, 9955–9962 (2009).
  Article PubMed PubMed Central Google Scholar
• 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
• 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
• 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
• Seehausen, O. Hybridization and adaptive radiation. Trends Ecol. Evol. 19, 198–207 (2004).
  Article PubMed Google Scholar
• 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
• 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
• 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
• 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
• 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
• Barton, N. H. Multilocus clines. Evolution 37, 454–471 (1983).
  Article CAS PubMed Google Scholar
• 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
• Nosil, P., Harmon, L. J. & Seehausen, O. Ecological explanations for (incomplete) speciation. Trends Ecol. Evol. 24, 145–156 (2009).
  Article PubMed Google Scholar
• Doebeli, M. & Dieckmann, U. Speciation along environmental gradients. Nature 421, 259–264 (2003).
  Article CAS PubMed Google Scholar
• 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
• 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
• Qvarnström, A. & Bailey, R. I. Speciation through evolution of sex-linked genes. Heredity 102, 4–15 (2009).
  Article CAS PubMed Google Scholar
• Pryke, S. R. & Griffith, S. C. Postzygotic genetic incompatibility between sympatric color morphs. Evolution 63, 793–798 (2009).
  Article PubMed Google Scholar
• 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
• 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
• 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
• Hopkins, R. & Rausher, M. D. Pollinator-mediated selection on flower color allele drives reinforcement. Science 335, 1090–1092 (2012).
  Article CAS PubMed Google Scholar
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• Saetre, G. P. & Saether, S. A. Ecology and genetics of speciation in Ficedula flycatchers. Mol. Ecol. 19, 1091–1106 (2010).
  Article PubMed Google Scholar
• 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
• 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
• 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
• Orr, H. A. The genetics of species differences. Trends Ecol. Evol. 16, 343–350 (2001).
  Article Google Scholar
• 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
• Fisher, R. A. The Genetical Theory of Natural Selection (Clarendon Press, 1930).
  Book Google Scholar
• 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
• Orr, H. A. The genetic theory of adaptation: a brief history. Nature Rev. Genet. 6, 119–127 (2005).
  Article CAS PubMed Google Scholar
• 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
• Gordo, I. & Campos, P. R. Evolution of clonal populations approaching a fitness peak. Biol. Lett. 9, 20120239 (2013).
  Article PubMed PubMed Central Google Scholar
• Guillaume, F. & Whitlock, M. C. Effects of migration on the genetic covariance matrix. Evolution 61, 2398–2409 (2007).
  Article PubMed Google Scholar
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• Lande, R. Quantitative genetic-analysis of multivariate evolution, applied to brain — body size allometry. Evolution 33, 402–416 (1979).
  Article PubMed Google Scholar
• 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
• Roff, D. The evolution of the G matrix: selection or drift? Heredity 84, 135–142 (2000).
  Article PubMed Google Scholar
• Martin, G., Chapuis, E. & Goudet, J. Multivariate _Q_st–_F_st 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• Kopp, A. Metamodels and phylogenetic replication: a systematic approach to the evolution of developmental pathways. Evolution 63, 2771–2789 (2009).
  Article PubMed Google Scholar
• 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
• Nolte, A. W. & Tautz, D. Understanding the onset of hybrid speciation. Trends Genet. 26, 54–58 (2010).
  Article CAS PubMed Google Scholar
• 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
• 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
• Seehausen, O. Conditions when hybridization might predispose populations for adaptive radiation. J. Evol. Biol. 26, 279–281 (2013).
  Article CAS PubMed Google Scholar
• Bolnick, D. I. & Fitzpatrick, B. M. Sympatric speciation: models and empirical evidence. Annu. Rev. Ecol. Evol. Systemat. 38, 459–487 (2007).
  Article Google Scholar
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• Buerkle, C. A. & Lexer, C. Admixture as the basis for genetic mapping. Trends Ecol. Evol. 23, 686–694 (2008).
  Article PubMed Google Scholar
• Gompert, Z. & Buerkle, C. A. Bayesian estimation of genomic clines. Mol. Ecol. 20, 2111–2127 (2011).
  Article PubMed Google Scholar
• 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
• 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
• 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
• Orr, H. A. The population-genetics of speciation — the evolution of hybrid incompatibilities. Genetics 139, 1805–1813 (1995).
  CAS PubMed PubMed Central Google Scholar
• Vonlanthen, P. et al. Eutrophication causes speciation reversal in whitefish adaptive radiations. Nature 482, 357–362 (2012).
  Article CAS PubMed Google Scholar
• 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
• Butlin, R. K., Bridle, J. R. & Schluter, D. Speciation and Patterns of Diversity (Cambridge Univ. Press, 2009).
  Book Google Scholar
• 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
• 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
• 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
• 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
• 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