Evolutionary Biology

, Volume 39, Issue 2, pp 158–180 | Cite as

Sympatric Speciation in the Post “Modern Synthesis” Era of Evolutionary Biology

  • Christopher E. BirdEmail author
  • Iria Fernandez-Silva
  • Derek J. Skillings
  • Robert J. Toonen
Synthesis Paper


Sympatric speciation is among the most controversial and challenging concepts in evolution. There are a multitude of definitions of speciation alone, and when combined with the biogeographic concept of sympatric range overlap, consensus on what sympatric speciation is, whether it happens, and its importance, is even more difficult to achieve. Providing the basis upon which to define and judge sympatric speciation, the Modern Evolutionary Synthesis (Huxley in Evolution: the modern synthesis. MIT Press, Cambridge, 1942) led to the conclusion that sympatric speciation is an inconsequential process in the generation of species diversity. In the post Modern Synthesis era of evolutionary biology, the PCR revolution and associated accumulation of DNA sequence data from natural populations has led to a resurgence of interest in sympatric speciation, and more importantly, the role of natural selection in lineage diversification. Much effort is currently being devoted to elucidating the processes by which the constituents of an initially panmictic population can become reproductively isolated and evolve some level of reproductive incompatibility without the complete cessation of gene flow due to geographic barriers. The evolution of reproductive isolation solely due to natural selection is perhaps the most controversial manner by which sympatric speciation occurs, and it is that which we focus upon in this review. Mathematical model simulations indicate that even strict definitions of sympatric speciation are possible to satisfy, empirical data consistent with sympatric divergence are accumulating, but irrefutable evidence of sympatric speciation in natural populations remains elusive. Genomic investigations are advancing our ability to identify genetic patterns caused by natural selection, thereby advancing our understanding of the power of natural selection relative to gene flow. Overall, sympatric lineage divergence, especially at the sub-species level, may have led to a substantial portion of biodiversity.


Lineage Population Divergence Selection Gene flow 



For intellectual discussions that motivated and significantly improved this manuscript, we would like to thank Stephen Karl, Brian Bowen, Richard Grosberg, Luiz Rocha, Matthew Craig, Jonathan Whitney, Maria Pia Miglietta, Anuschka Faucci, Francesco Santini, Giacomo Bernardi, Michael Hart, Bernard Crespi, Stephen Palumbi, John Geller, Steven Morgan, Rosemary Gillespi, George Roderick, Nina Yasuda, Gustav Paulay, Christopher Meyer, Harilaos Lessios, the SICB marine speciation group, and audiences at U. C. Davis, U. C. Berkeley, U. C. Santa Cruz, U. C. Davis’ Bodega Bay Marine Laboratory, Cal. State’s Moss Landing Marine Laboratory, Stanford’s Hopkins Marine Laboratory, Simon Frasier University, University of Connecticut, Texas A&M University-Corpus Christi, Florida International University, and the University of Hawai’i. We also thank the efforts of two anonymous reviewers that helped to substantially improved this manuscript. CEB was funded by a grant from the Seaver Institute, the Hawai’i Sea Grant College Program, and the Papahanaumokuakea Marine National Monument. This is publication number 1491 from the Hawai’i Institute of Marine Biology, 8604 from the School of Ocean, Earth Sciences and Technology at the University of Hawai’i, and XXXX from the Marine Biology Program at Texas A&M University-Corpus Christi.


  1. Adachi-Hagimori, T., Miura, K., & Abe, Y. (2011). Gene flow between sexual and asexual strains of parasitic wasps: A possible case of sympatric speciation caused by a parthenogenesis-inducing bacterium. Journal of Evolutionary Biology, 24, 1254–1262.PubMedGoogle Scholar
  2. Allendorf, F. W., Hohenlohe, P. A., & Luikart, G. (2010). Genomics and the future of conservation genetics. Nature Reviews Genetics, 11, 697–709.PubMedGoogle Scholar
  3. Altshuler, D. L., Durbin, R. M., Abecasis, G. R., Bentley, D. R., Chakravarti, A., 1000 Genomes Project Consortium, et al. (2010). A map of human genome variation from population-scale sequencing. Nature, 467, 1061–1073.Google Scholar
  4. Avise, J. C., & Wollenberg, K. (1997). Phylogenetics and the origin of species. Procedings of the National Academy of Sciences, USA, 94, 7748–7755.Google Scholar
  5. Babik, W., Butlin, R. K., Baker, W. J., Papadopulos, A. S. T., Boulesteix, M., Anstett, M., et al. (2009). How sympatric is speciation in the Howea palms of Lord Howe Island? Molecular Ecology, 18, 3629–3638.PubMedGoogle Scholar
  6. Baird, N. A., Etter, P. D., Atwood, T. S., Currey, M. C., Shiver, A. L., et al. (2008). Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE, 3, e3376. doi: 10.1371/journal.pone.0003376.PubMedGoogle Scholar
  7. Barbazuk, W. B., Emrich, S. J., Chen, H. D., Li, L., & Schnable, P. S. (2007). SNP discovery via 454 transcriptome sequencing. The Plant Journal, 51, 910–918.PubMedGoogle Scholar
  8. Barluenga, M., & Meyer, A. (2010). Phylogeography, colonization and population history of the Midas cichlid species complex (Amphilophus spp.) in the Nicaraguan crater lakes. BMC Evolutionary Biology, 10, 326.PubMedGoogle Scholar
  9. Barluenga, M., Stolting, K. N., Salzburger, W., Muschick, M., & Meyer, A. (2006). Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature, 439, 719–723.PubMedGoogle Scholar
  10. Barraclough, T. G., & Vogler, A. P. (2000). Detecting the geographical pattern of speciation from species-level phylogenies. American Naturalist, 155, 419–433.PubMedGoogle Scholar
  11. Barton, N. H. (2010). What role does natural selection play in speciation? Philosophical Transactions of the Royal Society B-Biological Sciences, 365, 1825–1840.Google Scholar
  12. Beaumont, M. A. (2008). Joint determination of topology, divergence time and immigration in population trees. In S. Matsumura, P. Forster, & C. Renfrew (Eds.), Simulations, genetics and human prehistory (pp. 135–154). Cambridge: McDonald Institute for Archaeological Research.Google Scholar
  13. Beaumont, M. A., Zhang, W., & Balding, D. J. (2002). Approximate Bayesian computation in population genetics. Genetics, 162, 2025–2035.PubMedGoogle Scholar
  14. Bertorelle, G., Benazzo, A., & Mona, S. (2010). ABC as a flexible framework to estimate demography over space and time: Some cons, many pros. Molecular Ecology, 19, 2609–2625.PubMedGoogle Scholar
  15. Bird, C. E. (2011). Morphological and behavioral evidence for adaptive diversification of sympatric Hawaiian limpets. Journal of Integrative and Comparative Biology, 51, 466–473.Google Scholar
  16. Bird, C. E., Holland, B. S., Bowen, B. W., & Toonen, R. J. (2007). Contrasting phylogeography in three endemic Hawaiian limpets (Cellana spp.) with similar life histories. Molecular Ecology, 16, 3173–3186.PubMedGoogle Scholar
  17. Bird, C. E., Holland, B. S., Bowen, B. W., & Toonen, R. J. (2011a). Diversification of sympatric broadcast-spawning limpets (Cellana spp.) within the Hawaiian archipelago. Molecular Ecology, 20, 2128–2141.PubMedGoogle Scholar
  18. Bird, C. E., Smouse, P. E., Karl, S. A., & Toonen, R. J. (2011b). Detecting and measuring genetic differentiation. In S. Koenemann, C. Schubart, & C. Held (Eds.), Crustacean issues: Phylogeography and population genetics in crustacea (pp. 31–73). Boca Raton, FL: CRC Press.Google Scholar
  19. Bolnick, D. I. (2004). Waiting for sympatric speciation. Evolution, 58, 895–899.PubMedGoogle Scholar
  20. Bolnick, D. I. (2011). Sympatric speciation in threespine stickleback: Why not? International Journal of Ecology. doi: 10.1155/2011/942847.Google Scholar
  21. Bolnick, D. I., & Doebeli, M. (2003). Sexual dimorphism and adaptive speciation: Two sides of the same ecological coin. Evolution, 57, 2433–2449.PubMedGoogle Scholar
  22. Bolnick, D. I., & Fitzpatrick, B. M. (2007). Sympatric speciation: Models and empirical evidence. Annual Review of Ecology Evolution and Systematics, 38, 459–487.Google Scholar
  23. Briggs, J. C. (2007). Marine longitudinal biodiversity: Causes and conservation. Diversity and Distributions, 13, 544–555.Google Scholar
  24. Butlin, R. K., Galindo, J., & Grahame, J. W. (2008). Sympatric, parapatric or allopatric: The most important way to classify speciation? Philosophical Transactions of the Royal Society B-Biological Sciences, 363, 2997–3007.Google Scholar
  25. Chan, Y. L., Anderson, C. N. K., & Hadly, E. A. (2006). Bayesian estimation of the timing and severity of a population bottleneck from ancient DNA. PLoS Genetics, 2, e59. doi: 10.1371/journal.pgen.0020059.PubMedGoogle Scholar
  26. Coyne, J. A. (2007). Sympatric speciation. Current Biology, 17, R787–R788.PubMedGoogle Scholar
  27. Coyne, J. A. (2011). Speciation in a small space. Proceedings of the National Academy of Sciences USA, 108, 12975–12976.Google Scholar
  28. Coyne, J. A., & Orr, H. A. (1989). Two rules of speciation. In D. Otte & J. A. Endler (Eds.), Speciation and its consequences (pp. 180–207). Sunderland, MA: Sinauer Associates.Google Scholar
  29. Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland, MA: Sinauer Associates.Google Scholar
  30. Coyne, J. A., & Price, T. D. (2000). Little evidence for sympatric speciation in island birds. Evolution, 54, 2166–2171.PubMedGoogle Scholar
  31. Crow, K. D., Munehara, H., & Bernardi, G. (2010). Sympatric speciation in a genus of marine reef fishes. Molecular Ecology, 19, 2089–2105.PubMedGoogle Scholar
  32. Darwin, C. (1859). On the origin of species by means of natural selection or the preservation of favored races in the struggle for life. London: J. Murray.Google Scholar
  33. de Queiroz, K. (1998). The general lineage concept of species, species criteria, and the process of speciation: A conceptual unification and terminological recommendations. In D. J. Howard & S. H. Berlocher (Eds.), Endless forms: Species and speciation (pp. 57–75). New York: Oxford University Press.Google Scholar
  34. de Queiroz, K. (1999). The general lineage concept of species and the defining properties of the species category. In R. A. Wilson (Ed.), Species: New interdisciplinary essays (pp. 49–89). Cambridge, MA: MIT Press.Google Scholar
  35. de Queiroz, K. (2005). A unified concept of species and its consequences for the future of taxonomy. Proceedings of the California Academy of Sciences, 56, 196–215.Google Scholar
  36. de Queiroz, K. (2007). Species concepts and delimitation. Systematic Biology, 56, 879–886.PubMedGoogle Scholar
  37. Dieckmann, U., & Doebeli, M. (1999). On the origin of species by sympatric speciation. Nature, 400, 354–357.PubMedGoogle Scholar
  38. Dieckmann, U., & Doebeli, M. (2005). Pluralism in evolutionary theory. Journal of Evolutionary Biology, 18, 1209–1213.PubMedGoogle Scholar
  39. Dobzhansky, T. (1937). Genetics and the origin of species. New York: Columbia University Press.Google Scholar
  40. Dobzhansky, T. (1950). Mendelian populations and their evolution. American Naturalist, 84, 401–418.Google Scholar
  41. Ellegren, H. (2008). Sequencing goes 454 and takes large-scale genomics into the wild. Molecular Ecology, 17, 1629–1631.PubMedGoogle Scholar
  42. Excoffier, L., Smouse, P. E., & Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics, 131, 479–491.PubMedGoogle Scholar
  43. Feder, J. L. (1998). The apple maggot fly, Rhagoletis pomonella: flies in the face of conventional wisdom about speciation? In D. Howard & S. H. Berlocher (Eds.), Endless forms: Species and speciation (pp. 130–144). London: Oxford University Press.Google Scholar
  44. Feder, J. L., Berlocher, S. H., Roethele, J. B., Dambroski, H., Smith, J. J., Perry, W. L., et al. (2003). Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis. Proceedings of the National Academy of Sciences, USA, 100, 10314–10319.Google Scholar
  45. Feder, J. L., Gejii, R., Powell, T. H. Q., & Nosil, P. (2011). Adaptive chromosomal divergence driven by mixed geographic mode of evolution. Evolution, 65, 2157–2170.PubMedGoogle Scholar
  46. Feder, J. L., & Nosil, P. (2010). The efficacy of divergence hitchhiking in generating genomic islands during ecological speciation. Evolution, 64, 1729–1747.PubMedGoogle Scholar
  47. Felsenstein, J. (1981). Skepticism towards Santa Rosalia, or why are there so few kinds of animals? Evolution, 35, 124–138.Google Scholar
  48. Fitzpatrick, B. M., Fordyce, J. A., & Gavrilets, S. (2008). What, if anything, is sympatric speciation? Journal of Evolutionary Biology, 21, 1452–1459.PubMedGoogle Scholar
  49. Fitzpatrick, B. M., Fordyce, J. A., & Gavrilets, S. (2009). Pattern, process and geographic modes of speciation. Journal of Evolutionary Biology, 22, 2342–2347.PubMedGoogle Scholar
  50. Fry, J. D. (2003). Detecting ecological trade-offs using selection experiments. Ecology, 84, 1672–1678.Google Scholar
  51. Gaggiotti, O. E. (2011). Making inferences about speciation using sophisticated statistical genetics methods: look before you leap. Molecular Ecology, 20, 2229–2232.PubMedGoogle Scholar
  52. Gavrilets, S. (2004). Fitness landscapes and the origin of species. Princeton, NJ: Princeton University Press.Google Scholar
  53. Gavrilets, S. (2005). The Maynard Smith model of sympatric speciation. Journal of Theoretical Biology, 239, 172–182.PubMedGoogle Scholar
  54. Gavrilets, S., & Vose, A. (2007). Case studies and mathematical models of ecological speciation. 2. Palms on an oceanic island. Molecular Ecology, 16, 2910–2921.PubMedGoogle Scholar
  55. Gavrilets, S., Vose, A., Barluenga, M., Salzburger, W., & Meyer, A. (2007). Case studies and mathematical models of ecological speciation. 1. Cichlids in a crater lake. Molecular Ecology, 16, 2893–2909.PubMedGoogle Scholar
  56. Getz, W. M., & Kaitala, V. (1989). Ecogenetic models, competition, and heteropatry. Theoretical Population Biology, 36, 34–58.Google Scholar
  57. Gourbiere, S., & Mallet, J. (2005). Has adaptive dynamics contributed to the understanding of adaptive and sympatric speciation? Journal of Evolutionary Biology, 18, 1201–1204.PubMedGoogle Scholar
  58. Hamilton, G., Currat, M., Ray, N., Heckel, G., Beaumont, M., & Excoffier, L. (2005). Bayesian estimation of recent migration rates after a spatial expansion. Genetics, 170, 409–417.PubMedGoogle Scholar
  59. Hammer, M. F., Woerner, A. E., Mendez, F. L., Watkins, J. C., & Wall, J. D. (2011). Genetic evidence for archaic admixture in Africa. Proceedings of the National Academy of Sciences, USA, 108, 15123–15128.Google Scholar
  60. Hart, M. W. (2010). The species concept as an emergent property of population biology. Evolution, 65, 613–616.PubMedGoogle Scholar
  61. Hedrick, P. W. (2005). A standardized genetic differentiation measure. Evolution, 59, 1633–1638.PubMedGoogle Scholar
  62. Hellberg, M. E. (1998). Sympatric sea shells along the sea’s shore: the geography of speciation in the marine gastropod Tegula. Evolution, 52, 1311–1324.Google Scholar
  63. Hendry, A. P., Vamosi, S. M., Latham, S. J., Heilbuth, J. C., & Day, T. (2000). Questioning species realities. Conservation Genetics, 1, 67–76.Google Scholar
  64. Hey, J. (2006). On the failure of modern species concepts. Trends in Ecology & Evolution, 21, 447–450.Google Scholar
  65. Hickerson, M. J., Carstens, B. C., Cavender-Bares, J., Crandall, K. A., Graham, J. B., Johnson, J. B., et al. (2010). Phylogeography’s past, present, and future: 10 years after Avise 2000. Molecular Phylogenetics and Evolution, 54, 291–301.PubMedGoogle Scholar
  66. Hohenlohe, P. A., Bassham, S., Etter, P. D., Stiffler, N., Johnson, E. A., et al. (2010a). Population genomics of parallel adaptation in threespine stickleback using sequenced RAD Tags. PLoS Genetics, 6, e1000862. doi: 10.1371/journal.pgen.1000862.PubMedGoogle Scholar
  67. Hohenlohe, P. A., Phillips, P. C., & Cresko, W. A. (2010b). Using population genomics to detect selection in natural populations: key concepts and methodological considerations. International Journal of Plant Sciences, 171, 1059–1071.PubMedGoogle Scholar
  68. Huxley, J. S. (1942). Evolution: The modern synthesis. Cambridge, MA: MIT Press.Google Scholar
  69. Ilves, K., Huang, W., Wares, J. P., & Hickerson, M. J. (2010). Congruent histories of colonization and/or mitochondrial selective sweeps across the North Atlantic intertidal assemblage. Molecular Ecology, 19, 4505–4519.PubMedGoogle Scholar
  70. Jaarola, M., Martin, R. H., & Ashley, T. (1998). Direct evidence for suppression of recombination within two pericentric inversions in humans: A new sperm-FISH technique. American Journal of Human Genetics, 63, 218–224.PubMedGoogle Scholar
  71. Jiggins, C. D., Salazar, C., Linares, M., & Mavarez, J. (2008). Review. Hybrid trait speciation and Heliconius butterflies. Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 3047–3054.Google Scholar
  72. Johannesson, K. (2009). Inverting the null-hypothesis of speciation: a marine snail perspective. Evolutionary Ecology, 23, 5–16.Google Scholar
  73. Johannesson, K. (2010). Are we analyzing speciation without prejudice? Annals of the New York Academy of Sciences, 1206, 143–149.PubMedGoogle Scholar
  74. Johannesson, K., Panova, M., Kemppainen, P., Andre, C., Rolan-Alvarez, E., & Butlin, R. K. (2010). Repeated evolution of reproductive isolation in a marine snail: unveiling mechanisms of speciation. Philosophical Transactions of the Royal Society B-Biological Sciences, 365, 1735–1747.Google Scholar
  75. Johannesson, K., Rolan-Alvarez, E., & Ekendahl, A. (1995). Incipient reproductive isolation between two sympatric morphs of the intertidal snail Littorina saxatilis. Evolution, 49, 1180–1190.Google Scholar
  76. Jost, L. (2008). GST and its relatives do not measure differentiation. Molecular Ecology, 17, 4015–4026.PubMedGoogle Scholar
  77. Kelly, R. P., & Eernisse, D. J. (2008). Reconstructing a radiation: the chiton genus Mopalia in the north Pacific. Invertebrate Systematics, 22, 1–12.Google Scholar
  78. Kingman, J. F. C. (2000). Origins of the Coalescent: 1974–1982. Genetics, 156, 1461–1463.PubMedGoogle Scholar
  79. Kirkpatrick, M., & Ravigné, V. (2002). Speciation by natural and sexual selection: Models and experiments. American Naturalist, 159, S22–S35.PubMedGoogle Scholar
  80. Kisel, Y., & Barraclough, T. G. (2010). Speciation has a spatial scale that depends on levels of gene flow. American Naturalist, 175, 316–334.PubMedGoogle Scholar
  81. Krug, P. J. (2011). Patterns of speciation in marine gastropods: A review of the phylogenetic evidence for localized radiations in the sea. American Malacological Bulletin, 29, 169–186.Google Scholar
  82. Levene, H. (1953). Genetic equilibrium when more than one ecological niche is available. American Naturalist, 87, 331–333.Google Scholar
  83. Levin, D. A. (2009). Flowering-time plasticity facilitates niche shifts in adjacent populations. The New Phytologist, 183, 661–666.PubMedGoogle Scholar
  84. Losos, J. B., & Schluter, D. (2000). Analysis of an evolutionary species-area relationship. Nature, 408, 847–850.PubMedGoogle Scholar
  85. Love, A. C. (2009). Marine invertebrates, model organisms, and the modern synthesis: Epistemic values, evo-devo, and exclusion. Theory in Biosciences, 128, 19–42.PubMedGoogle Scholar
  86. Mallet, J., Meyer, A., Nosil, P., & Feder, J. L. (2009). Space, sympatry and speciation. Journal of Evolutionary Biology, 22, 2332–2341.PubMedGoogle Scholar
  87. Mardis, E. R. (2008). Next-generation DNA sequencing methods. Annual Review of Genomics and Human Genetics, 9, 387–402.PubMedGoogle Scholar
  88. Marie Curie SPECIATION Network. (2011). What do we need to know about speciation? Trends in Ecology and Evolution, 27, 27–39.Google Scholar
  89. Masly, J. P., & Presgraves, D. C. (2007). High-resolution genome-wide dissection of the two rules of speciation in Drosophila. PLoS Biology, 5, e243. doi: 10.1371/journal.pbio.0050243.PubMedGoogle Scholar
  90. Mayden, R. L. (1997). A hierarchy of species concepts: The denouement in the saga of the species problem. In M. F. Claridge, H. A. Dawah, & M. R. Wilson (Eds.), Species: The units of biodiversity (pp. 381–424). London: Chapman and Hall.Google Scholar
  91. Mayden, R. L. (1999). Consilience and a hierarchy of species concepts: Advances toward closure on the species puzzle. Journal of Nematology, 31, 95–116.PubMedGoogle Scholar
  92. Maynard Smith, J. (1966). Sympatric speciation. American Naturalist, 100, 637–650.Google Scholar
  93. Mayr, E. (1942). Systematics and the origin of species. New York: Columbia University Press.Google Scholar
  94. Mayr, E. (1954a). Geographic speciation in tropical echinoids. Evolution, 8, 1–18.Google Scholar
  95. Mayr, E. (1954b). Change of genetic environment and evolution. In J. Huxley, A. C. Hardy, & E. B. Ford (Eds.), Evolution as a process (pp. 157–180). London: Unwin Brothers.Google Scholar
  96. Mayr, E. (1963). Animal species and evolution. Cambridge, MA: Belknap Press of Harvard University Press.Google Scholar
  97. Mayr, E. (2001). Wu’s genic view of speciation. Journal of Evolutionary Biology, 14, 866–867.Google Scholar
  98. Meirmans, P. G. (2006). Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution, 60, 2399–2402.PubMedGoogle Scholar
  99. Mendel, G. (1866). Versuche über Pflanzen-Hybriden. Verh. Naturforsch. Ver. Brünn, 4, 3–47 (in English in 1901, Journal of the Royal Horticulture Society, 26, 1–32).Google Scholar
  100. Merrill, R. M., Gompert, Z., Dembeck, L. M., Kronforst, M. R., McMillan, W. O., & Jiggins, C. D. (2011). Mate preference across the speciation continuum in a clade of mimetic butterflies. Evolution, 65, 1489–1500.PubMedGoogle Scholar
  101. Messina, F. J., & Jones, J. C. (2011). Inheritance of traits mediating a major host shift by a seed beetle, Callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchinae). Annals of the Entomological Society of America, 104, 808–815.Google Scholar
  102. Messina, F. J., Mendenhall, M., & Jones, J. C. (2009). An experimentally induced host shift in a seed beetle. Entomologia Experimentalis et Applicata, 132, 39–49.Google Scholar
  103. Michel, A. P., Sim, S., Powell, T. H. Q., Taylor, M. S., Nosil, P., & Feder, J. L. (2010). Widespread genomic divergence during sympatric speciation. Proceedings of the Natural Academy of Science, USA, 107, 9724–9729.Google Scholar
  104. Miller, M. R., Dunham, J. P., Amores, A., Cresko, W. A., & Johnson, E. A. (2007). Rapid and cost-effective polymorphism identification and genotyping using restriction site associated DNA (RAD) markers. Genome Research, 17, 240–248.PubMedGoogle Scholar
  105. Muller, H. J. (1942). Isolation mechanisms, evolution and temperature. Biological Symposia, 6, 71–125.Google Scholar
  106. Mullis, K. (1990). The unusual origin of the polymerase chain reaction. Scientific American, 262, 56–65.PubMedGoogle Scholar
  107. Munday, P. L., Van Herwerden, L., & Dudgeon, C. L. (2004). Evidence for sympatric speciation by host shift in the sea. Current Biology, 14, 1498–1504.PubMedGoogle Scholar
  108. Nadeau, N. J., & Jiggins, C. D. (2010). A golden age for evolutionary genetics? Genomic studies of adaptation in natural populations. Trends in Genetics, 26, 484–492.PubMedGoogle Scholar
  109. Naomi, S.-I. (2011). On the integrated frameworks of species concepts: Mayden’s hierarchy of species concepts and de Queiroz’s unified concept of species. Journal of Zoological Systematics and Evolutionary Research, 49, 177–184.Google Scholar
  110. Niemiller, M. L., Fitzpatrick, B. M., & Miller, B. T. (2008). Recent divergence with gene flow in Tennessee cave salamanders (Plethodontidae: Gyrinophilus) inferred from gene genealogies. Molecular Ecology, 17, 2258–2275.PubMedGoogle Scholar
  111. Noor, M. A. F., Grams, K. L., Bertucci, L. A., & Reiland, J. (2001). Chromosomal inversions and the persistence of species. Proceedings of the Natural Academy of Science, USA, 98, 12084–12088.Google Scholar
  112. Nosil, P., & Feder, J. L. (2012). Genomic divergence during speciation: causes and consequences. Philosophical Transactions of the Royal Society B-Biological Sciences, 367, 332–342.Google Scholar
  113. Nosil, P., Funk, D. J., & Ortíz-Barrientos, D. (2009a). Divergent selection and heterogeneous genomic divergence. Molecular Ecology, 18, 375–402.PubMedGoogle Scholar
  114. Nosil, P., Harmon, L. J., & Seehausen, O. (2009b). Ecological explanations for (incomplete) speciation. Trends in Ecology & Evolution, 24, 145–156.Google Scholar
  115. O’Malley, K. G., Camara, M. D., & Banks, M. A. (2007). Candidate loci reveal genetic differentiation between temporally divergent migratory runs of Chinook salmon (Oncorhynchus tshawytscha). Molecular Ecology, 16, 4930–4941.PubMedGoogle Scholar
  116. Orr, H. A. (1996). Dobzhansky, Bateson, and the genetics of speciation. Genetics, 144, 1331–1335.PubMedGoogle Scholar
  117. Otto, S. P., & Whitton, J. (2000). Polyploid incidence and evolution. Annual Review of Genetics, 34, 401–437.PubMedGoogle Scholar
  118. Papadopulos, A. S. T., Baker, W. J., Crayn, D., Butlin, R. K., Kynast, R. G., Hutton, I., et al. (2011). Speciation with gene flow on Lord Howe Island. Proceedings of the National Academy of Sciences, USA, 108, 13188–13193.Google Scholar
  119. Patterson, N., Richter, D. J., Gnerre, S., Lander, E., & Reich, D. (2006). Genetic evidence for complex speciation of humans and chimpanzees. Nature, 441, 1103–1108.PubMedGoogle Scholar
  120. Patterson, N., Richter, D. J., Gnerre, S., Lander, E., & Reich, D. (2008). Reply: Complex speciation of humans and chimpanzees. Nature, 452, E4.Google Scholar
  121. Pinho, C., & Hey, J. (2010). Divergence with gene flow: Models and data. Annual Review of Ecology Evolution and Systematics, 41, 215–230.Google Scholar
  122. Poulton, E. B. (1904). What is a species? (Presidential address to the Entomological Society of London) Proceedings of the Entomological Society London (revised version in Poulton E. B. Essays on Evolution. 1889–1907. (1908) Clarendon Press, Oxford. pp. 46–94).Google Scholar
  123. Presgraves, D. C., & Yi, S. V. (2009). Doubts about complex speciation between humans and chimpanzees. Trends in Ecology & Evolution, 24, 533–540.Google Scholar
  124. Ribeiro, F., & Caticha, N. (2009). Emergence and loss of assortative mating in sympatric speciation. Journal of Theoretical Biology, 258, 465–477.PubMedGoogle Scholar
  125. Rocha, L. A., & Bowen, B. W. (2008). Speciation in coral reef fishes. Journal of Fish Biology, 72, 1101–1121.Google Scholar
  126. Rocha, L. A., Robertson, D. R., Roman, J., & Bowen, B. W. (2005). Ecological speciation in tropical reef fishes. Proceedings of the Royal Society of London. Series B, 272, 573–579.PubMedGoogle Scholar
  127. Rosenblum, E. B., & Harmon, L. J. (2011). “Same same but different”: Replicated ecological speciation at White Sands. Evolution, 65, 946–960.PubMedGoogle Scholar
  128. Rundle, H. D., & Nosil, P. (2005). Ecological speciation. Ecology Letters, 8, 336–352.Google Scholar
  129. Sadedin, S., Hollander, J., Panova, M., Johannesson, K., & Gavrilets, S. (2009). Case studies and mathematical models of ecological speciation. 3: Ecotype formation in a Swedish snail. Molecular Ecology, 18, 4006–4023.PubMedGoogle Scholar
  130. Sanger, F., Nicklen, S., & Coulson, A. R. (1977). DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences, USA, 74, 5463–5467.Google Scholar
  131. Savolainen, V., Anstett, M. C., Lexer, C., et al. (2006). Sympatric speciation in palms on an oceanic island. Nature, 441, 210–213.PubMedGoogle Scholar
  132. Schliewen, U. K., Tautz, D., & Paabo, S. (1994). Sympatric speciation suggested by monophyly of crater lake cichlids. Nature, 368, 629–632.PubMedGoogle Scholar
  133. Schluter, D. (2000). The ecology of adaptive radiation. New York: Oxford University Press Inc.Google Scholar
  134. Schluter, D. (2001). Ecology and the origin of species. Trends in Ecology & Evolution, 16, 372–380.Google Scholar
  135. Schluter, D. (2009). Evidence for ecological speciation and its alternative. Science, 323, 737–741.PubMedGoogle Scholar
  136. Seehausen, O. (1997). Distribution of and reproductive isolation among color morphs of a rock-dwelling Lake Victoria cichlid (Haplochromis nyererei). Ecology of Freshwater Fish, 6, 59–66.Google Scholar
  137. Servedio, M. R., Van Doorn, G. S., Kopp, M., Frame, A. M., & Nosil, P. (2011). Magic traits in speciation: ‘Magic’ but not rare? Trends in Ecology & Evolution, 26, 389–397.Google Scholar
  138. Simpson, G. G. (1944). Tempo and mode in evolution. New York: Columbia University Press.Google Scholar
  139. Simpson, G. G. (1951). The species concept. Evolution, 5, 285–298.Google Scholar
  140. Slatkin, M. (1987). Gene flow and the geographic structure of natural populations. Science, 236, 787–792.PubMedGoogle Scholar
  141. Smadja, C. M., & Butlin, R. K. (2011). A framework for comparing processes of speciation in the presence of gene flow. Molecular Ecology, 20, 5123–5140.PubMedGoogle Scholar
  142. Sobel, J. M., Chen, G. F., Watt, L. R., & Schemske, D. W. (2010). The biology of speciation. Evolution, 64, 295–315.PubMedGoogle Scholar
  143. Sousa, V. C., Fritz, M., Beaumont, M. A., & Chikhi, L. (2009). Approximate Bayesian computation without summary statistics: The case of admixture. Genetics, 181, 1507–1519.PubMedGoogle Scholar
  144. Sousa, V. C., Grelaud, A., & Hey, J. (2011). On the nonidentifiability of migration time estimates in isolation with migration models. Molecular Ecology, 20, 3956–3962.PubMedGoogle Scholar
  145. Stam, P. (1983). The evolution of reproductive isolation in closely adjacent populations through differential flowering time. Heredity, 50, 105–118.Google Scholar
  146. Stamatakis, A. (2006). RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.PubMedGoogle Scholar
  147. Strasburg, J. L., & Rieseberg, L. H. (2011). Interpreting the estimated timing of migration events between hybridizing species. Molecular Ecology, 20, 2353–2366.PubMedGoogle Scholar
  148. Stuessy, T. F. (2006). Sympatric plant speciation in islands? Nature, 443, E12.PubMedGoogle Scholar
  149. Templeton, A. R. (2008). The reality and importance of founder speciation in evolution. BioEssays, 30, 470–479.PubMedGoogle Scholar
  150. Thibert-Plante, X., & Hendry, A. P. (2011). The consequences of phenotypic plasticity for ecological speciation. Journal of Evolutionary Biology, 24, 326–342.PubMedGoogle Scholar
  151. Tomaiuolo, M., Hansen, T. F., & Levitan, D. R. (2007). A theoretical investigation of sympatric evolution of temporal reproductive isolation as illustrated by marine broadcast spawners. Evolution, 61, 2584–2595.PubMedGoogle Scholar
  152. Tucker, P. K., Sage, R. D., Wilson, A. C., & Eichler, E. M. (1992). Abrupt cline for sex chromosomes in a hybrid zone between two species of mice. Evolution, 46, 1146–1163.Google Scholar
  153. Turelli, M., Barton, N. H., & Coyne, J. A. (2001). Theory and speciation. Trends in Ecology & Evolution, 16, 330–342.Google Scholar
  154. Turner, T. L., Hahn, M. W., & Nuzhdin, S. V. (2005). Genomic islands of speciation in Anopheles gambiae. PLoS Biology, 3, e285. doi: 10.1371/journal.pbio.0030285.PubMedGoogle Scholar
  155. Via, S. (2001). Sympatric speciation in animals: The ugly duckling grows up. Trends in Ecology and Evolution, 16, 381–390.PubMedGoogle Scholar
  156. Via, S. (2009). Natural selection in action during speciation. Proceedings of the National Academy of Sciences, USA, 106, 9939–9946.Google Scholar
  157. Via, S., & West, J. A. (2008). The genetic mosaic suggests a new role for hitchhiking in ecological speciation. Molecular Ecology, 17, 4334–4345.PubMedGoogle Scholar
  158. Wakeley, J. (2008). Response: Complex speciation of humans and chimpanzees. Nature, 452, E3–E4.PubMedGoogle Scholar
  159. Wang, Y., & Hey, J. (2010). Estimating divergence parameters with small samples from a large number of loci. Genetics, 184, 363–379.PubMedGoogle Scholar
  160. Waxman, D., & Gavrilets, S. (2005a). 20 Questions on adaptive dynamics: a target review. Journal of Evolutionary Biology, 18, 1139–1154.PubMedGoogle Scholar
  161. Waxman, D., & Gavrilets, S. (2005b). Issues of terminology, gradient dynamics and the ease of sympatric speciation in adaptive dynamics. Journal of Evolutionary Biology, 18, 1214–1219.PubMedGoogle Scholar
  162. Weersing, K., & Toonen, R. J. (2010). Population genetics, larval dispersal, and connectivity in marine systems. Marine Ecology Progress Series, 393, 1–12.Google Scholar
  163. Wiley, E. O. (1978). The evolutionary species concept reconsidered. Systematic Zoology, 27, 17–26.Google Scholar
  164. Wiley, E. O., & Mayden, R. L. (2000a). The evolutionary species concept. In Q. D. Wheeler & R. Meiner (Eds.), Species concept and phylogenetic theory: A debate (pp. 70–89). New York: Columbia University Press.Google Scholar
  165. Wiley, E. O., & Mayden, R. L. (2000b). A critique from the evolutionary species concept perspective. In Q. D. Wheeler & R. Meiner (Eds.), Species concept and phylogenetic theory: A debate (pp. 146–158). New York: Columbia University Press.Google Scholar
  166. Wiley, E. O., & Mayden, R. L. (2000c). A defense of the evolutionary species concept. In Q. D. Wheeler & R. Meiner (Eds.), Species concept and phylogenetic theory: A debate (pp. 198–208). New York: Columbia University Press.Google Scholar
  167. Wood, T. E., Takebayashi, N., Barker, M. S., Mayrose, I., Greenspoon, P. B., & Rieseberg, L. H. (2009). The frequency of polyploid speciation in vascular plants. Proceedings of the National Academy of Sciences USA, 106, 13875–13879.Google Scholar
  168. Wright, S. (1940). The statistical consequences of Mendelian heredity in relation to speciation. In J. Huxley (Ed.), The new systematics (pp. 161–183). London: Oxford University Press.Google Scholar
  169. Wright, S. (1943). Isolation by distance. Genetics, 28, 114–138.PubMedGoogle Scholar
  170. Yatabe, Y., Kane, N. C., Scotti-Saintagne, C., & Rieseberg, L. H. (2007). Rampant gene exchange across a strong reproductive barrier between the annual sunflowers, Helianthus annuus and H. petiolaris. Genetics, 175, 1883–1893.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Christopher E. Bird
    • 1
    • 2
    Email author
  • Iria Fernandez-Silva
    • 2
  • Derek J. Skillings
    • 2
  • Robert J. Toonen
    • 2
  1. 1.Department of Life SciencesTexas A&M University-Corpus ChristiCorpus ChristiUSA
  2. 2.Hawai’i Institute of Marine BiologyUniversity of Hawai’iKāne’oheUSA

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