Abstract
Species are generally viewed by evolutionists as ‘real’ distinct entities in nature, making speciation appear difficult. Charles Darwin had originally promoted a very different uniformitarian view that biological species were continuous with ‘varieties’ below the level of species and became distinguishable from them only when divergent natural selection led to gaps in the distribution of morphology. This Darwinian view on species came under immediate attack, and the consensus among evolutionary biologists today appears to side more with the ideas of Ernst Mayr and Theodosius Dobzhansky, who argued 70 years ago that Darwin was wrong about species. Here, I show how recent genetic studies of supposedly well-behaved animals, such as insects and vertebrates, including our own species, have supported the existence of the Darwinian continuum between varieties and species. Below the level of species, there are well-defined ecological races, while above the level of species, hybridization still occurs, and may often lead to introgression and, sometimes, hybrid speciation. This continuum is evident, not only across vast geographical regions, but also locally in sympatry. The existence of this continuum provides good evidence for gradual evolution of species from ecological races and biotypes, to hybridizing species and, ultimately, to species that no longer cross. Continuity between varieties and species not only provides an excellent argument against creationism, but also gives insight into the process of speciation. The lack of a hiatus between species and ecological races suggests that speciation may occur, perhaps frequently, in sympatry, and the abundant intermediate stages suggest that it is happening all around us. Speciation is easy!
References
-
Abbott R.J& Comes H.P . 2007 Blowin' in the wind: the transition from ecotype to species. New Phytol. 175, 197–200.doi:10.1111/j.1469-8137.2007.02127.x. . Crossref, PubMed, Web of Science, Google Scholar -
Abrahamson W.G& Blair C.P Sequential radiation through host-race formation: herbivore diversity leads to diversity in natural enemies. Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects& Tilmon K.J . 2007pp. 188–202. Eds. Berkeley, CA:University of California Press. Google Scholar -
Alipaz J.A, Wu C.I& Karr T.L . 2001 Gametic incompatibilities between races of Drosophila melanogaster. Proc. R. Soc. B. 268, 789–795.doi:10.1098/rspb.2000.1420. . Link, Web of Science, Google Scholar -
Anderson T.J.C, Romero-Abal M.E& Jaenike J . 1995 Mitochondrial DNA and Ascaris epidemiology: the composition of parasite populations from individual hosts, families and villages. Parasitology. 110, 221–229. Crossref, PubMed, Web of Science, Google Scholar -
Arnold M.L Natural hybridization and evolution. 1997 Oxford, UK:Oxford University Press. Google Scholar -
Aubert J, Barascud B, Descimon H& Michel F . 1997 Ecology and genetics of interspecific hybridization in the swallowtails, Papilio hospiton Géné and P. machaon L., in Corsica (Lepidoptera: Papilionidae). Biol. J. Linn. Soc. 60, 467–492. Web of Science, Google Scholar -
Barton N.H& Hewitt G.M . 1989 Adaptation, speciation and hybrid zones. Nature. 341, 497–503.doi:10.1038/341497a0. . Crossref, PubMed, Web of Science, Google Scholar -
Baum D . 1992 Phylogenetic species concepts. Trends Ecol. Evol. 7, 1–2.doi:10.1016/0169-5347(92)90187-G. . Crossref, PubMed, Web of Science, Google Scholar -
Baum D.A& Shaw K.L Genealogical perspectives on the species problem. Experimental and molecular approaches to plant biosystematics& Hoch P.C . 1995pp. 289–303. Eds. St. Louis, MI:Missouri Botanical Garden. Google Scholar -
Bell M.A& Foster S.A The evolutionary biology of the threespine stickleback. 1994 Oxford, UK:Oxford University Press. Google Scholar -
Benkman C.W . 2003 Divergent selection causes the adaptive radiation of crossbills. Evolution. 57, 1176–1181.doi:10.1554/0014-3820(2003)057[1176:DSDTAR]2.0.CO;2. . Crossref, PubMed, Web of Science, Google Scholar -
Berlocher S.H& Feder J.L . 2002 Sympatric speciation in phytophagous insects: moving beyond controversy?. Annu. Rev. Entomol. 47, 773–815.doi:10.1146/annurev.ento.47.091201.145312. . Crossref, PubMed, Web of Science, Google Scholar -
Bérubé M& Aguilar A . 1998 A new hybrid between a blue whale, Balaenoptera musculus, and a fin whale, B. physalus: frequency and implications of hybridization. Mar. Mamm. Sci. 14, 82–98.doi:10.1111/j.1748-7692.1998.tb00692.x. . Crossref, Web of Science, Google Scholar -
Bolnick D.I& Fitzpatrick B.M . 2007 Sympatric speciation: models and empirical evidence. Annu. Rev. Ecol. Evol. Syst. 38, 459–487.doi:10.1146/annurev.ecolsys.38.091206.095804. . Crossref, Web of Science, Google Scholar -
Bolnick D.I& Near T.J . 2005 Tempo of hybrid inviability in centrarchid fishes (Teleostei: Centrarchidae). Evolution. 59, 1754–1767.doi:10.1554/04-563.1. . Crossref, PubMed, Web of Science, Google Scholar -
Bull V, Beltrán M, Jiggins C.D, McMillan W.O, Bermingham E& Mallet J . 2006 Polyphyly and gene flow between non-sibling Heliconius species. BMC Biol. 4, 11 doi:10.1186/1741-7007-4-11. . Crossref, PubMed, Web of Science, Google Scholar -
Butlin R.K, Galindo J& Grahame J.W . 2008 Sympatric, parapatric or allopatric: the most important way to classify speciation?. Phil. Trans. R. Soc. B. 363, 2997–3007.doi:10.1098/rstb.2008.0076. . Link, Web of Science, Google Scholar -
Capy P, Veuille M, Paillette M, Jallon J.M, Vouidibio J& David J.R . 2000 Sexual isolation of genetically differentiated sympatric populations of Drosophila melanogaster in Brazzaville, Congo: the first step towards speciation?. Heredity. 84, 468–475.doi:10.1046/j.1365-2540.2000.00711.x. . Crossref, PubMed, Web of Science, Google Scholar -
Cianchi R, Ungaro A, Marini M& Bullini L . 2003 Differential patterns of hybridization and introgression between the swallowtails Papilio machaon and P. hospiton from Sardinia and Corsica islands (Lepidoptera, Papilionidae). Mol. Ecol. 12, 1461–1471.doi:10.1046/j.1365-294X.2003.01813.x. . Crossref, PubMed, Web of Science, Google Scholar -
Coyne J.A& Orr H.A . 1997 “Patterns of speciation in Drosophila” revisited. Evolution. 51, 295–303.doi:10.2307/2410984. . PubMed, Web of Science, Google Scholar -
Cracraft J Speciation and its ontology: the empirical consequences of alternative species concepts for understanding patterns and processes of differentiation. Speciation and its consequences& Otte D . 1989pp. 28–59. Eds. Sunderland, MA:Sinauer Associates. Google Scholar -
Cruz R, Vilas C, Mosquera J& García C . 2004 Relative contribution of dispersal and natural selection to the maintenance of a hybrid zone in Littorina. Evolution. 58, 2734–2746.doi:10.1111/j.0014-3820.2004.tb01625.x. . Crossref, PubMed, Web of Science, Google Scholar -
Dalby J.E . 1997 Reproductive and electrophoretic evidence for genetic maintenance of dimorphism in the ascidian Pyura stolonifera near Melbourne, Australia. Ophelia. 47, 227–243. Crossref, Google Scholar -
Darwin C On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. 1859 London, UK:John Murray. Google Scholar -
Dasmahapatra K.K, Silva A, Chung J.-W& Mallet J . 2007 Genetic analysis of a wild-caught hybrid between non-sister Heliconius butterfly species. Biol. Lett. 3, 660–663.doi:10.1098/rsbl.2007.0401. . Link, Web of Science, Google Scholar -
Descimon H& Mallet J Bad species. Ecology and evolution of European butterflies& Shreeve T.G . 2008 London, UK:Oxford University Press. Google Scholar -
Dieckmann U& Doebeli M . 1999 On the origin of species by sympatric speciation. Nature. 400, 354–357.doi:10.1038/22521. . Crossref, PubMed, Web of Science, Google Scholar -
Dobzhansky T Genetics and the origin of species. 1937 New York, NY:Columbia University Press. Google Scholar -
Dopman E.B, Perez L, Bogdanowicz S.M& Harrison R.G . 2005 Consequences of reproductive barriers for genealogical discordance in the European corn borer. Proc. Natl Acad. Sci. USA. 102, 14 706–14 711.doi:10.1073/pnas.0502054102. . Crossref, Web of Science, Google Scholar -
Drès M& Mallet J . 2002 Host races in plant-feeding insects and their importance in sympatric speciation. Phil. Trans. R. Soc. B. 357, 471–492.doi:10.1098/rstb.2002.1059. . Link, Web of Science, Google Scholar -
Eldredge N& Gould S.J Punctuated equilibria: an alternative to phyletic gradualism. Models in paleobiology& Schopf T.J.M . 1972pp. 82–115. Eds. San Francisco, CA:Freeman, Cooper, & Co. Google Scholar -
Ellstrand N.C, Whitkus R& Rieseberg L.H . 1996 Distribution of spontaneous plant hybrids. Proc. Natl Acad. Sci. USA. 93, 5090–5093.doi:10.1073/pnas.93.10.5090. . Crossref, PubMed, Web of Science, Google Scholar -
Feder J.L The apple maggot fly, Rhagoletis pomonella: flies in the face of conventional wisdom. Endless forms. Species and speciation& Howard D.J . 1998pp. 130–144. Eds. New York, NY:Oxford University Press. Google Scholar -
Felsenstein J . 1981 Skepticism towards Santa Rosalia, or why are there so few kinds of animals?. Evolution. 35, 124–138.doi:10.2307/2407946. . Crossref, PubMed, Web of Science, Google Scholar -
Foltz D.W . 1997 Hybridization frequency is negatively correlated with divergence time of mitochondrial DNA haplotypes in a sea star (Leptasterias spp.) species complex. Evolution. 51, 283–288.doi:10.2307/2410982. . Crossref, PubMed, Web of Science, Google Scholar -
Ford J.K.B, Ellis G.M, Barrett-Lennard L.G, Morton A.B, Palm R.S& Balcomb K.C . 1998 Dietary specialization in two sympatric populations of killer whales (Orcinus orca) in coastal British Columbia and adjacent waters. Can. J. Zool. 76, 1456–1471.doi:10.1139/cjz-76-8-1456. . Crossref, Web of Science, Google Scholar -
Gavrilets S . 2003 Models of speciation: what have we learned in 40 years?. Evolution. 57, 2197–2215. Crossref, PubMed, Web of Science, Google Scholar -
Gompert Z, Fordyce J.A, Forister M, Shapiro A.M& Nice C.C . 2006 Homoploid hybrid speciation in an extreme habitat. Science. 314, 1923–1925.doi:10.1126/science.1135875. . Crossref, PubMed, Web of Science, Google Scholar -
Gould S.J . 1980 Is a new and general theory of evolution emerging?. Paleobiology. 6, 119–130. Crossref, Web of Science, Google Scholar -
Gourbiere, S. & Mallet, J. In press. Meta-analysis of incompatibility between species. Exponential failure, reinforcement, and the ‘missing snowball’. Evolution. Google Scholar
-
Grant P.R& Grant B.R . 1992 Hybridization of bird species. Science. 256, 193–197.doi:10.1126/science.256.5054.193. . Crossref, PubMed, Web of Science, Google Scholar -
Grant P.R& Grant B.R . 1996 Speciation and hybridization in island birds. Phil. Trans. R. Soc. B. 351, 765–772.doi:10.1098/rstb.1996.0071. . Link, Web of Science, Google Scholar -
Grant P.R& Grant B.R How and why species multiply. The radiation of Darwin's finches. 2008 Princeton, NJ:Princeton University Press. Google Scholar -
Haerty W, Lesbats M& Capy P . 2005 Pre-reproductive isolation as a consequence of allopatric differentiation between populations of Drosophila melanogaster. Mol. Ecol. 14, 3801–3807.doi:10.1111/j.1365-294X.2005.02688.x. . Crossref, PubMed, Web of Science, Google Scholar -
Harrison R.G Linking evolutionary pattern and process. The relevance of species concepts for the study of speciation. Endless Forms. Species and speciation& Howard D.J . 1998pp. 19–31. Eds. New York, NY:Oxford University Press. Google Scholar -
Hegarty M.J, Barker G.L, Brennan A.C, Edwards K.J, Abbott R.J& Hiscock S.J . 2008 Changes to gene expression associated with hybrid speciation in plants: further insights from transcriptomic studies in Senecio. Phil. Trans. R. Soc. B. 363, 3055–3069.doi:10.1098/rstb.2008.0080. . Link, Web of Science, Google Scholar -
Heide-Jorgensen M.P& Reeves R.R . 1993 Description of an anomalous monodontid skull from West Greenland — a possible hybrid. Mar. Mamm. Sci. 9, 258–268.doi:10.1111/j.1748-7692.1993.tb00454.x. . Crossref, Web of Science, Google Scholar -
Hennig W Elementos de una Sistemática Filogenética (Translation of Grundzüge einer Theorie der phylogenetischen Systematik). 1968 Buenos Aires, Argentina:Editorial Universitaria de Buenos Aires. Google Scholar -
Hoelzel A.R, Hey J, Dahlheim M.E, Nicholson C, Burkanov V& Black N . 2007 Evolution of population structure in a highly social top predator, the killer whale. Mol. Biol. Evol. 24, 1407–1415.doi:10.1093/molbev/msm063. . Crossref, PubMed, Web of Science, Google Scholar -
Hollocher H, Ting C.T, Pollack F& Wu C.I . 1997 Incipient speciation by sexual isolation in Drosophila melanogaster: variation in mating preference and correlation between sexes. Evolution. 51, 1175–1181.doi:10.2307/2411047. . PubMed, Web of Science, Google Scholar -
Huxley, T. H. 1860 The origin of species. In Collected essays. “Lectures to Working Men” (Republished 1899), pp. 22–79. London, UK: Macmillan & Co., Ltd. Google Scholar
-
Isaac N.J.B, Mallet J& Mace G.M . 2004 Taxonomic inflation: its influence on macroecology and conservation. Trends Ecol. Evol. 19, 464–469.doi:10.1016/j.tree.2004.06.004. . Crossref, PubMed, Web of Science, Google Scholar -
Jakobsson M, 2008 Genotype, haplotype and copy-number variation in worldwide human populations. Nature. 451, 998–1003.doi:10.1038/nature06742. . Crossref, PubMed, Web of Science, Google Scholar -
Jiggins C.D& Mallet J . 2000 Bimodal hybrid zones and speciation. Trends Ecol. Evol. 15, 250–255.doi:10.1016/S0169-5347(00)01873-5. . Crossref, PubMed, Web of Science, Google Scholar -
Jiggins C.D, Salazar C, Linares M& Mavarez J . 2008 Hybrid trait speciation and Heliconius butterflies. Phil. Trans. R. Soc. B. 363, 3047–3054.doi:10.1098/rstb.2008.0065. . Link, Web of Science, Google Scholar -
Johannesson K, Johannesson B& Rolán-Alvarez E . 1993 Morphological differentiation and genetic cohesiveness over a microenvironmental gradient in the marine snail Littorina saxatilis. Evolution. 47, 1770–1787.doi:10.2307/2410220. . Crossref, PubMed, Web of Science, Google Scholar -
Jonsson B& Jonsson N . 2001 Polymorphism and speciation in Arctic charr. J. Fish Biol. 58, 605–638.doi:10.1111/j.1095-8649.2001.tb00518.x. . Crossref, Web of Science, Google Scholar -
Kauer M.O& Schlotterer C . 2004 An analysis of genetic differentiation among assortatively mating Drosophila melanogaster in Zimbabwe. J. Evol. Biol. 17, 493–500.doi:10.1111/j.1420-9101.2004.00709.x. . Crossref, PubMed, Web of Science, Google Scholar -
Kittler R, Kayser M& Stoneking M . 2003 Molecular evolution of Pediculus humanus and the origin of clothing. Curr. Biol. 13, 1414–1417.doi:10.1016/S0960-9822(03)00507-4. . Crossref, PubMed, Web of Science, Google Scholar -
Knudsen R, Klemetsen A, Amundsen P.A& Hermansen B . 2006 Incipient speciation through niche expansion: an example from the Arctic charr in a subarctic lake. Proc. R. Soc. B. 273, 2291–2298.doi:10.1098/rspb.2006.3582. . Link, Web of Science, Google Scholar -
Kondrashov A.S& Kondrashov F.A . 1999 Interactions among quantitative traits in the course of sympatric speciation. Nature. 400, 351–354.doi:10.1038/22514. . Crossref, PubMed, Web of Science, Google Scholar -
Kondrashov A.S& Mina M.V . 1986 Sympatric speciation: when is it possible?. Biol. J. Linn. Soc. 27, 201–223.doi:10.1111/j.1095-8312.1986.tb01734.x. . Crossref, Web of Science, Google Scholar -
Kronforst M.R, Young L.G, Blume L.M& Gilbert L.E . 2006 Multilocus analysis of admixture and introgression among hybridizing Heliconius butterflies. Evolution. 60, 1254–1268.doi:10.1554/06-005.1. . Crossref, PubMed, Web of Science, Google Scholar -
Leo N.P, Campbell N.J.H, Yang X, Mumcuoglu K& Barker S.C . 2002 Evidence from mitochondrial DNA that head lice and body lice of humans (Phthiraptera: Pediculidae) are conspecific. J. Med. Entomol. 39, 662–666. Crossref, PubMed, Web of Science, Google Scholar -
Lexer C& Widmer A . 2008 The genic view of plant speciation: recent progress and emerging questions. Phil. Trans. R. Soc. B. 363, 3023–3036.doi:10.1098/rstb.2008.0078. . Link, Web of Science, Google Scholar -
Liti G, Barton D.B.H& Louis E.J . 2006 Sequence diversity, reproductive isolation and species concepts in Saccharomyces. Genetics. 174, 839–850.doi:10.1534/genetics.106.062166. . Crossref, PubMed, Web of Science, Google Scholar -
Lowry D.B, Modliszewski J.L, Wright K.M, Wu C.A& Willis J.H . 2008 The strength and genetic basis of reproductive isolating barriers in flowering plants. Phil. Trans. R. Soc. B. 363, 3009–3022.doi:10.1098/rstb.2008.0064. . Link, Web of Science, Google Scholar -
Lu G& Bernatchez L . 1999 Correlated trophic specialization and genetic divergence in sympatric lake whitefish ecotypes (Coregonus clupeaformis): support for the ecological speciation hypothesis. Evolution. 53, 1491–1505.doi:10.2307/2640895. . PubMed, Web of Science, Google Scholar -
MacDonald D& Barrett P European mammals. Evolution and behaviour. 1995 London, UK:HarperCollins. Google Scholar -
Machado C.A, Kliman R.M, Markert J.A& Hey J . 2002 Inferring the history of speciation from multilocus DNA sequence data: the case of Drosophila pseudoobscura and its close relatives. Mol. Biol. Evol. 19, 472–488. Crossref, PubMed, Web of Science, Google Scholar -
Malausa T, Leniaud L, Martin J.-F, Audiot P, Bourguet D, Ponsard S, Lee S.-F, Harrison R.G& Dopman E.B . 2006 Molecular differentiation at nuclear loci in French host races of the European Corn Borer (Ostrinia nubilalis). Genetics. 176, 2343–2355.doi:10.1534/genetics.107.072108. . Crossref, Web of Science, Google Scholar -
Mallet J . 1995 A species definition for the modern synthesis. Trends Ecol. Evol. 10, 294–299.doi:10.1016/0169-5347(95)90031-4. . Crossref, PubMed, Web of Science, Google Scholar -
Mallet J . 2004 Poulton, Wallace and Jordan: how discoveries in Papilio butterflies initiated a new species concept 100 years ago. Syst. Biodiv. 1, 441–452.doi:10.1017/S1477200003001300. . Crossref, Google Scholar -
Mallet J . 2005 Hybridization as an invasion of the genome. Trends Ecol. Evol. 20, 229–237.doi:10.1016/j.tree.2005.02.010. . Crossref, PubMed, Web of Science, Google Scholar -
Mallet J . 2007 Hybrid speciation. Nature. 446, 279–283.doi:10.1038/nature05706. . Crossref, PubMed, Web of Science, Google Scholar -
Mallet, J. In press a. Mayr's view of Darwin: was Darwin wrong about speciation? Biol. J. Linn. Soc. Google Scholar
-
Mallet J Rapid speciation, hybridization and adaptive radiation in the Heliconius melpomene group. Speciation and ecology p. 000 Eds., Butlin R.K, Schluter D& Bridle J.R . (In press). Google Scholar -
Mallet J Wallace and the species concept of the early Darwinians. Natural selection and beyond: the intellectual legacy of Alfred Russell Wallace, Smith C.R& Beccaloni G.W . In press Oxford, UK:Oxford University Press. Google Scholar -
Mallet J, Beltrán M, Neukirchen W& Linares M . 2007 Natural hybridization in heliconiine butterflies: the species boundary as a continuum. BMC Evol. Biol. 7, 28 doi:10.1186/1471-2148-7-28. . Crossref, PubMed, Web of Science, Google Scholar -
Mavárez J, Salazar C, Bermingham E, Salcedo C, Jiggins C.D& Linares M . 2006 Speciation by hybridization in Heliconius butterflies. Nature. 441, 868–871.doi:10.1038/nature04738. . Crossref, PubMed, Web of Science, Google Scholar -
Maynard Smith J . 1966 Sympatric speciation. Am. Nat. 100, 637–650.doi:10.1086/282457. . Crossref, Web of Science, Google Scholar -
Mayr E Systematics and origin of species. 1942 New York, NY:Columbia University Press. Google Scholar -
Mayr E Prologue: some thoughts on the history of the evolutionary synthesis. The evolutionary synthesis. Perspectives on the unification of biology, Mayr E& Provine W.B . 1981pp. 1–48. Eds. Cambridge, MA:Harvard University Press. Google Scholar -
Mayr E The growth of biological thought. Diversity, evolution, and inheritance. 1982 Cambridge, MA:Belknap. Google Scholar -
Mayr E . 1992 A local flora and the biological species concept. Am. J. Bot. 79, 222–238.doi:10.2307/2445111. . Crossref, Web of Science, Google Scholar -
Natoli A, Peddemors V.M& Hoelzel A.R . 2004 Population structure and speciation in the genus Tursiops based on microsatellite and mitochondrial DNA analyses. J. Evol. Biol. 17, 363–375.doi:10.1046/j.1420-9101.2003.00672.x. . Crossref, PubMed, Web of Science, Google Scholar -
Nolte A.W, Freyhof J, Stemshorn K.C& Tautz D . 2005 An invasive lineage of sculpins, Cottus sp. (Pisces, Teleostei) in the Rhine with new habitat adaptations has originated from hybridization between old phylogeographic groups. Proc. R. Soc. B. 272, 2379–2387.doi:10.1098/rspb.2005.3231. . Link, Web of Science, Google Scholar -
Noor M.A.F, Johnson N.A& Hey J . 2000 Gene flow between Drosophila pseudoobscura and D. persimilis. Evolution. 54, 2174–2175.doi:10.1111/j.0014-3820.2000.tb01262.x. . Crossref, PubMed, Web of Science, Google Scholar -
Otto S.P& Whitton J . 2000 Polyploid incidence and evolution. Annu. Rev. Genet. 34, 401–437.doi:10.1146/annurev.genet.34.1.401. . Crossref, PubMed, Web of Science, Google Scholar -
Papadopoulou A, Bergsten J, Fujisawa T, Monaghan M.T, Barraclough T.G& Vogler A.P . 2008 Speciation and DNA barcodes: testing the effects of dispersal on the formation of discrete sequence clusters. Phil. Trans. R. Soc. B. 363, 2987–2996.doi:10.1098/rstb.2008.0066. . Link, Web of Science, Google Scholar -
Parmenter T& Byers C A guide to the Warblers of the Western Palaearctic. 1991 Uxbridge, UK:Bruce Coleman. Google Scholar -
Poulton, E. B. 1904 What is a species? Proc. Entomol. Soc. Lond. 1903, lxxvii–cxvi. Google Scholar
-
Presgraves D.C . 2002 Patterns of postzygotic isolation in Lepidoptera. Evolution. 56, 1168–1183.doi:10.1111/j.0014-3820.2002.tb01430.x. . Crossref, PubMed, Web of Science, Google Scholar -
Price T.D& Bouvier M.M . 2002 The evolution of F1 postzygotic incompatibilities in birds. Evolution. 56, 2083–2089. Crossref, PubMed, Web of Science, Google Scholar -
Quicke D.L.J, Donoghue A.M& Brace R.C . 1983 Biochemical-genetic and ecological evidence that red/brown individuals of the anemone Actinia equina comprise two morphs in Britain. Mar. Biol. 77, 29–37.doi:10.1007/BF00393207. . Crossref, Web of Science, Google Scholar -
Quintana-Murci L, 2008 Maternal traces of deep common ancestry and asymmetric gene flow between Pygmy hunter-gatherers and Bantu-speaking farmers. Proc. Natl Acad. Sci. USA. 105, 1596–1601.doi:10.1073/pnas.0711467105. . Crossref, PubMed, Web of Science, Google Scholar -
Ramsey J& Schemske D.W . 2002 Neopolyploidy in flowering plants. Annu. Rev. Ecol. Syst. 33, 589–639.doi:10.1146/annurev.ecolsys.33.010802.150437. . Crossref, Google Scholar -
Raven P.H . 1976 Systematics and plant population biology. Syst. Bot. 1, 284–316.doi:10.2307/2418721. . Crossref, Google Scholar -
Reed D.L, Smith V.S, Hammond S.L, Rogers A.R& Clayton D.H . 2004 Genetic analysis of lice supports direct contact between modern and archaic humans. PLoS Biol. 2, e340 doi:10.1371/journal.pbio.0020340. . Crossref, PubMed, Web of Science, Google Scholar -
Rieseberg L.H . 1997 Hybrid origins of plant species. Annu. Rev. Ecol. Syst. 28, 359–389.doi:10.1146/annurev.ecolsys.28.1.359. . Crossref, Google Scholar -
Rieseberg L.H, Raymond O, Rosenthal D.M, Lai Z& Livingstone K . 2003 Major ecological transitions in wild sunflowers facilitated by hybridization. Science. 301, 1211–1216.doi:10.1126/science.1086949. . Crossref, PubMed, Web of Science, Google Scholar -
Roach, J. 2006 Grizzly-polar bear hybrid found — but what does it mean? National Geographic News. Google Scholar
-
Romanes G.J . 1886 Physiological selection; an additional suggestion on the origin of species. J. Linn. Soc. Zool. 19, 337–411.doi:10.1111/j.1096-3642.1886.tb01869.x. . Crossref, Google Scholar -
Sasa M.M, Chippindale P.T& Johnson N.A . 1998 Patterns of postzygotic isolation in frogs. Evolution. 52, 1811–1820.doi:10.2307/2411351. . Crossref, PubMed, Web of Science, Google Scholar -
Schluter D& Nagel L.M . 1995 Parallel speciation by natural selection. Am. Nat. 146, 292–301.doi:10.1086/285799. . Crossref, Web of Science, Google Scholar -
Seehausen O . 2004 Hybridization and adaptive radiation. Trends Ecol. Evol. 19, 198–207.doi:10.1016/j.tree.2004.01.003. . Crossref, PubMed, Web of Science, Google Scholar -
Skulason S& Smith T.B . 1995 Resource polymorphisms in vertebrates. Trends Ecol. Evol. 10, 366–370.doi:10.1016/S0169-5347(00)89135-1. . Crossref, PubMed, Web of Science, Google Scholar -
Smith J.W& Benkman C.W . 2007 A coevolutionary arms race causes ecological speciation in crossbills. Am. Nat. 169, 455–465.doi:10.1086/511961. . Crossref, PubMed, Web of Science, Google Scholar -
Sokal R.R& Crovello T.J . 1970 The biological species concept: a critical evaluation. Am. Nat. 104, 107–123.doi:10.1086/282646. . Crossref, Web of Science, Google Scholar -
Solecava A.M& Thorpe J.P . 1992 Genetic divergence between color morphs in populations of the common intertidal sea anemones Actinia equina and A. prasina (Anthozoa, Actiniaria) in the Isle of Man. Mar Biol. 112, 243–252.doi:10.1007/BF00702468. . Crossref, Web of Science, Google Scholar -
Soltis D.E, Soltis P.S& Tate J.A . 2004 Advances in the study of polyploidy since plant speciation. New Phytol. 161, 173–191.doi:10.1046/j.1469-8137.2003.00948.x. . Crossref, Web of Science, Google Scholar -
Soltis D.E, Soltis P.S, Schemske D.W, Hancock J.F, Thompson J.N, Husband B.C& Judd W.S . 2007 Autopolyploidy in angiosperms: have we grossly underestimated the number of species?. Taxon. 56, 13–30. Web of Science, Google Scholar -
Spilliaert R, Vikingsson G, Arnason U, Pálsdóttir A, Sigurjónsson J& Arnason A . 1991 Species hybridization between a female blue whale (Balaenoptera musculus) and a male fin whale (B. physalus): molecular and morphological identification. J. Hered. 82, 269–274. Crossref, PubMed, Web of Science, Google Scholar -
Stace C.A Hybridization and the flora of the British Isles. 1975 London, UK:Academic Press. Google Scholar -
Stace C.A The new flora of the British Isles. 1997 Cambridge, UK:Cambridge University Press. Google Scholar -
Stebbins G.L Variation and evolution in plants. 1950 New York, NY:Columbia University Press. Google Scholar -
Stebbins G.L . 1959 The role of hybridization in evolution. Proc. Am. Philos. Soc. 103, 231–251. Google Scholar -
Sylvestre J.-P& Tasaka S . 1985 On the intergeneric hybrids in cetaceans. Aquatic Mamm. 11, 101–108. Google Scholar -
Tripet F, Touré Y.T, Taylor C.E, Norris D.E, Dolo G& Lanzaro G.C . 2001 DNA analysis of transferred sperm reveals significant levels of gene flow between molecular forms of Anopheles gambiae. Mol. Ecol. 10, 1725–1732.doi:10.1046/j.0962-1083.2001.01301.x. . Crossref, PubMed, Web of Science, Google Scholar -
Turelli M& Moyle L.G . 2007 Asymmetric postmating isolation: Darwin's corollary to Haldane's Rule. Genetics. 176, 1059–1088.doi:10.1534/genetics.106.065979. . Crossref, PubMed, Web of Science, Google Scholar -
Turelli M& Orr H.A . 1995 The dominance theory of Haldane's rule. Genetics. 140, 389–402. Crossref, PubMed, Web of Science, Google Scholar -
Turner T.L, Hahn M.W& Nuzhdin S.V . 2005 Genomic islands of speciation in Anopheles gambiae. PLoS Biol. 3, e285 doi:10.1371/journal.pbio.0030285. . Crossref, PubMed, Web of Science, Google Scholar -
Wallace A.R . 1865 On the phenomena of variation and geographical distribution as illustrated by the Papilionidae of the Malayan region. Trans. Linn. Soc. Lond. 25, 1–71. Crossref, Google Scholar -
Wallace A.R Darwinism. An exposition of the theory of natural selection with some of its applications. 1889 London, UK:Macmillan & Co. Google Scholar -
Wang J.Y, Chou L.S& White B.N . 1999 Mitochondrial DNA analysis of sympatric morphotypes of bottlenose dolphins (genus: Tursiops) in Chinese waters. Mol. Ecol. 8, 1603–1612.doi:10.1046/j.1365-294x.1999.00741.x. . Crossref, PubMed, Web of Science, Google Scholar -
Watts P.C& Thorpe J.P . 1998 Phenotypic identification of three genetically differentiated morphs of the intertidal beadlet anemone Actinia equina (Anthozoa: Cnidaria). J. Mar. Biol. Assoc. UK. 78, 1365–1368. Crossref, Google Scholar -
Wilding C.S, Butlin R.K& Grahame J . 2001 Differential gene exchange between parapatric morphs of Littorina saxatilis detected using AFLP markers. J. Evol. Biol. 14, 611–619.doi:10.1046/j.1420-9101.2001.00304.x. . Crossref, Web of Science, Google Scholar -
Willis P.M, Crespi B.J, Dill L.M, Baird R.W& Hanson M.B . 2004 Natural hybridization between Dall's porpoises (Phocoenoides dalli) and harbour porpoises (Phocoena phocoena). Can. J. Zool. 82, 828–834.doi:10.1139/z04-059. . Crossref, Web of Science, Google Scholar -
Wu C.I, Hollocher H, Begun D.J, Aquadro C.F, Xu Y& Wu M.L . 1995 Sexual isolation in Drosophila melanogaster: a possible case of incipient speciation. Proc. Natl Acad. Sci. USA. 92, 2519–2523.doi:10.1073/pnas.92.7.2519. . Crossref, PubMed, Web of Science, Google Scholar -
Zawadzki P, Roberts M.S& Cohan F.M . 1995 The log-linear relationship between sexual isolation and sequence divergence in Bacillus is robust. Genetics. 140, 917–932. Crossref, PubMed, Web of Science, Google Scholar -
Zink R.M . 2002 A new perspective on the evolutionary history of Darwin's finches. Auk. 119, 864–871.doi:10.1642/0004-8038(2002)119[0864:ANPOTE]2.0.CO;2. . Crossref, Web of Science, Google Scholar