PERSPECTIVES that the availability of ecological niches or appear in the fossil record at approximately 16. Jaillon, 0. et a. The grapevine genome e o lant ancestors18592-9. Therefore, we argue of pollinating insects, Lepidoptera and bees, 15. Tang. H et and collinear seque severely perturbed ecosystems could be the the same time as angiosperms. 100. Early single most important determinant for angiosperm polyploidizations occurring 17. Scannell, D. R, Butler, G. Wolfe, K. H. Yeast genome the survival and long-term evolutionary at this time might have helped plants to tion- the origin of the species. Yeast 24 success of a WGD conquer these newly unclosed niches. 18. Dehal, P. Boore, J. L. Two rounds of whole geno Mass extinctions are among the most It may prove difficult to determine drastic events by which old or new niches hether polyploidy enabled organisms to 19. Putnam, N H et al. The amphioxus genome and the become available for colonization(FIG. le, f). survive extinctions or whether polyploidy evolution of the chordate karyotype. Nature 453 WGDs occurring close to these extinc facilitated evolutionary transitions and 20. Jaillon, O et a. Genome duplication in the teleost fish tions probably contributed to the radia increased biological complexity. Sequencing tion of vertebrates in the Cambrian period more genomes and \ ols that proto-karyotype. Nature 431,946-957(2004) A. a Van de peer. y from 2F and of several angiosperm families at the are more able to detect and correctly date K-Tboundary. The K-T mass extinction ncient polyploidy events may unveil corre- 22. Crow, K D. Wagner, G P wi might also have played an important part in lations between polyploidy and evolutionary 2 unlocking the diversification potential of 3r changes that are currently unknown, and in teleosts, even >150 million years after studying the gene aining after a WGD 3R occurred. Conversely, the reason why the and their interactors at a systems level may ends Eco. Evol. 20, 312-319(2005 awcett, J.A. Maere, S. Van de Peer, Y Plants with teleosts did not diversify right after the P-t provide clues as to why polyploids occasion double genomes might have had a better chance to mass extinction may have been because the ally might have had a selective advantage Proc. Nat Acad. SC. USA 106, 5737-5742(2001 few survivors from the Triassic period still over their diploid sister species 25. Levin, D. A Polyploidy and novelty in flowering plants occupied most of the relevant niche space However, new niches may also become wes available through biotic evolution. For instance, the rise of angiosperm plants led to B9052 Ghent, Belgium, and the Bioinformatics and mE730=307092 the emergence of sugar-rich fruits. Conant Evolutionary Genomics research group,Department of d role in the evolution of autopolyploid plants. New Phytol. 129, 1-22(1995) and Wolfe have suggested that the success Plant Biotechnology and Genetics, Ghent University, 28. Osborn, T C et al. Understanding mechanisms of of the genome duplication in budding yeast, B9052 Ghent, Belgum. pression in polyploids. Tends Genet. 19 approximately 100 mya, may be linked to Axe! Meyer is at the Department of Biology, University 29. Rieseberg, L H et al. Hybridization and the the emergence of this new ecological niche They showed that the retention of glycolytic Institute for Advanced Study, WallotstraBe 19 D-14193 Berlin, Germany. 50. Rieseberg, L.H. et al. Major ecological transitions in pathway genes after the WGD in yeasts sup by hybridization. Science ported an increase in glycolytic flux that gave Correspondence to y..dP e-mail: yes. Vandepeergpsh yib-ugent he post-WGD yeast species a growth advantage in glucose-rich environments (FIG. Ic, d) doi:10.1038mrg2600 Lond B 363 The angiosperms also did not rise Published online 4 August 2009 32. Ellstran ecological dominance by filling niches that 1. Masterston,J Stomatal size in fossil plants: evidence Proc. Nat! Acad. Sci. USA 97.70 event". It is possible that angiosperms filled 2 264,.421-423( 994). widespread pale ist became available after a mass extinction or poly ploidy in majority of angiosperms. Science 33. Pandit, M. K, Tan, H. T w.& Bisht, M.S. Polyploidy in ve plant species of Singapore. Bot. J. Linn. Soc. of duplicate genes. Plant Ce 16. sage dis 34. Soltis, D. E, Soltis, P.S. existed but that had remained largely unoc- 3.Tang.Het al udy of polyploidy since plant speciation. New Phytol veling ancient hexaploidy th upied because the necessary phenotypic giosperm gene maps. Genome Res. 35. Lokki, J characteristics had not yet been developed 4. Cui. L et al. widespread) Basic Life Sci. 13. 277-312 spread genome duplications (FIG 1a, b). Specifically, angiosperm-insect EmMD1.21002m由解中 36. Weldon, C, du Preez, L H, Hyatt, A. D, Muller, Spears, R Origin of interactions may have been important in 5. Ramsey, J. Schemske. D. W. Pathways, mechanisms, 37. Parker, J M, Mikaelian, I, Hahn, N. Diggs, H.E. angiosperm niche diversification. Although insect pollination evolved in several nor angiosperm plants, such as Welwitschia 6. otto,SP&Whitton,J.Pol 34.401-437(200 in evolutionary success Curr Biol. 17, R97-R929". mirabilis(a gnetophyte), angiosperms devel. 7. Soltis p s &soltis, D E. The role of hyb ant speciation. Annu. Rev. Pf oped several innovations that dramatically l, R A o Koltunow, A M. Understanding increased the effectiveness of insect pol ancient duplication of the entire yeast genome. conundrums. Plant Cell 16, $228-5245(2004]. lination, such as the association of male and female reproductive organs on the same axis 9.Aury.JMet al.Global trends of whole-genome illuminates vertebrate origins and cephalochordate and the development of colourful perianth 10. Wittbrodt, Meyer,A schartl,M. More 41. xiao, s. Laflamme, M. On the eve of animal tion over large distances, which might have 12. polyploidy Cell 131. 452-462(2007 ' in organs"bss. These specialized angiosperm diacar release to surface enabled angiosperm plants to colonize previ ously unoccupied habitats, such as dispersed 13. Soltis, D.E.et al. Polyploidy and 43. Knoll, A H. Carroll, S. B. Early animal evolution from comparative biology and geology. microhabitats, or disturbed or resource-poor habitats. Indeed, some of the major classes rigin and early evolution of angiosperms. Ann. NY Acad.sai1133,3-2502008 A new time scale for ray-finned fish olution. Proc R Soc. B274, 489-498(2007) NATURE REVIEWS GENETICS VOLUME 10 lOCTOBER 20091731 22009 Macmillan Publishers Limited All rights reservedancestors11,85,92–95. Therefore, we argue that the availability of ecological niches or severely perturbed ecosystems could be the single most important determinant for the survival and long-term evolutionary success of a WGD. Mass extinctions are among the most drastic events by which old or new niches become available for colonization (FIG. 1e,f). WGDs occurring close to these extinc￾tions probably contributed to the radia￾tion of vertebrates in the Cambrian period and of several angiosperm families at the K–T boundary. The K–T mass extinction might also have played an important part in unlocking the diversification potential of 3r in teleosts, even >150 million years after 3r occurred. Conversely, the reason why the teleosts did not diversify right after the P–T mass extinction may have been because the few survivors from the Triassic period still occupied most of the relevant niche space95. However, new niches may also become available through biotic evolution. For instance, the rise of angiosperm plants led to the emergence of sugar-rich fruits. Conant and Wolfe93 have suggested that the success of the genome duplication in budding yeast, approximately 100 mya, may be linked to the emergence of this new ecological niche. They showed that the retention of glycolytic pathway genes after the WGD in yeasts sup￾ported an increase in glycolytic flux that gave post-WGD yeast species a growth advantage in glucose-rich environments (FIG. 1c,d). The angiosperms also did not rise to ecological dominance by filling niches that became available after a mass extinction event85. It is possible that angiosperms filled niches in phenotype space that already existed but that had remained largely unoc￾cupied because the necessary phenotypic characteristics had not yet been developed (FIG. 1a,b). Specifically, angiosperm–insect interactions may have been important in angiosperm niche diversification. Although insect pollination evolved in several non￾angiosperm plants, such as Welwitschia mirabilis (a gnetophyte), angiosperms devel￾oped several innovations that dramatically increased the effectiveness of insect pol￾lination, such as the association of male and female reproductive organs on the same axis and the development of colourful perianth organs96–98. These specialized angiosperm– insect associations allow efficient pollina￾tion over large distances, which might have enabled angiosperm plants to colonize previ￾ously unoccupied habitats, such as dispersed microhabitats, or disturbed or resource-poor habitats. Indeed, some of the major classes of pollinating insects, lepidoptera and bees, appear in the fossil record at approximately the same time as angiosperms96,99,100. Early angiosperm polyploidizations occurring at this time might have helped plants to conquer these newly unclosed niches. It may prove difficult to determine whether polyploidy enabled organisms to survive extinctions or whether polyploidy facilitated evolutionary transitions and increased biological complexity. Sequencing more genomes and developing tools that are more able to detect and correctly date ancient polyploidy events may unveil corre￾lations between polyploidy and evolutionary changes that are currently unknown, and studying the genes remaining after a WGD and their interactors at a systems level may provide clues as to why polyploids occasion￾ally might have had a selective advantage over their diploid sister species. Yves Van de Peer and Steven Maere are at the Department of Plant Systems Biology, VIB (Flanders Institute of Biotechnology), B‑9052 Ghent, Belgium, and the Bioinformatics and Evolutionary Genomics research group, Department of Plant Biotechnology and Genetics, Ghent University, B‑9052 Ghent, Belgium. Axel Meyer is at the Department of Biology, University of Konstanz, D‑78457 Konstanz, Germany, and the Institute for Advanced Study, Wallotstraße 19, D‑14193 Berlin, Germany. Correspondence to Y.V.d.P. e‑mail: Yves.Vandepeer@psb.vib‑ugent.be doi:10.1038/nrg2600 Published online 4 August 2009 1. Masterston, J. Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264, 421–423 (1994). 2. Blanc, G. & Wolfe, K. H. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16, 1667–1678 (2004). 3. Tang, H. et al. Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. Genome Res. 18, 1944–1954 (2008). 4. Cui, L. et al. Widespread genome duplications throughout the history of flowering plants. Genome Res. 16, 738–749 (2006). 5. Ramsey, J. & Schemske, D. W. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu. Rev. Ecol. Syst. 29, 467–501 (1998). 6. Otto, S. P. & Whitton, J. Polyploid incidence and evolution. Annu. Rev. Genet. 34, 401–437 (2000). 7. Soltis, P. S. & Soltis, D. E. The role of hybridization in plant speciation. Annu. Rev. Plant Biol. 60, 561–588 (2009). 8. Wolfe, K. H. & Shields, D. C. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387, 708–713 (1997). 9. Aury, J. M. et al. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444, 171–178 (2006). 10. Wittbrodt, J., Meyer, A. & Schartl, M. More genes in fish? Bioessays 20, 511–515 (1998). 11. Otto, S. P. The evolutionary consequences of polyploidy. Cell 131, 452–462 (2007). 12. Comai, L. The advantages and disadvantages of being polyploid. Nature Rev. Genet. 6, 836–846 (2005). 13. Soltis, D. E. et al. Polyploidy and angiosperm diversification. Am. J. Bot. 96, 336–348 (2009). 14. Soltis, D. E., Bell, C. D., Kim, S. & Soltis, P. S. Origin and early evolution of angiosperms. Ann. NY Acad. Sci. 1133, 3–25 (2008). 15. Tang, H. et al. Synteny and collinearity in plant genomes. Science 320, 486–488 (2008). 16. Jaillon, O. et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449, 463–467 (2007). 17. Scannell, D. R., Butler, G. & Wolfe, K. H. Yeast genome evolution — the origin of the species. Yeast 24, 929–942 (2007). 18. Dehal, P. & Boore, J. L. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 3, e314 (2005). 19. Putnam, N. H. et al. The amphioxus genome and the evolution of the chordate karyotype. Nature 453, 1064–1071 (2008). 20. Jaillon, O. et al. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431, 946–957 (2004). 21. Meyer, A. & Van de Peer, Y. From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 27, 937–945 (2005). 22. Crow, K. D. & Wagner, G. P. What is the role of genome duplication in the evolution of complexity and diversity? Mol. Biol. Evol. 23, 887–892 (2006). 23. Donoghue, P. C. J. & Purnell, M. A. Genome duplication, extinction and vertebrate evolution. Trends Ecol. Evol. 20, 312–319 (2005). 24. Fawcett, J. A., Maere, S. & Van de Peer, Y. Plants with double genomes might have had a better chance to survive the Cretaceous–Tertiary extinction event. Proc. Natl Acad. Sci. USA 106, 5737–5742 (2009). 25. Levin, D. A. Polyploidy and novelty in flowering plants. Am. Nat. 122, 1–25 (1983). 26. Thompson, J. D. & Lumaret, R. The evolutionary dynamics of polyploid plants — origins, establishment and persistence. Trends Ecol. Evol. 7, 302–307 (1992). 27. Bretagnolle, F. & Thompson, J. D. Gametes with the somatic chromosome number: mechanisms of their formation and role in the evolution of autopolyploid plants. New Phytol. 129, 1–22 (1995). 28. Osborn, T. C. et al. Understanding mechanisms of novel gene expression in polyploids. Trends Genet. 19, 141–147 (2003). 29. Rieseberg, L. H. et al. Hybridization and the colonization of novel habitats by annual sunflowers. Genetica 129, 149–165 (2007). 30. Rieseberg, L. H. et al. Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301, 1211–1216 (2003). 31. Hegarty, M. J. et al. Changes to gene expression associated with hybrid speciation in plants: further insights from transcriptomic studies in Senecio. Philos. Trans. R. Soc. Lond. B 363, 3055–3069 (2008). 32. Ellstrand, N. C. & Schierenbeck, K. A. Hybridization as a stimulus for the evolution of invasiveness in plants? Proc. Natl Acad. Sci. USA 97, 7043–7050 (2000). 33. Pandit, M. K., Tan, H. T. W. & Bisht, M. S. Polyploidy in invasive plant species of Singapore. Bot. J. Linn. Soc. 151, 395–403 (2006). 34. Soltis, D. E., Soltis, P. S. & Tate, J. A. Advances in the study of polyploidy since plant speciation. New Phytol. 161, 173–191 (2003). 35. Lokki, J. & Saura, A. Polyploidy in insect evolution. Basic Life Sci. 13, 277–312 (1979). 36. Weldon, C., du Preez, L. H., Hyatt, A. D., Muller, R. & Spears, R. Origin of the amphibian chytrid fungus. Emerg. Infect. Dis. 10, 2100–2105 (2004). 37. Parker, J. M., Mikaelian, I., Hahn, N. & Diggs, H. E. Clinical diagnosis and treatment of epidermal chytridiomycosis in African clawed frogs (Xenopus tropicalis). Comp. Med. 52, 265–268 (2002). 38. Hegarty, M. & Hiscock, S. Polyploidy: doubling up for evolutionary success. Curr. Biol. 17, R927–R929 (2007). 39. Bicknell, R. A. & Koltunow, A. M. Understanding apomixis: recent advances and remaining conundrums. Plant Cell 16, S228–S245 (2004). 40. Holland, L. Z. et al. The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res. 18, 1100–1111 (2008). 41. Xiao, S. & Laflamme, M. On the eve of animal radiation: phylogeny, ecology and evolution of the Ediacara biota. Trends Ecol. Evol. 24, 31–40 (2009). 42. Wille, M., Nagler, T. F., Lehmann, B., Schroder, S. & Kramers, J. D. Hydrogen sulphide release to surface waters at the Precambrian/Cambrian boundary. Nature 453, 767–769 (2008). 43. Knoll, A. H. & Carroll, S. B. Early animal evolution: emerging views from comparative biology and geology. Science 284, 2129–2137 (1999). 44. Hurley, I. A. et al. A new time-scale for ray-finned fish evolution. Proc. R. Soc. B 274, 489–498 (2007). Pers P ectives nATurE rEvIEWS | Genetics voluME 10 | oCToBEr 2009 | 731 © 2009 Macmillan Publishers Limited. All rights reserved