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The evolutionary significance of polyploidy

Key Points

  • Polyploidy, or whole-genome duplication (WGD), is usually an evolutionary dead end. Although polyploidy is a frequent and recurrent phenomenon, the number of WGDs that have become established in the long term is low.

  • The occurrence of WGDs in the tree of life is not random and seems to correlate with periods of environmental upheaval.

  • WGDs increase the adaptive potential of cells and organisms exposed to stressful conditions.

  • The biased retention of genes following WGDs offers a unique evolutionary potential to evolve key innovations and to increase biological complexity in the long term.

  • In cancer, WGD is a transient state that promotes aneuploidy, and is responsible for increased genetic variation and subsequent adaptive potential.

Abstract

Polyploidy, or the duplication of entire genomes, has been observed in prokaryotic and eukaryotic organisms, and in somatic and germ cells. The consequences of polyploidization are complex and variable, and they differ greatly between systems (clonal or non-clonal) and species, but the process has often been considered to be an evolutionary 'dead end'. Here, we review the accumulating evidence that correlates polyploidization with environmental change or stress, and that has led to an increased recognition of its short-term adaptive potential. In addition, we discuss how, once polyploidy has been established, the unique retention profile of duplicated genes following whole-genome duplication might explain key longer-term evolutionary transitions and a general increase in biological complexity.

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Figure 1: A phylogenetic tree showing known whole-genome duplications.
Figure 2: A schematic representation of the effects of whole-genome duplication and environmental stress on the evolution of gene number and fitness.
Figure 3: The distribution of diploid and tetraploid Neobatrachus species.
Figure 4: Polyploidy in different systems.

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References

  1. Soltis, D. E., Visger, C. J. & Soltis, P. S. The polyploidy revolution then...and now: Stebbins revisited. Am. J. Bot. 101, 1057–1078 (2014).

    Article  PubMed  Google Scholar 

  2. Mable, B. K., Alexandrou, M. A. & Taylor, M. I. Genome duplication in amphibians and fish: an extended synthesis. J. Zool. 284, 151–182 (2011).

    Article  Google Scholar 

  3. Otto, S. P. & Whitton, J. Polyploid incidence and evolution. Annu. Rev. Genet. 34, 401–437 (2000).

    Article  CAS  PubMed  Google Scholar 

  4. Wolfe, K. H. & Shields, D. C. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387, 708–713 (1997).

    Article  CAS  PubMed  Google Scholar 

  5. The Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796–815 (2000).

  6. Dehal, P. & Boore, J. L. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 3, e314 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Ohno, S. Evolution by Gene Duplication (Springer, 1970).

    Book  Google Scholar 

  8. Amores, A. et al. Zebrafish hox clusters and vertebrate genome evolution. Science 282, 1711–1714 (1998).

    Article  CAS  PubMed  Google Scholar 

  9. Soltis, P. S., Marchant, D. B., Van de Peer, Y. & Soltis, D. E. Polyploidy and genome evolution in plants. Curr. Opin. Genet. Dev. 35, 119–125 (2015).

    Article  CAS  PubMed  Google Scholar 

  10. Arrigo, N. & Barker, M. S. Rarely successful polyploids and their legacy in plant genomes. Curr. Opin. Plant Biol. 15, 140–146 (2012).

    Article  CAS  PubMed  Google Scholar 

  11. Meyers, L. A. & Levin, D. A. On the abundance of polyploids in flowering plants. Evolution 60, 1198–1206 (2006).

    Article  PubMed  Google Scholar 

  12. Scarpino, S. V., Levin, D. A. & Meyers, L. A. Polyploid formation shapes flowering plant diversity. Am. Nat. 184, 456–465 (2014).

    Article  PubMed  Google Scholar 

  13. Soltis, D. E. & Soltis, P. S. Polyploidy: recurrent formation and genome evolution. Trends Ecol. Evol. 14, 348–352 (1999).

    Article  CAS  PubMed  Google Scholar 

  14. Campbell, M. A., Ganley, A. R. D., Gabaldón, T. & Cox, M. P. The case of the missing ancient fungal polyploids. Am. Nat. 188, 602–614 (2016).

    Article  PubMed  Google Scholar 

  15. Vanneste, K., Maere, S. & Van de Peer, Y. Tangled up in two: a burst of genome duplications at the end of the Cretaceous and the consequences for plant evolution. Phil. Trans. R. Soc. B. 369, 20130353 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  16. Mayrose, I. et al. Methods for studying polyploid diversification and the dead end hypothesis: a reply to Soltis et al. (2014). New Phytol. 206, 27–35 (2015).

    Article  PubMed  Google Scholar 

  17. Van de Peer, Y., Maere, S. & Meyer, A. The evolutionary significance of ancient genome duplications. Nat. Rev. Genet. 10, 725–732 (2009).

    Article  CAS  PubMed  Google Scholar 

  18. Lohaus, R. & Van de Peer, Y. Of dups and dinos: evolution at the K/Pg boundary. Curr. Opin. Plant Biol. 30, 62–69 (2016).

    Article  CAS  PubMed  Google Scholar 

  19. Kagale, S. et al. Polyploid evolution of the Brassicaceae during the Cenozoic era. Plant Cell 26, 2777–2791 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Van de Peer, Y. Computational approaches to unveiling ancient genome duplications. Nat. Rev. Genet. 5, 752–763 (2004).

    Article  CAS  PubMed  Google Scholar 

  21. Taylor, J. S. & Raes, J. Duplication and divergence: the evolution of new genes and old ideas. Annu. Rev. Genet. 38, 615–643 (2004).

    Article  CAS  PubMed  Google Scholar 

  22. Bowers, J. E., Chapman, B. A., Rong, J. & Paterson, A. H. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422, 433–438 (2003).

    Article  CAS  PubMed  Google Scholar 

  23. Conant, G. C. & Wolfe, K. H. Turning a hobby into a job: how duplicated genes find new functions. Nat. Rev. Genet. 9, 938–950 (2008).

    Article  CAS  PubMed  Google Scholar 

  24. Comai, L. The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 6, 836–846 (2005).

    Article  CAS  PubMed  Google Scholar 

  25. Soltis, D. E. et al. Polyploidy and angiosperm diversification. Am. J. Bot. 96, 336–348 (2009).

    Article  PubMed  Google Scholar 

  26. te Beest, M. et al. The more the better? The role of polyploidy in facilitating plant invasions. Ann. Bot. 109, 19–45 (2012). This detailed review discusses the genomic and ecological consequences of polyploidization and how they might affect life-history traits and species invasiveness.

    Article  PubMed  Google Scholar 

  27. Madlung, A. Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity 110, 99–104 (2013).

    Article  CAS  PubMed  Google Scholar 

  28. Leitch, A. R. & Leitch, I. J. Perspective — genomic plasticity and the diversity of polyploid plants. Science 320, 481–483 (2008).

    Article  CAS  PubMed  Google Scholar 

  29. Bomblies, K. & Madlung, A. Polyploidy in the Arabidopsis genus. Chromosome Res. 22, 117–134 (2014).

    Article  CAS  PubMed  Google Scholar 

  30. Lavania, U. C. et al. Autopolyploidy differentially influences body size in plants, but facilitates enhanced accumulation of secondary metabolites, causing increased cytosine methylation. Plant J. 71, 539–549 (2012).

    Article  CAS  PubMed  Google Scholar 

  31. Shi, X., Zhang, C., Ko, D. K. & Chen, Z. J. Genome-wide dosage-dependent and -independent regulation contributes to gene expression and evolutionary novelty in plant polyploids. Mol. Biol. Evol. 32, 2351–2366 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Song, Q. & Chen, Z. J. Epigenetic and developmental regulation in plant polyploids. Curr. Opin. Plant Biol. 24, 101–109 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Soltis, P. S., Liu, X., Marchant, D. B., Visger, C. J. & Soltis, D. E. Polyploidy and novelty: Gottlieb's legacy. Phil. Trans. R. Soc. B. 369, 20130351 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  34. Parisod, C., Holderegger, R. & Brochmann, C. Evolutionary consequences of autopolyploidy. New Phytol. 186, 5–17 (2010).

    Article  CAS  PubMed  Google Scholar 

  35. Zhang, H. et al. Transcriptome shock invokes disruption of parental expression-conserved genes in tetraploid wheat. Sci. Rep. 6, 26363 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Doyle, J. J. et al. Evolutionary genetics of genome merger and doubling in plants. Annu. Rev. Genet. 42, 443–461 (2008).

    Article  CAS  PubMed  Google Scholar 

  37. Schoenfelder, K. P. & Fox, D. T. The expanding implications of polyploidy. J. Cell Biol. 209, 485–491 (2015). This interesting review discusses how polyploidy (mainly in animals and fungi) frequently confers resistance to environmental stresses that are not tolerated by diploid cells. It also highlights the accumulating evidence that indicates how the study of polyploid cells might improve our understanding of human disease.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. McCarthy, E. W. et al. Transgressive phenotypes and generalist pollination in the floral evolution of Nicotiana polyploids. Nat. Plants 2, 16119 (2016).

    Article  PubMed  Google Scholar 

  39. Segraves, K. A. & Anneberg, T. J. Species interactions and plant polyploidy. Am. J. Bot. 103, 1326–1335 (2016).

    Article  PubMed  Google Scholar 

  40. Gross, K. & Schiestl, F. P. Are tetraploids more successful? Floral signals, reproductive success and floral isolation in mixed-ploidy populations of a terrestrial orchid. Ann. Bot. 115, 263–273 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. McCarthy, E. W. et al. The effect of polyploidy and hybridization on the evolution of floral colour in Nicotiana (Solanaceae). Ann. Bot. 115, 1117–1131 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Edger, P. P. et al. The butterfly plant arms-race escalated by gene and genome duplications. Proc. Natl Acad. Sci. USA 112, 8362–8366 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. van den Bergh, E., Hofberger, J. A. & Schranz, M. E. Flower power and the mustard bomb: comparative analysis of gene and genome duplications in glucosinolate biosynthetic pathway evolution in Cleomaceae and Brassicaceae. Am. J. Bot. 103, 1212–1222 (2016).

    Article  CAS  PubMed  Google Scholar 

  44. Vergara, F., Kikuchi, J. & Breuer, C. Artificial autopolyploidization modifies the tricarboxylic acid cycle and GABA shunt in Arabidopsis thaliana Col-0. Sci. Rep. 6, 26515 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Oswald, B. P. & Nuismer, S. L. Neopolyploidy and pathogen resistance. Proc. Biol. Sci. 274, 2393–2397 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  46. Hahn, M. A., van Kleunen, M. & Muller-Scharer, H. Increased phenotypic plasticity to climate may have boosted the invasion success of polyploid Centaurea stoebe. PLoS ONE 7, e50284 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Ramsey, J. Polyploidy and ecological adaptation in wild yarrow. Proc. Natl Acad. Sci. USA 108, 7096–7101 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  48. Diallo, A. M., Nielsen, L. R., Kjaer, E. D., Petersen, K. K. & Raebild, A. Polyploidy can confer superiority to West African Acacia senegal (L.) Willd. trees. Front. Plant Sci. 7, 821 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Chao, D. Y. et al. Polyploids exhibit higher potassium uptake and salinity tolerance in Arabidopsis. Science 341, 658–659 (2013). This paper shows that both natural polyploidy and artificially-induced polyploidy in A. thaliana confer increased salt tolerance by regulating leaf potassium levels.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Ruiz, M. et al. Tetraploidy enhances the ability to exclude chloride from leaves in carrizo citrange seedlings. J. Plant Physiol. 205, 1–10 (2016).

    Article  CAS  PubMed  Google Scholar 

  51. Yang, P. M., Huang, Q. C., Qin, G. Y., Zhao, S. P. & Zhou, J. G. Different drought-stress responses in photosynthesis and reactive oxygen metabolism between autotetraploid and diploid rice. Photosynthetica 52, 193–202 (2014).

    Article  CAS  Google Scholar 

  52. Wood, T. E. et al. The frequency of polyploid speciation in vascular plants. Proc. Natl Acad. Sci. USA 106, 13875–13879 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  53. Barker, M. S., Arrigo, N., Baniaga, A. E., Li, Z. & Levin, D. A. On the relative abundance of autopolyploids and allopolyploids. New Phytol. 210, 391–398 (2016).

    Article  PubMed  Google Scholar 

  54. Fowler, N. L. & Levin, D. A. Critical factors in the establishment of allopolyploids. Am. J. Bot. 103, 1236–1251 (2016).

    Article  PubMed  Google Scholar 

  55. Mayrose, I. et al. Recently formed polyploid plants diversify at lower rates. Science 333, 1257 (2011).

    Article  CAS  PubMed  Google Scholar 

  56. Oberlander, K. C., Dreyer, L. L., Goldblatt, P., Suda, J. & Linder, H. P. Species-rich and polyploid-poor: insights into the evolutionary role of whole-genome duplication from the Cape flora biodiversity hotspot. Am. J. Bot. 103, 1336–1347 (2016).

    Article  PubMed  Google Scholar 

  57. Husband, B. C., Baldwin, S. J. & Sabara, H. A. Direct versus indirect effects of whole-genome duplication on prezygotic isolation in Chamerion angustifolium: implications for rapid speciation. Am. J. Bot. 103, 1259–1271 (2016).

    Article  PubMed  Google Scholar 

  58. Schranz, M. E., Mohammadin, S. & Edger, P. P. Ancient whole genome duplications, novelty and diversification: the WGD Radiation Lag-Time Model. Curr. Opin. Plant Biol. 15, 147–153 (2012).

    Article  PubMed  Google Scholar 

  59. Tank, D. C. et al. Nested radiations and the pulse of angiosperm diversification: increased diversification rates often follow whole genome duplications. New Phytol. 207, 454–467 (2015).

    Article  PubMed  Google Scholar 

  60. Clarke, J. T., Lloyd, G. T. & Friedman, M. Little evidence for enhanced phenotypic evolution in early teleosts relative to their living fossil sister group. Proc. Natl Acad. Sci. USA 113, 11531–11536 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Robertson, F. M. et al. Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification. Preprint at bioRxiv http://doi.org/10.1101/098582 (2017).

    Google Scholar 

  62. Furlong, R. F. & Holland, P. W. Were vertebrates octoploid? Phil. Trans. R. Soc. B 357, 531–544 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Kellogg, E. A. Has the connection between polyploidy and diversification actually been tested? Curr. Opin. Plant Biol. 30, 25–32 (2016).

    Article  PubMed  Google Scholar 

  64. Huang, C. H. et al. Multiple polyploidization events across Asteraceae with two nested events in the early history revealed by nuclear phylogenomics. Mol. Biol. Evol. 33, 2820–2835 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Barker, M. S. et al. Most Compositae (Asteraceae) are descendants of a paleohexaploid and all share a paleotetraploid ancestor with the Calyceraceae. Am. J. Bot. 103, 1203–1211 (2016).

    Article  CAS  PubMed  Google Scholar 

  66. Crow, K. D., Wagner, G. P. & SMBE Tri-National Young Investigators. Proceedings of the SMBE Tri-National Young Investigators' Workshop 2005. What is the role of genome duplication in the evolution of complexity and diversity? Mol. Biol. Evol. 23, 887–892 (2006).

    Article  CAS  PubMed  Google Scholar 

  67. 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).

    Article  PubMed  PubMed Central  Google Scholar 

  68. Vanneste, K., Baele, G., Maere, S. & Van de Peer, Y. Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous–Paleogene boundary. Genome Res. 24, 1334–1347 (2014). This paper provides strong support for a previously suggested, but controversial, correlation between WGDs and the most recent mass extinction.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Cannon, S. B. et al. Multiple polyploidy events in the early radiation of nodulating and nonnodulating legumes. Mol. Biol. Evol. 32, 193–210 (2015).

    Article  CAS  PubMed  Google Scholar 

  70. Yu, Y. et al. Whole-genome duplication and molecular evolution in Cornus L. (Cornaceae) — insights from transcriptome sequences. PLoS ONE 12, e0171361 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Renne, P. R. et al. State shift in Deccan volcanism at the Cretaceous–Paleogene boundary, possibly induced by impact. Science 350, 76–78 (2015).

    Article  CAS  PubMed  Google Scholar 

  72. Petersen, S. V., Dutton, A. & Lohmann, K. C. End-Cretaceous extinction in Antarctica linked to both Deccan volcanism and meteorite impact via climate change. Nat. Commun. 7, 12079 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Li, Z. et al. Early genome duplications in conifers and other seed plants. Sci. Adv. 1, e1501084 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  74. 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).

    Article  CAS  PubMed  Google Scholar 

  75. Hurley, I. A. et al. A new time-scale for ray-finned fish evolution. Proc. Biol. Sci. 274, 489–498 (2007).

    Article  CAS  PubMed  Google Scholar 

  76. Soltis, D. E. & Burleigh, J. G. Surviving the K-T mass extinction: new perspectives of polyploidization in angiosperms. Proc. Natl Acad. Sci. USA 106, 5455–5456 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  77. Estep, M. C. et al. Allopolyploidy, diversification, and the Miocene grassland expansion. Proc. Natl Acad. Sci. USA 111, 15149–15154 (2014). In this paper, the authors show that a wave of allopolyploidizations in C 4 grasses seems to have coincided with the worldwide expansion of C 4 grasslands. Polyploidy seems to be correlated with the dominance of C 4 grasses over C 3 grasses and large-scale displacement of the latter.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Edwards, E. J. et al. The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328, 587–591 (2010).

    Article  CAS  PubMed  Google Scholar 

  79. Stebbins, G. L. Polyploidy and the distribution of the arctic–alpine flora — new evidence and a new approach. Bot. Helv. 94, 1–13 (1984).

    Google Scholar 

  80. Theodoridis, S., Randin, C., Broennimann, O., Patsiou, T. & Conti, E. Divergent and narrower climatic niches characterize polyploid species of European primroses in Primula sect. Aleuritia. J. Biogeogr. 40, 1278–1289 (2013).

    Article  Google Scholar 

  81. Ramsey, J. & Schemske, D. W. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu. Rev. Ecol. Syst. 29, 467–501 (1998).

    Article  Google Scholar 

  82. Kreiner, J. M., Kron, P. & Husband, B. C. Frequency and maintenance of unreduced gametes in natural plant populations: associations with reproductive mode, life history and genome size. New Phytol. 214, 879–889 (2017).

    Article  CAS  PubMed  Google Scholar 

  83. Pecrix, Y. et al. Polyploidization mechanisms: temperature environment can induce diploid gamete formation in Rosa sp. J. Exp. Bot. 62, 3587–3597 (2011).

    Article  CAS  PubMed  Google Scholar 

  84. De Storme, N., Copenhaver, G. P. & Geelen, D. Production of diploid male gametes in Arabidopsis by cold-induced destabilization of postmeiotic radial microtubule arrays. Plant Physiol. 160, 1808–1826 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Mason, A. S., Nelson, M. N., Yan, G. & Cowling, W. A. Production of viable male unreduced gametes in Brassica interspecific hybrids is genotype specific and stimulated by cold temperatures. BMC Plant Biol. 11, 103 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Kurschner, W. M., Batenburg, S. J. & Mander, L. Aberrant Classopollis pollen reveals evidence for unreduced (2n) pollen in the conifer family Cheirolepidiaceae during the Triassic–Jurassic transition. Proc. Biol. Sci. 280, 20131708 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  87. Foster, C. B. & Afonin, S. A. Abnormal pollen grains: an outcome of deteriorating atmospheric conditions around the Permian–Triassic boundary. J. Geol. Soc. London 162, 653–659 (2005).

    Article  Google Scholar 

  88. Visscher, H. et al. Environmental mutagenesis during the end-Permian ecological crisis. Proc. Natl Acad. Sci. USA 101, 12952–12956 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Hovick, S. M. & Whitney, K. D. Hybridisation is associated with increased fecundity and size in invasive taxa: meta-analytic support for the hybridisation-invasion hypothesis. Ecol. Lett. 17, 1464–1477 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  90. Bock, D. G. et al. What we still don't know about invasion genetics. Mol. Ecol. 24, 2277–2297 (2015).

    Article  PubMed  Google Scholar 

  91. Pandit, M. K., Pocock, M. J. O. & Kunin, W. E. Ploidy influences rarity and invasiveness in plants. J. Ecol. 99, 1108–1115 (2011).

    Article  Google Scholar 

  92. Parisod, C. & Broennimann, O. Towards unified hypotheses of the impact of polyploidy on ecological niches. New Phytol. 212, 540–542 (2016).

    Article  PubMed  Google Scholar 

  93. Glennon, K. L., Ritchie, M. E. & Segraves, K. A. Evidence for shared broad-scale climatic niches of diploid and polyploid plants. Ecol. Lett. 17, 574–582 (2014).

    Article  CAS  PubMed  Google Scholar 

  94. Marchant, B. D., Soltis, D. E. & Soltis, P. S. Patterns of abiotic niche shifts in allopolyploids relative to their progenitors. New Phytol. 212, 708–718 (2016).

    Article  CAS  Google Scholar 

  95. Jiao, Y. et al. Ancestral polyploidy in seed plants and angiosperms. Nature 473, 97–100 (2011).

    Article  CAS  PubMed  Google Scholar 

  96. Vekemans, D. et al. Gamma paleohexaploidy in the stem lineage of core eudicots: significance for MADS-box gene and species diversification. Mol. Biol. Evol. 29, 3793–3806 (2012).

    Article  CAS  PubMed  Google Scholar 

  97. Ming, R. et al. The pineapple genome and the evolution of CAM photosynthesis. Nat. Genet. 47, 1435–1442 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Soltis, P. S. & Soltis, D. E. Ancient WGD events as drivers of key innovations in angiosperms. Curr. Opin. Plant Biol. 30, 159–165 (2016).

    Article  PubMed  Google Scholar 

  99. Nakatani, Y., Takeda, H., Kohara, Y. & Morishita, S. Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Res. 17, 1254–1265 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Makino, T. & McLysaght, A. Ohnologs in the human genome are dosage balanced and frequently associated with disease. Proc. Natl Acad. Sci. USA 107, 9270–9274 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  101. Singh, P. P. et al. On the expansion of “dangerous” gene repertoires by whole-genome duplications in early vertebrates. Cell Rep. 2, 1387–1398 (2012).

    Article  CAS  PubMed  Google Scholar 

  102. Singh, P. P., Arora, J. & Isambert, H. Identification of ohnolog genes originating from whole genome duplication in early vertebrates, based on synteny comparison across multiple genomes. PLoS Comput. Biol. 11, e1004394 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Berthelot, C. et al. The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat. Commun. 5, 3657 (2014).

    Article  PubMed  Google Scholar 

  104. Session, A. M. et al. Genome evolution in the allotetraploid frog Xenopus laevis. Nature 538, 336–343 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Li, Z. et al. Gene duplicability of core genes is highly consistent across all angiosperms. Plant Cell 28, 326–344 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Maere, S. et al. Modeling gene and genome duplications in eukaryotes. Proc. Natl Acad. Sci. USA 102, 5454–5459 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Freeling, M. Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu. Rev. Plant Biol. 60, 433–453 (2009).

    Article  CAS  PubMed  Google Scholar 

  108. Conant, G. C. Comparative genomics as a time machine: how relative gene dosage and metabolic requirements shaped the time-dependent resolution of yeast polyploidy. Mol. Biol. Evol. 31, 3184–3193 (2014).

    Article  CAS  PubMed  Google Scholar 

  109. Birchler, J. A. & Veitia, R. A. Gene balance hypothesis: connecting issues of dosage sensitivity across biological disciplines. Proc. Natl Acad. Sci. USA 109, 14746–14753 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  110. De Smet, R. & Van de Peer, Y. Redundancy and rewiring of genetic networks following genome-wide duplication events. Curr. Opin. Plant Biol. 15, 168–176 (2012).

    Article  CAS  PubMed  Google Scholar 

  111. Zhou, W. et al. Evolution of herbivore-induced early defense signaling was shaped by genome-wide duplications in Nicotiana. eLife 5, e19531 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  112. Schmitz, J. F., Zimmer, F. & Bornberg-Bauer, E. Mechanisms of transcription factor evolution in Metazoa. Nucleic Acids Res. 44, 6287–6297 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Edgar, B. A., Zielke, N. & Gutierrez, C. Endocycles: a recurrent evolutionary innovation for post-mitotic cell growth. Nat. Rev. Mol. Cell Biol. 15, 197–210 (2014).

    Article  CAS  PubMed  Google Scholar 

  114. De Veylder, L., Larkin, J. C. & Schnittger, A. Molecular control and function of endoreplication in development and physiology. Trends Plant Sci. 16, 624–634 (2011).

    Article  CAS  PubMed  Google Scholar 

  115. Orr-Weaver, T. L. When bigger is better: the role of polyploidy in organogenesis. Trends Genet. 31, 307–315 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Cho, E. H. & Nijhout, H. F. Development of polyploidy of scale-building cells in the wings of Manduca sexta. Arthropod Struct. Dev. 42, 37–46 (2013).

    Article  PubMed  Google Scholar 

  117. Davoli, T. & de Lange, T. The causes and consequences of polyploidy in normal development and cancer. Annu. Rev. Cell Dev. Biol. 27, 585–610 (2011).

    Article  CAS  PubMed  Google Scholar 

  118. Ceccarelli, M., Santantonio, E., Marmottini, F., Amzallag, G. N. & Cionini, P. G. Chromosome endoreduplication as a factor of salt adaptation in Sorghum bicolor. Protoplasma 227, 113–118 (2006).

    Article  CAS  PubMed  Google Scholar 

  119. Yant, L. & Bomblies, K. Genome management and mismanagement — cell-level opportunities and challenges of whole-genome duplication. Genes Dev. 29, 2405–2419 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Coward, J. & Harding, A. Size does matter: why polyploid tumor cells are critical drug targets in the war on cancer. Front. Oncol. 4, 123 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  121. Fujiwara, T. et al. Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 437, 1043–1047 (2005).

    Article  CAS  PubMed  Google Scholar 

  122. Lv, L. et al. Tetraploid cells from cytokinesis failure induce aneuploidy and spontaneous transformation of mouse ovarian surface epithelial cells. Cell Cycle 11, 2864–2875 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Kuznetsova, A. Y. et al. Chromosomal instability, tolerance of mitotic errors and multidrug resistance are promoted by tetraploidization in human cells. Cell Cycle 14, 2810–2820 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Mardin, B. R. et al. A cell-based model system links chromothripsis with hyperploidy. Mol. Syst. Biol. 11, 828 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Caldwell, C. M., Green, R. A. & Kaplan, K. B. APC mutations lead to cytokinetic failures in vitro and tetraploid genotypes in Min mice. J. Cell Biol. 178, 1109–1120 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Dikovskaya, D. et al. Loss of APC induces polyploidy as a result of a combination of defects in mitosis and apoptosis. J. Cell Biol. 176, 183–195 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. de Bruin, E. C. et al. Spatial and temporal diversity in genomic instability processes defines lung cancer evolution. Science 346, 251–256 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Rode, A., Maass, K. K., Willmund, K. V., Lichter, P. & Ernst, A. Chromothripsis in cancer cells: an update. Int. J. Cancer 138, 2322–2333 (2016).

    Article  CAS  PubMed  Google Scholar 

  129. Borodkina, A. V. et al. Tetraploidization or autophagy: the ultimate fate of senescent human endometrial stem cells under ATM or p53 inhibition. Cell Cycle 15, 117–127 (2016).

    Article  CAS  PubMed  Google Scholar 

  130. Gerstein, A. C. et al. Polyploid titan cells produce haploid and aneuploid progeny to promote stress adaptation. mBio 6, e01340–15 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Yona, A. H. et al. Chromosomal duplication is a transient evolutionary solution to stress. Proc. Natl Acad. Sci. USA 109, 21010–21015 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  132. Gordon, D. J., Resio, B. & Pellman, D. Causes and consequences of aneuploidy in cancer. Nat. Rev. Genet. 13, 189–203 (2012).

    Article  CAS  PubMed  Google Scholar 

  133. Kaya, A. et al. Adaptive aneuploidy protects against thiol peroxidase deficiency by increasing respiration via key mitochondrial proteins. Proc. Natl Acad. Sci. USA 112, 10685–10690 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Selmecki, A. M. et al. Polyploidy can drive rapid adaptation in yeast. Nature 519, 349–352 (2015). This study provides quantitative evidence that polyploidy can accelerate evolutionary adaptation in yeast in some, typically stressful, environments.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Voordeckers, K. et al. Adaptation to high ethanol reveals complex evolutionary pathways. PLoS Genet. 11, e1005635 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Tanaka, K. & Hirota, T. Chromosomal instability: a common feature and a therapeutic target of cancer. Biochim. Biophys. Acta 1866, 64–75 (2016).

    CAS  PubMed  Google Scholar 

  137. Santaguida, S. & Amon, A. Short- and long-term effects of chromosome mis-segregation and aneuploidy. Nat. Rev. Mol. Cell Biol. 16, 473–485 (2015).

    Article  CAS  PubMed  Google Scholar 

  138. Dewhurst, S. M. et al. Tolerance of whole-genome doubling propagates chromosomal instability and accelerates cancer genome evolution. Cancer Discov. 4, 175–185 (2014). This seminal paper shows how rare cells that survive a WGD event have increased tolerance to chromosome aberrations.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Barrick, J. E. & Lenski, R. E. Genome dynamics during experimental evolution. Nat. Rev. Genet. 14, 827–839 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Breuert, S., Allers, T., Spohn, G. & Soppa, J. Regulated polyploidy in halophilic archaea. PLoS ONE 1, e92 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Pecoraro, V., Zerulla, K., Lange, C. & Soppa, J. Quantification of ploidy in proteobacteria revealed the existence of monoploid, (mero-)oligoploid and polyploid species. PLoS ONE 6, e16392 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Soppa, J. Polyploidy and community structure. Nat. Microbiol. 2, 16261 (2017).

    Article  CAS  PubMed  Google Scholar 

  143. Soppa, J. Ploidy and gene conversion in Archaea. Biochem. Soc. Trans. 39, 150–154 (2011).

    Article  CAS  PubMed  Google Scholar 

  144. Lange, C., Zerulla, K., Breuert, S. & Soppa, J. Gene conversion results in the equalization of genome copies in the polyploid haloarchaeon Haloferax volcanii. Mol. Microbiol. 80, 666–677 (2011). This seminal paper demonstrates the existence of gene conversion, one of the processes that is key to the survival of polyploid prokaryotes.

    Article  CAS  PubMed  Google Scholar 

  145. Maciver, S. K. Asexual amoebae escape Muller's ratchet through polyploidy. Trends Parasitol. 32, 855–862 (2016).

    Article  PubMed  Google Scholar 

  146. Markov, A. V. & Kaznacheev, I. S. Evolutionary consequences of polyploidy in prokaryotes and the origin of mitosis and meiosis. Biol. Direct 11, 28 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Ainouche, M. L. & Jenczewski, E. Focus on polyploidy. New Phytol. 186, 1–4 (2010).

    Article  PubMed  Google Scholar 

  148. Barker, M. S., Husband, B. C. & Pires, J. C. Spreading Winge and flying high: the evolutionary importance of polyploidy after a century of study. Am. J. Bot. 103, 1139–1145 (2016).

    Article  CAS  PubMed  Google Scholar 

  149. Mable, B. K. Polyploids and hybrids in changing environments: winners or losers in the struggle for adaptation? Heredity 110, 95–96 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Soltis, D. E., Visger, C. J., Marchant, D. B. & Soltis, P. S. Polyploidy: pitfalls and paths to a paradigm. Am. J. Bot. 103, 1146–1166 (2016).

    Article  PubMed  Google Scholar 

  151. Soltis, D. E., Buggs, R. J. A., Doyle, J. J. & Soltis, P. S. What we still don't know about polyploidy. Taxon 59, 1387–1403 (2010).

    Article  Google Scholar 

  152. Poustka, A. J. et al. A global view of gene expression in lithium and zinc treated sea urchin embryos: new components of gene regulatory networks. Genome Biol. 8, R85 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Salman-Minkov, A., Sabath, N. & Mayrose, I. Whole-genome duplication as a key factor in crop domestication. Nat. Plants 2, 16115 (2016).

    Article  CAS  PubMed  Google Scholar 

  154. Fang, Z. & Morrell, P. L. Domestication: polyploidy boosts domestication. Nat. Plants 2, 16116 (2016).

    Article  PubMed  Google Scholar 

  155. Hu, G., Koh, J., Yoo, M. J., Chen, S. & Wendel, J. F. Gene-expression novelty in allopolyploid cotton: a proteomic perspective. Genetics 200, 91–104 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Yoo, M. J., Liu, X., Pires, J. C., Soltis, P. S. & Soltis, D. E. Nonadditive gene expression in polyploids. Annu. Rev. Genet. 48, 485–517 (2014).

    Article  CAS  PubMed  Google Scholar 

  157. Gallagher, J. P., Grover, C. E., Hu, G. & Wendel, J. F. Insights into the ecology and evolution of polyploid plants through network analysis. Mol. Ecol. 25, 2644–2660 (2016).

    Article  PubMed  Google Scholar 

  158. Freeling, M. Picking up the ball at the K/Pg boundary: the distribution of ancient polyploidies in the plant phylogenetic tree as a spandrel of asexuality with occasional sex. Plant Cell 29, 202–206 (2017). This paper proposes an interesting hypothesis about how polyploid plants might be able to survive periods of mass extinction.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Pierazzo, E. et al. Ozone perturbation from medium-size asteroid impacts in the ocean. Earth Planet. Sci. Lett. 299, 263–272 (2010).

    Article  CAS  Google Scholar 

  160. Ruhfel, B. R., Gitzendanner, M. A., Soltis, P. S., Soltis, D. E. & Burleigh, J. G. From algae to angiosperms — inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes. BMC Evol. Biol. 14, 23 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  161. Magallon, S. A review of the effect of relaxed clock method, long branches, genes, and calibrations in the estimation of angiosperm age. Bot. Sci. 92, 1–22 (2014).

    Article  Google Scholar 

  162. Cai, J. et al. The genome sequence of the orchid Phalaenopsis equestris. Nat. Genet. 47, 65–72 (2015).

    Article  CAS  PubMed  Google Scholar 

  163. Olsen, J. L. et al. The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature 530, 331–335 (2016).

    Article  CAS  PubMed  Google Scholar 

  164. Myburg, A. A. et al. The genome of Eucalyptus grandis. Nature 510, 356–362 (2014).

    Article  CAS  PubMed  Google Scholar 

  165. Vanneste, K., Sterck, L., Myburg, A. A., Van de Peer, Y. & Mizrachi, E. Horsetails are ancient polyploids: evidence from Equisetum giganteum. Plant Cell 27, 1567–1578 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Kenny, N. J. et al. Ancestral whole-genome duplication in the marine chelicerate horseshoe crabs. Heredity (Edinb.) 116, 190–199 (2016).

    Article  CAS  Google Scholar 

  167. Lien, S. et al. The Atlantic salmon genome provides insights into rediploidization. Nature 533, 200–205 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Iorizzo, M. et al. A high-quality carrot genome assembly provides new insights into carotenoid accumulation and asterid genome evolution. Nat. Genet. 48, 657–666 (2016).

    Article  CAS  PubMed  Google Scholar 

  169. Corrochano, L. M. et al. Expansion of signal transduction pathways in fungi by extensive genome duplication. Curr. Biol. 26, 1577–1584 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Bredeson, J. V. et al. Sequencing wild and cultivated cassava and related species reveals extensive interspecific hybridization and genetic diversity. Nat. Biotechnol. 34, 562–570 (2016).

    Article  CAS  PubMed  Google Scholar 

  171. Hoshino, A. et al. Genome sequence and analysis of the Japanese morning glory Ipomoea nil. Nat. Commun. 7, 13295 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Sollars, E. S. et al. Genome sequence and genetic diversity of European ash trees. Nature 541, 212–216 (2017).

    Article  CAS  PubMed  Google Scholar 

  173. Van de Peer, Y., Fawcett, J. A., Proost, S., Sterck, L. & Vandepoele, K. The flowering world: a tale of duplications. Trends Plant Sci. 14, 680–688 (2009).

    Article  CAS  PubMed  Google Scholar 

  174. Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).

    Article  Google Scholar 

  175. Yant, L. et al. Meiotic adaptation to genome duplication in Arabidopsis arenosa. Curr. Biol. 23, 2151–2156 (2013).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Y.V.d.P. and K.M. acknowledge the Multidisciplinary Research Partnership “Bioinformatics: from nucleotides to networks” Project (no. 01MR0310W) of Ghent University, Belgium. Y.V.d.P. acknowledges funding from the European Union Seventh Framework Programme (FP7/2007-2013) under European Research Council Advanced Grant Agreement 322739 –DOUBLEUP. K.M. acknowledges support from the Fonds voor Wetenschappelijk Onderzoek – Flanders (FWO15/PRJ/396). Special thanks go to R. Lohaus for helpful discussions and to P. Novikova for providing Figure 3. Y.V.d.P., E.M. and K.M. also thank the University of Pretoria, South Africa, for general support. The authors apologize to the many researchers whose work was overlooked or could not be included owing to space constraints. Finally, the authors thank the four anonymous reviewers for their comments and suggestions, which greatly helped to improve this Review.

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Glossary

Polyploidy

The condition in which cells or organisms possess more than two complete sets of chromosomes.

Speciation

The evolutionary process by which biological populations evolve to become distinct species.

Recurrent polyploidy

Polyploidy that has occurred multiple times in the same population or evolutionary lineage.

Neutral processes

Mechanisms that do not immediately lead to specific adaptation.

Adaptive processes

Evolutionary changes that occur as a consequence of natural selection and that are adaptive to a certain environment. Such changes increase survivorship or reproduction by addressing a specific challenge or opportunity presented by the environment.

Minority cytotype exclusion

A setting in which one cytotype (for example, diploid) is dominant over the other (for example, tetraploid), such that the less common cytotype has difficulty finding suitable partners to mate with.

Assortative mating

A mating pattern in which individuals with common traits prefer to mate with one another; for example, polyploids mating with other polyploids, rather than with diploids.

Neofunctionalization

The process by which a gene acquires a novel gene function after a duplication event.

Niche separation

The process by which competing species use the environment differently in a way that helps them to coexist.

Sympatric speciation

The process through which new species evolve while inhabiting the same geographical region.

Prezygotic barriers

Mechanisms that prevent fertilization from occurring.

Ohnologues

Duplicated genes (paralogues) that originate from a whole-genome duplication event.

Paleopolyploidies

Polyploidies that have occurred at least several million years ago. Most paleopolyploids have lost their polyploid status through a process called diploidization (the evolutionary process by which a polyploid genome turns into a diploid one) and are currently considered as functional diploids.

Ecological tolerance

The range of conditions — or niche breadth — in which an organism can thrive. More tolerant organisms can withstand a broader range of environmental conditions.

Key innovations

Important adaptations that lead to subsequent species radiation or that are of major importance for the success of a taxonomic group.

Dosage balance

The state in which the stoichiometry between all interacting partners (that is, proteins) is maintained.

Spandrel

In evolutionary biology, a spandrel is a by-product of the evolution of some other characteristic or trait, rather than a direct product of adaptive selection. At later stages of evolution, such a by-product can become (that is, can evolve into) an important adaptation.

Aneuploid

A term that describes a cell or organism that has an abnormal number of chromosomes. For instance, in humans, trisomy 21 (an extra copy of chromosome 21) is a form of aneuploidy.

Chromothripsis

The phenomenon by which potentially thousands of chromosomal rearrangements occur in a single event in localized and confined regions of the genome.

Standing variation

The presence of two or more alleles at a locus in a population that have not yet been fixed in the population.

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Van de Peer, Y., Mizrachi, E. & Marchal, K. The evolutionary significance of polyploidy. Nat Rev Genet 18, 411–424 (2017). https://doi.org/10.1038/nrg.2017.26

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