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.
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.
This is a preview of subscription content, access via your institution
Open Access articles citing this article.
Functional and evolutionary study of MLO gene family in the regulation of Sclerotinia stem rot resistance in Brassica napus L.
Biotechnology for Biofuels and Bioproducts Open Access 23 May 2023
Independent rediploidization masks shared whole genome duplication in the sturgeon-paddlefish ancestor
Nature Communications Open Access 19 May 2023
POInTbrowse: orthology prediction and synteny exploration for paleopolyploid genomes
BMC Bioinformatics Open Access 27 April 2023
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 print issues and online access
$189.00 per year
only $15.75 per issue
Rent or buy this article
Get just this article for as long as you need it
Prices may be subject to local taxes which are calculated during checkout
Soltis, D. E., Visger, C. J. & Soltis, P. S. The polyploidy revolution then...and now: Stebbins revisited. Am. J. Bot. 101, 1057–1078 (2014).
Mable, B. K., Alexandrou, M. A. & Taylor, M. I. Genome duplication in amphibians and fish: an extended synthesis. J. Zool. 284, 151–182 (2011).
Otto, S. P. & Whitton, J. Polyploid incidence and evolution. Annu. Rev. Genet. 34, 401–437 (2000).
Wolfe, K. H. & Shields, D. C. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387, 708–713 (1997).
The Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796–815 (2000).
Dehal, P. & Boore, J. L. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 3, e314 (2005).
Ohno, S. Evolution by Gene Duplication (Springer, 1970).
Amores, A. et al. Zebrafish hox clusters and vertebrate genome evolution. Science 282, 1711–1714 (1998).
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).
Arrigo, N. & Barker, M. S. Rarely successful polyploids and their legacy in plant genomes. Curr. Opin. Plant Biol. 15, 140–146 (2012).
Meyers, L. A. & Levin, D. A. On the abundance of polyploids in flowering plants. Evolution 60, 1198–1206 (2006).
Scarpino, S. V., Levin, D. A. & Meyers, L. A. Polyploid formation shapes flowering plant diversity. Am. Nat. 184, 456–465 (2014).
Soltis, D. E. & Soltis, P. S. Polyploidy: recurrent formation and genome evolution. Trends Ecol. Evol. 14, 348–352 (1999).
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).
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).
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).
Van de Peer, Y., Maere, S. & Meyer, A. The evolutionary significance of ancient genome duplications. Nat. Rev. Genet. 10, 725–732 (2009).
Lohaus, R. & Van de Peer, Y. Of dups and dinos: evolution at the K/Pg boundary. Curr. Opin. Plant Biol. 30, 62–69 (2016).
Kagale, S. et al. Polyploid evolution of the Brassicaceae during the Cenozoic era. Plant Cell 26, 2777–2791 (2014).
Van de Peer, Y. Computational approaches to unveiling ancient genome duplications. Nat. Rev. Genet. 5, 752–763 (2004).
Taylor, J. S. & Raes, J. Duplication and divergence: the evolution of new genes and old ideas. Annu. Rev. Genet. 38, 615–643 (2004).
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).
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).
Comai, L. The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 6, 836–846 (2005).
Soltis, D. E. et al. Polyploidy and angiosperm diversification. Am. J. Bot. 96, 336–348 (2009).
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.
Madlung, A. Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity 110, 99–104 (2013).
Leitch, A. R. & Leitch, I. J. Perspective — genomic plasticity and the diversity of polyploid plants. Science 320, 481–483 (2008).
Bomblies, K. & Madlung, A. Polyploidy in the Arabidopsis genus. Chromosome Res. 22, 117–134 (2014).
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).
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).
Song, Q. & Chen, Z. J. Epigenetic and developmental regulation in plant polyploids. Curr. Opin. Plant Biol. 24, 101–109 (2015).
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).
Parisod, C., Holderegger, R. & Brochmann, C. Evolutionary consequences of autopolyploidy. New Phytol. 186, 5–17 (2010).
Zhang, H. et al. Transcriptome shock invokes disruption of parental expression-conserved genes in tetraploid wheat. Sci. Rep. 6, 26363 (2016).
Doyle, J. J. et al. Evolutionary genetics of genome merger and doubling in plants. Annu. Rev. Genet. 42, 443–461 (2008).
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.
McCarthy, E. W. et al. Transgressive phenotypes and generalist pollination in the floral evolution of Nicotiana polyploids. Nat. Plants 2, 16119 (2016).
Segraves, K. A. & Anneberg, T. J. Species interactions and plant polyploidy. Am. J. Bot. 103, 1326–1335 (2016).
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).
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).
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).
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).
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).
Oswald, B. P. & Nuismer, S. L. Neopolyploidy and pathogen resistance. Proc. Biol. Sci. 274, 2393–2397 (2007).
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).
Ramsey, J. Polyploidy and ecological adaptation in wild yarrow. Proc. Natl Acad. Sci. USA 108, 7096–7101 (2011).
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).
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.
Ruiz, M. et al. Tetraploidy enhances the ability to exclude chloride from leaves in carrizo citrange seedlings. J. Plant Physiol. 205, 1–10 (2016).
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).
Wood, T. E. et al. The frequency of polyploid speciation in vascular plants. Proc. Natl Acad. Sci. USA 106, 13875–13879 (2009).
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).
Fowler, N. L. & Levin, D. A. Critical factors in the establishment of allopolyploids. Am. J. Bot. 103, 1236–1251 (2016).
Mayrose, I. et al. Recently formed polyploid plants diversify at lower rates. Science 333, 1257 (2011).
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).
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).
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).
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).
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).
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).
Furlong, R. F. & Holland, P. W. Were vertebrates octoploid? Phil. Trans. R. Soc. B 357, 531–544 (2002).
Kellogg, E. A. Has the connection between polyploidy and diversification actually been tested? Curr. Opin. Plant Biol. 30, 25–32 (2016).
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).
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).
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).
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).
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.
Cannon, S. B. et al. Multiple polyploidy events in the early radiation of nodulating and nonnodulating legumes. Mol. Biol. Evol. 32, 193–210 (2015).
Yu, Y. et al. Whole-genome duplication and molecular evolution in Cornus L. (Cornaceae) — insights from transcriptome sequences. PLoS ONE 12, e0171361 (2017).
Renne, P. R. et al. State shift in Deccan volcanism at the Cretaceous–Paleogene boundary, possibly induced by impact. Science 350, 76–78 (2015).
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).
Li, Z. et al. Early genome duplications in conifers and other seed plants. Sci. Adv. 1, e1501084 (2015).
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).
Hurley, I. A. et al. A new time-scale for ray-finned fish evolution. Proc. Biol. Sci. 274, 489–498 (2007).
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).
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.
Edwards, E. J. et al. The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328, 587–591 (2010).
Stebbins, G. L. Polyploidy and the distribution of the arctic–alpine flora — new evidence and a new approach. Bot. Helv. 94, 1–13 (1984).
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).
Ramsey, J. & Schemske, D. W. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu. Rev. Ecol. Syst. 29, 467–501 (1998).
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).
Pecrix, Y. et al. Polyploidization mechanisms: temperature environment can induce diploid gamete formation in Rosa sp. J. Exp. Bot. 62, 3587–3597 (2011).
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).
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).
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).
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).
Visscher, H. et al. Environmental mutagenesis during the end-Permian ecological crisis. Proc. Natl Acad. Sci. USA 101, 12952–12956 (2004).
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).
Bock, D. G. et al. What we still don't know about invasion genetics. Mol. Ecol. 24, 2277–2297 (2015).
Pandit, M. K., Pocock, M. J. O. & Kunin, W. E. Ploidy influences rarity and invasiveness in plants. J. Ecol. 99, 1108–1115 (2011).
Parisod, C. & Broennimann, O. Towards unified hypotheses of the impact of polyploidy on ecological niches. New Phytol. 212, 540–542 (2016).
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).
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).
Jiao, Y. et al. Ancestral polyploidy in seed plants and angiosperms. Nature 473, 97–100 (2011).
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).
Ming, R. et al. The pineapple genome and the evolution of CAM photosynthesis. Nat. Genet. 47, 1435–1442 (2015).
Soltis, P. S. & Soltis, D. E. Ancient WGD events as drivers of key innovations in angiosperms. Curr. Opin. Plant Biol. 30, 159–165 (2016).
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).
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).
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).
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).
Berthelot, C. et al. The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat. Commun. 5, 3657 (2014).
Session, A. M. et al. Genome evolution in the allotetraploid frog Xenopus laevis. Nature 538, 336–343 (2016).
Li, Z. et al. Gene duplicability of core genes is highly consistent across all angiosperms. Plant Cell 28, 326–344 (2016).
Maere, S. et al. Modeling gene and genome duplications in eukaryotes. Proc. Natl Acad. Sci. USA 102, 5454–5459 (2005).
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).
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).
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).
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).
Zhou, W. et al. Evolution of herbivore-induced early defense signaling was shaped by genome-wide duplications in Nicotiana. eLife 5, e19531 (2016).
Schmitz, J. F., Zimmer, F. & Bornberg-Bauer, E. Mechanisms of transcription factor evolution in Metazoa. Nucleic Acids Res. 44, 6287–6297 (2016).
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).
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).
Orr-Weaver, T. L. When bigger is better: the role of polyploidy in organogenesis. Trends Genet. 31, 307–315 (2015).
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).
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).
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).
Yant, L. & Bomblies, K. Genome management and mismanagement — cell-level opportunities and challenges of whole-genome duplication. Genes Dev. 29, 2405–2419 (2015).
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).
Fujiwara, T. et al. Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 437, 1043–1047 (2005).
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).
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).
Mardin, B. R. et al. A cell-based model system links chromothripsis with hyperploidy. Mol. Syst. Biol. 11, 828 (2015).
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).
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).
de Bruin, E. C. et al. Spatial and temporal diversity in genomic instability processes defines lung cancer evolution. Science 346, 251–256 (2014).
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).
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).
Gerstein, A. C. et al. Polyploid titan cells produce haploid and aneuploid progeny to promote stress adaptation. mBio 6, e01340–15 (2015).
Yona, A. H. et al. Chromosomal duplication is a transient evolutionary solution to stress. Proc. Natl Acad. Sci. USA 109, 21010–21015 (2012).
Gordon, D. J., Resio, B. & Pellman, D. Causes and consequences of aneuploidy in cancer. Nat. Rev. Genet. 13, 189–203 (2012).
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).
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.
Voordeckers, K. et al. Adaptation to high ethanol reveals complex evolutionary pathways. PLoS Genet. 11, e1005635 (2015).
Tanaka, K. & Hirota, T. Chromosomal instability: a common feature and a therapeutic target of cancer. Biochim. Biophys. Acta 1866, 64–75 (2016).
Santaguida, S. & Amon, A. Short- and long-term effects of chromosome mis-segregation and aneuploidy. Nat. Rev. Mol. Cell Biol. 16, 473–485 (2015).
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.
Barrick, J. E. & Lenski, R. E. Genome dynamics during experimental evolution. Nat. Rev. Genet. 14, 827–839 (2013).
Breuert, S., Allers, T., Spohn, G. & Soppa, J. Regulated polyploidy in halophilic archaea. PLoS ONE 1, e92 (2006).
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).
Soppa, J. Polyploidy and community structure. Nat. Microbiol. 2, 16261 (2017).
Soppa, J. Ploidy and gene conversion in Archaea. Biochem. Soc. Trans. 39, 150–154 (2011).
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.
Maciver, S. K. Asexual amoebae escape Muller's ratchet through polyploidy. Trends Parasitol. 32, 855–862 (2016).
Markov, A. V. & Kaznacheev, I. S. Evolutionary consequences of polyploidy in prokaryotes and the origin of mitosis and meiosis. Biol. Direct 11, 28 (2016).
Ainouche, M. L. & Jenczewski, E. Focus on polyploidy. New Phytol. 186, 1–4 (2010).
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).
Mable, B. K. Polyploids and hybrids in changing environments: winners or losers in the struggle for adaptation? Heredity 110, 95–96 (2013).
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).
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).
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).
Salman-Minkov, A., Sabath, N. & Mayrose, I. Whole-genome duplication as a key factor in crop domestication. Nat. Plants 2, 16115 (2016).
Fang, Z. & Morrell, P. L. Domestication: polyploidy boosts domestication. Nat. Plants 2, 16116 (2016).
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).
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).
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).
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.
Pierazzo, E. et al. Ozone perturbation from medium-size asteroid impacts in the ocean. Earth Planet. Sci. Lett. 299, 263–272 (2010).
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).
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).
Cai, J. et al. The genome sequence of the orchid Phalaenopsis equestris. Nat. Genet. 47, 65–72 (2015).
Olsen, J. L. et al. The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature 530, 331–335 (2016).
Myburg, A. A. et al. The genome of Eucalyptus grandis. Nature 510, 356–362 (2014).
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).
Kenny, N. J. et al. Ancestral whole-genome duplication in the marine chelicerate horseshoe crabs. Heredity (Edinb.) 116, 190–199 (2016).
Lien, S. et al. The Atlantic salmon genome provides insights into rediploidization. Nature 533, 200–205 (2016).
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).
Corrochano, L. M. et al. Expansion of signal transduction pathways in fungi by extensive genome duplication. Curr. Biol. 26, 1577–1584 (2016).
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).
Hoshino, A. et al. Genome sequence and analysis of the Japanese morning glory Ipomoea nil. Nat. Commun. 7, 13295 (2016).
Sollars, E. S. et al. Genome sequence and genetic diversity of European ash trees. Nature 541, 212–216 (2017).
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).
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).
Yant, L. et al. Meiotic adaptation to genome duplication in Arabidopsis arenosa. Curr. Biol. 23, 2151–2156 (2013).
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.
The authors declare no competing financial interests.
The condition in which cells or organisms possess more than two complete sets of chromosomes.
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.
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.
Duplicated genes (paralogues) that originate from a whole-genome duplication event.
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.
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.
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.
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.
Rights and permissions
About this article
Cite this article
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
This article is cited by
POInTbrowse: orthology prediction and synteny exploration for paleopolyploid genomes
BMC Bioinformatics (2023)
Asymmetric gene expression and cell-type-specific regulatory networks in the root of bread wheat revealed by single-cell multiomics analysis
Genome Biology (2023)
Deciphering evolutionary dynamics of WRKY genes in Arachis species
BMC Genomics (2023)
Functional and evolutionary study of MLO gene family in the regulation of Sclerotinia stem rot resistance in Brassica napus L.
Biotechnology for Biofuels and Bioproducts (2023)
Independent rediploidization masks shared whole genome duplication in the sturgeon-paddlefish ancestor
Nature Communications (2023)