Abstract
Whole-genome duplication (WGD) appears to be a widespread phenomenon, occurring in diverse taxa including many of the model organisms used in molecular, cellular, and developmental biology. It is therefore essential to understand the potential evolutionary consequences for individual duplicated genes, as well as for the lineage as a whole. For example, duplicate genes may undergo pseudogenization or may be maintained due to neofunctionalization, subfunctionalization, or selection for increased dosage or dosage balance. Duplicates created via WGD are maintained at higher rates than single-gene duplicates, perhaps due to dosage-balance constraints. Duplicate-gene maintenance may lead to heterodimerization of an existing homodimer or to the divergence of an entire duplicated network or pathway. Allopolyploids and autopolyploids are likely to undergo different evolutionary pressures due to increased divergence between allopolyploid paralogs and an increased prevalence of multivalent formation at meiosis in autopolyploids. Perhaps most importantly, duplicate-gene loss following a WGD may significantly increase the rate of reproductive isolation between geographically isolated subpopulations and may therefore temporarily increase the speciation rate within polyploid lineages.
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References
Adams KL (2007) Evolution of duplicate gene expression in polyploid and hybrid plants. J Hered 98(2):136–141
Adams KL, Cronn R et al (2003) Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc Nat Acad Sci U S A 100:4649–4654
Adams KL, Liu Z (2007) Expression partitioning between genes duplicated by polyploidy under abiotic stress and during organ development. Curr Biol 17(19):1669–1674
Altschmied J, Delfgaauw J et al (2002) Subfunctionalization of duplicate mitf genes associated with differential degeneration of alternative exons in fish. Genetics 161(1):259–267
Anderson DW, Evans BJ (2009) Regulatory evolution of a duplicated heterodimer across species and tissues of allopolyploid clawed frogs (Xenopus). J Mol Evol 68:236–247
Aury J-M, Jaillon O et al (2006) Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444:171–178
Baack EJ (2005) To succeed globally, disperse locally: effects of local pollen and seed dispersal on tetraploid establishment. Heredity 94:538–546
Barker MS, Kane NC et al (2008) Multiple paleopolyploidizations during the evolution of the compositae reveal parallel patterns of duplicate gene retention after millions of years. Mol Biol Evol 25(11):2445–2455
Bikard D, Patel D et al (2009) Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana. Science 323:623–626
Birchler JA, Riddle NC et al (2005) Dosage balance in gene regulation: biological implications. Trends Genet 21(4):219–226
Blanc G, Wolfe KH (2004) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16:1679–1691
Bottley A, Xia GM et al (2006) Homoeologous gene silencing in hexaploid wheat. Plant J 47:897–906
Brown MT, Goldstone HMH et al (2007) A functionally divergent hydrogenosomal peptidase with protomitochondrial ancestry. Mol Microbiol 64(5):1154–1163
Buggs RJA, Elliott NM et al (2010) Tissue-specific silencing of homoeologs in natural populations of the recent allopolyploid Tragopogon mirus. New Phytol 186:175–183
Byrne KP, Wolfe KH (2007) Consistent patterns of rate asymmetry and gene loss indicate widespread neofunctionalization of yeast genes after whole-genome duplication. Genetics 175(3):1341–1350
Colon M, Hernandez F et al (2011) Saccharomyces cerevisiae Bat1 and Bat2 aminotransferases have functionally diverged from the ancestral-like Kluyveromyces lactis orthologous enzyme. PLoS ONE 6(1):e16099
Conant GC, Wolfe KH (2006) Functional partitioning of yeast co-expression networks after genome duplication. PLoS Biol 4(4):0545–0554
Conant GC, Wolfe KH (2007) Increased glycolytic flux as an outcome of whole-genome duplication in yeast. Mol Syst Biol 3:129
Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Inc, Sunderland, MA
Davis JC, Petrov DA (2005) Do disparate mechanisms of duplication add similar genes to the genome? Trends Genet 21(10):548–551
Deng C, Cheng CHC et al (2010) Evolution of an antifreeze protein by neofunctionalization under escape from adaptive conflict. Proc Nat Acad Sci U S A 107(50):21593–21598
Des Marais DL, Rausher MD (2008) Escape from adaptive conflict after duplication in an anthocyanin pathway gene. Nature 454(7205):762–765
Doyle JJ, Flagel LE et al (2008) Evolutionary genetics of genome merger and doubling in plants. Annu Rev Genet 42:443–461
Edger PP, Pires JC (2009) Gene and genome duplications: the impact of dosage-sensitivity on the fate of nuclear genes. Chromosome Res 17:699–717
Erdmann R, Gramzow L et al (2010) GORDITA (AGL63) is a young paralog of the Arabidopsis thaliana B (sister) MADS box gene ABS (TT16) that has undergone neofunctionalization. Plant J 63(6):914–924
Evans BJ (2008) Genome evolution and speciation genetics of clawed frogs (Xenopus and Silurana). Front Biosci 13:4687–4706
Evlampiev K, Isambert H (2007) Modeling protein network evolution under genome duplication and domain shuffling. BMC Syst Biol 1:49
Flagel LE, Udall JA et al (2008) Duplicate gene expression in allopolyploid gossypium reveals two temporally distinct phases of expression evolution. BMC Biol 6:16
Force A, Cresko WA et al (2005) The origin of subfunctions and modular gene regulation. Genetics 170(1):433–446
Force A, Lynch M et al (1999) The preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545
Froyd CA, Rusche LN (2011) The duplicated deacetylases sir2 and hst1 subfunctionalized by acquiring complementary inactivating mutations. Mol Cell Biol 31(16):3351–3365
Gaeta RT, Pires JC et al (2007) Genomic changes in resynthesized brassica napus and their effect on gene expression and phenotype. Plant Cell 19(11):3403–3417
Gout J-F, Duret L, et al. (2009) Differential retention of metabolic genes following whole-genome duplication. Mol Biol Evol 26(5):1067–1072
Gout J-F, Kahn D, et al. (2010) The relationship among gene expression, the evolution of gene dosage, and the rate of protein evolution. PLoS Genetics 6(5):e1000944
Han MV, Demuth JP et al (2009) Adaptive evolution of young gene duplicates in mammals. Genome Res 19(5):859–867
Hegarty MJ, Barker GL et al (2006) Transcriptome shock after interspecific hybridization in Senecio is ameliorated by genome duplication. Curr Biol 16:1652–1659
Hickman MA, Rusche LN (2010) Transcriptional silencing functions of the yeast protein Orc1/Sir3 subfunctionalized after gene duplication. Proc Nat Acad Sci U S A 107(45):19384–19389
Hughes AL (1994) The evolution of functionally novel proteins after gene duplication. Proc R Soc Lond B Biol Sci 256:119–124
Hughes T, Liberles DA (2008) Whole-genome duplications in the ancestral vertebrate are detectable in the distribution of gene family sizes of tetrapod species. J Mol Evol 67(4):343–357
Innan H, Kondrashov F (2010) The evolution of gene duplications: classifying and distinguishing between models. Nat Rev Genet 11:97–108
Jiao YN, Wickett NJ et al (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473(7345):97–100
Jimenez-Sanchez G, Childs B et al (2001) Human disease genes. Nature 409:853–855
Johnson DA, Thomas MA (2007) The monosaccharide transporter gene family in Arabidopsis and rice: a history of duplications, adaptive evolution, and functional divergence. Mol Biol Evol 24(11):2412–2423
Josefsson C, Dilkes B et al (2006) Parent-dependent loss of gene silencing during interspecies hybridization. Curr Biol 16:1322–1328
Kanno A, Saeki H et al (2003) Heterotopic expression of class B floral homeotic genes supports a modified ABC model for tulip (Tulipa gesneriana). Plant Mol Biol 52:831–841
Layeghifard M, Pirhaji L et al (2009) Adaptive evolution in the Per gene family of vertebrates: neofunctionalization by positive Darwinian selection after two major gene duplications. Biol Rhythm Res 40(6):433–444
Liang H, Plazonic KR et al (2008) Protein under-wrapping causes dosage sensitivity and decreases gene duplicability. PLoS Genet 4(1):0072–0077
Lipinski KJ, Farslow JC et al (2011) High spontaneous rate of gene duplication in Caenorhabditis elegans. Curr Biol 21:306–310
Lolkema JS, Dobrowolski A et al (2008) Evolution of antiparallel two-domain membrane proteins: tracing multiple gene duplication events in the DUF606 family. J Mol Biol 378:596–606
Lynch M (2007) The origins of genome architecture. Sinauer Associates, Sunderland, MA
Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290(5494):1151–1155
Lynch, M, Conery JS (2003a). The evolutionary demography of duplicate genes. In: Meyer A, Van de Peer Y (eds) Genome evolution. Kluwer Academic Publishers, Dordrecht, 35–44
Lynch M, Conery JS (2003) The origins of genome complexity. Science 302:1401–1404
Lynch M, Force AG (2000) The origin of interspecific genomic incompatibility via gene duplication. Am Naturaliste 156(6):590–605
Lynch M, Katju V (2004) The altered evolutionary trajectories of gene duplicates. Trends Genet 20:544–549
Lynch M, O’Hely M et al (2001) The probability of preservation of a newly arisen gene duplicate. Genetics 159:1789–1804
Maclean CJ, Greig D (2010) Reciprocal gene loss following experimental whole-genome duplication causes reproductive isolation in yeast. Evolution 65(4):932–945
MacNeil AJ, McEachern LA et al (2008) Gene duplication in early vertebrates results in tissue-specific subfunctionalized adaptor proteins: CASP and GRASP. J Mol Evol 67(2):168–178
Maere S, De Bodt S et al (2005) Modeling gene and genome duplications in eukaryotes. Proc Nat Acad Sci U S A 102(15):5454–5459
Makino T, McLysaght A (2010) Ohnologs in the human genome are dosage balanced and frequently associated with disease. Proc Nat Acad Sci U S A 107:9270–9274
Masly JP, Jones CD et al (2006) Gene transposition as a cause of hybrid sterility in Drosophila. Science 313:1448–1450
Mayrose I, Zhan SH et al (2011) Recently formed polyploid plants diversify at lower rates. Science 333(6047):1257
Meyer A, Van de Peer Y (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). BioEssays 27:937–945
Mizuta Y, Harushima Y et al (2010) Rice pollen hybrid incompatibility caused by reciprocal gene loss of duplicated genes. Proc Nat Acad Sci U S A 107(47):20417–20422
Morin RD, Chang E et al (2006) Sequencing and analysis of 10,967 full-length cDNA clones from Xenopus laevis and Xenopus tropicalis reveals post-tetraploidization transcriptome remodeling. Genome Res 16:796–803
Ngai J, Dowling MM et al (1993) The family of genes encoding odorant receptors in the channel catfish. Cell 72:657–666
Ohno S (1970) Evolution by gene duplication. Springer, Berlin
Oka HI (1988). Functions and genetic bases of reproductive barriers. Origin of cultivated rice. Japan Scientific Societies Press/Elsevier, HI Oka, Tokyo, pp 181–209
Otto SP (2007) The evolutionary consequences of polyploidy. Cell 131:452–462
Panopoulou G, Poustka AJ (2005) Timing and mechanism of ancient vertebrate genome duplications—the adventure of a hypothesis. Trends Genet 21:559–567
Papp B, Pal C et al (2003) Dosage sensitivity and the evolution of gene families in yeast. Nature 424:194–197
Paterson AH, Chapman BA et al (2006) Many gene and domain families have convergent fates following independent whole-genome duplication events in Arabidopsis, Oryza, Saccharomyces and Tetraodon. Trends Genet 22(11):597–602
Piatigorsky J, Wistow G (1991) The recruitment of crystallins—new functions precede gene duplication. Science 252(5009):1078–1079
Pinhal D, Yoshimura TS et al (2011) The 5S rDNA family evolves through concerted and birth-and-death evolution in fish genomes: an example from freshwater stingrays. BMC Evol Biol 11:151
Pires JC, Gaeta RT (2011) Structural and functional evolution of resynthesized polyploids. In: Schmidt R, Bandcroft I (eds) Genetics and genomics of the brassicaceae, Springer, New York, 9:195–214
Postlethwait JH, Woods IG et al (2000) Zebrafish comparative genomics and the origins of vertebrate chromosomes. Genome Res 10:1890–1902
Presgraves DC (2010) The molecular evolutionary basis of species formation. Nat Rev Genet 11:175–180
Putnam NH, Butts T et al (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453:1064–1071
Qian W, Zhang J (2008) Gene dosage and gene duplicability. Genetics 179:2319–2324
Qian WF, Liao BY et al (2010) Maintenance of duplicate genes and their functional redundancy by reduced expression. Trends Genet 26(10):425–430
Ramsey J, Schemske DW (2002) Neopolyploidy in flowering plants. Annu Rev Ecol Syst 33:589–639
Rapp RA, Udall JA et al (2009) Genomic expression dominance in allopolyploids. BMC Biol 7:18
Rausch JH, Morgan MT (2005) The effect of self-fertilization, inbreeding depression, and population size on autopolyploid establishment. Evolution 59(9):1867–1875
Rodriguez DJ (1996) A model for the establishment of polyploidy in plants. Am Naturalist 147(1):33–46
Salmon A, Ainouche ML et al (2005) Genetic and epigenetic consequences of recent hybridization and polyploidy in Spartina (Poaceae). Mol Ecol 14:1163–1175
Scannell DR, Byrne KP et al (2006) Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts. Nature 440:341–345
Scannell DR, Frank AC et al (2007) Independent sorting-out of thousands of duplicated gene pairs in two yeast species descended from a whole-genome duplication. Proc Nat Acad Sci U S A 104(20):8397–8402
Scannell DR, Wolfe KH (2008) A burst of protein sequence evolution and a prolonged period of asymmetric evolution follow gene duplication in yeast. Genome Res 18(1):137–147
Semon M, Wolfe KH (2007) Reciprocal gene loss between Tetraodon and zebrafish after whole genome duplication in their ancestor. Trends Genet 23(3):108–112
Semon M, Wolfe KH (2008) Preferential subfunctionalization of slow-evolving genes after allopolyploidization in Xenopus laevis. Proc Nat Acad Sci U S A 105(24):8333–8338
Simillion C, Vandepoele K et al (2002) The hidden duplication past of Arabidopsis thaliana. Proc Nat Acad Sci U S A 99:13627–13632
Sinha SC, Wetterer M et al (2005) Origin of asymmetry in adenylyl cyclases: structures of Mycobacterium tuberculosis Rv1900c. EMBO J 24:663–673
Soltis DE, Albert VA et al (2009) Polyploidy and angiosperm diversification. Am J Bot 96(1):336–348
Soltis PS, Soltis DE et al (2006) Expression of floral regulators in basal angiosperms and the origin and evolution of ABC-function. Adv Bot Res 44:483–506
Stoltzfus A (1999) On the possibility of constructive neutral evolution. J Mol Evol 49:169–181
Surcel A, Zhou X et al (2008) Long-term maintenance of stable copy number in the eukaryotic SMC family: origin of a vertebrate meiotic SMC1 and fate of recent segmental duplicates. J Syst Evol 46(3):405–423
Tate JA, Ni Z et al (2006) Evolution and expression of homeologous loci in Tragopogon miscellus (Asteraceae), a recent and reciprocally formed allopolyploid. Genetics 173:1599–1611
Taylor JS, Raes J (2004) Duplication and divergence: The evolution of new genes and old ideas. Annu Rev Genet 38:615–643
Thomas BC, Pedersen B et al (2006) Following tetraploidy in an Arabidopsis ancestor, genes were removed preferentially from one homeolog leaving clusters enriched in dose-sensitive genes. Genome Res 16:934–946
Tirosh I, Barkai N (2007) Comparative analysis indicates regulatory neofunctionalization of yeast duplicates. Genome Biol 8(4):R50
Udall JA, Swanson JM et al (2006) A novel approach for characterizing expression levels of genes duplicated by polyploidy. Genetics 173:1823–1827
Veitia RA (2002) Exploring the etiology of haploinsufficiency. BioEssays 24(2):175–184
Veitia RA, Bottani S et al (2008) Cellular reactions to gene dosage imbalance: genomic, transcriptomic, and proteomic effects. Trends Genet 24(8):390–397
Wang J, Tian L et al (2006) Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172:507–517
Watterson GA (1983) On the time for gene silencing at duplicate loci. Genetics 105(3):745–766
Werth CR, Windham MD (1991) A model for divergent, allopatric speciation of polyploid Pteridophytes resulting from silencing of duplicate-gene expression. Am Naturalist 137(4):515–526
Winter KU, Weiser C et al (2002) Evolution of class B floral homeotic proteins: obligate heterodimerization orginated from homodimerization. Mol Biol Evol 19(5):587–596
Wolfe KH, Shields DC (1997) Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387:708–713
Wood TE, Takebayashi N et al (2009) The frequency of polyploid speciation in vascular plants. Proc Nat Acad Sci US A 106(33):13875–13879
Woolfe A, Elgar G (2007) Comparative genomics using Fugu reveals insights into regulatory subfunctionalization. Genome Biol 8(4):R53
Yamagata Y, Yamamoto E et al (2010) Mitochondrial gene in the nuclear genome induces reproductive barrier in rice. Proc Nat Acad Sci U S A 107(4):1494–1499
Yang J, Lusk R et al (2003) Organismal complexity, protein complexity, and gene duplicability. Proc Nat Acad Sci U S A 100(26):15661–15665
Yu W-P, Brenner S et al (2003) Duplication, degeneration and subfunctionalization of the nested synapsin-Timp genes in Fugu. Trends Genet 19:180–183
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McGrath, C.L., Lynch, M. (2012). Evolutionary Significance of Whole-Genome Duplication. In: Soltis, P., Soltis, D. (eds) Polyploidy and Genome Evolution. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-31442-1_1
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