Genetics, Vol. 159, 1789-1804, December 2001, Copyright © 2001

The Probability of Preservation of a Newly Arisen Gene Duplicate

Michael Lyncha, Martin O'Helyb, Bruce Walshc, and Allan Forced
a Department of Biology, Indiana University, Bloomington, Indiana 47405,
b Department of Integrative Biology, University of California, Berkeley, California 94720,
c Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721
d Virginia Mason Research Center, Benaroya Research Institute, Seattle, Washington 98101

Corresponding author: Michael Lynch, Department of Biology, Indiana University, Bloomington, IN 47405., mlynch{at}bio.indiana.edu (E-mail)

Communicating editor: M. A. ASMUSSEN

Newly emerging data from genome sequencing projects suggest that gene duplication, often accompanied by genetic map changes, is a common and ongoing feature of all genomes. This raises the possibility that differential expansion/contraction of various genomic sequences may be just as important a mechanism of phenotypic evolution as changes at the nucleotide level. However, the population-genetic mechanisms responsible for the success vs. failure of newly arisen gene duplicates are poorly understood. We examine the influence of various aspects of gene structure, mutation rates, degree of linkage, and population size (N) on the joint fate of a newly arisen duplicate gene and its ancestral locus. Unless there is active selection against duplicate genes, the probability of permanent establishment of such genes is usually no less than 1/(4N) (half of the neutral expectation), and it can be orders of magnitude greater if neofunctionalizing mutations are common. The probability of a map change (reassignment of a key function of an ancestral locus to a new chromosomal location) induced by a newly arisen duplicate is also generally >1/(4N) for unlinked duplicates, suggesting that recurrent gene duplication and alternative silencing may be a common mechanism for generating microchromosomal rearrangements responsible for postreproductive isolating barriers among species. Relative to subfunctionalization, neofunctionalization is expected to become a progressively more important mechanism of duplicate-gene preservation in populations with increasing size. However, even in large populations, the probability of neofunctionalization scales only with the square of the selective advantage. Tight linkage also influences the probability of duplicate-gene preservation, increasing the probability of subfunctionalization but decreasing the probability of neofunctionalization.




This article has been cited by other articles:


Home page
 Proc. Natl. Acad. Sci. USAHome page
M. Semon and K. H. Wolfe
Preferential subfunctionalization of slow-evolving genes after allopolyploidization in Xenopus laevis
PNAS, June 17, 2008; 105(24): 8333 - 8338.
[Abstract] [Full Text] [PDF]

Home page
 Plant Physiol.Home page
J. Sitaraman, M. Bui, and Z. Liu
LEUNIG_HOMOLOG and LEUNIG Perform Partially Redundant Functions during Arabidopsis Embryo and Floral Development
Plant Physiology, June 1, 2008; 147(2): 672 - 681.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
J. F. Storz, F. G. Hoffmann, J. C. Opazo, and H. Moriyama
Adaptive Functional Divergence Among Triplicated {alpha}-Globin Genes in Rodents
Genetics, March 1, 2008; 178(3): 1623 - 1638.
[Abstract] [Full Text] [PDF]

Home page
 Plant Physiol.Home page
C. Lin, B. Shen, Z. Xu, T. G. Kollner, J. Degenhardt, and H. K. Dooner
Characterization of the Monoterpene Synthase Gene tps26, the Ortholog of a Gene Induced by Insect Herbivory in Maize
Plant Physiology, March 1, 2008; 146(3): 940 - 951.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
R. Kafri, O. Dahan, J. Levy, and Y. Pilpel
Preferential protection of protein interaction network hubs in yeast: Evolved functionality of genetic redundancy
PNAS, January 29, 2008; 105(4): 1243 - 1248.
[Abstract] [Full Text] [PDF]

Home page
 Genome ResHome page
D. R. Scannell and K. H. Wolfe
A burst of protein sequence evolution and a prolonged period of asymmetric evolution follow gene duplication in yeast
Genome Res., January 1, 2008; 18(1): 137 - 147.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
X. Wang, H. Tang, J. E. Bowers, F. A. Feltus, and A. H. Paterson
Extensive Concerted Evolution of Rice Paralogs and the Road to Regaining Independence
Genetics, November 1, 2007; 177(3): 1753 - 1763.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
M. W. Hahn, J. P. Demuth, and S.-G. Han
Accelerated Rate of Gene Gain and Loss in Primates
Genetics, November 1, 2007; 177(3): 1941 - 1949.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
E. W. Ganko, B. C. Meyers, and T. J. Vision
Divergence in Expression between Duplicated Genes in Arabidopsis
Mol. Biol. Evol., October 1, 2007; 24(10): 2298 - 2309.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
B. J. Evans
Ancestry Influences the Fate of Duplicated Genes Millions of Years After Polyploidization of Clawed Frogs (Xenopus)
Genetics, June 1, 2007; 176(2): 1119 - 1130.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
M. Lynch
Colloquium Papers: The frailty of adaptive hypotheses for the origins of organismal complexity
PNAS, May 15, 2007; 104(suppl_1): 8597 - 8604.
[Abstract] [Full Text] [PDF]

Home page
 ScienceHome page
Rhesus Macaque Genome Sequencing and Analysis Cons, R. A. Gibbs, J. Rogers, M. G. Katze, R. Bumgarner, G. M. Weinstock, E. R. Mardis, K. A. Remington, R. L. Strausberg, J. C. Venter, et al.
Evolutionary and Biomedical Insights from the Rhesus Macaque Genome
Science, April 13, 2007; 316(5822): 222 - 234.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
S. O. Sassi, E. L. Braun, and S. A. Benner
The Evolution of Seminal Ribonuclease: Pseudogene Reactivation or Multiple Gene Inactivation Events?
Mol. Biol. Evol., April 1, 2007; 24(4): 1012 - 1024.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
P. Labbe, A. Berthomieu, C. Berticat, H. Alout, M. Raymond, T. Lenormand, and M. Weill
Independent Duplications of the Acetylcholinesterase Gene Conferring Insecticide Resistance in the Mosquito Culex pipiens
Mol. Biol. Evol., April 1, 2007; 24(4): 1056 - 1067.
[Abstract] [Full Text] [PDF]

Home page
 Plant CellHome page
S. Bezhani, C. Winter, S. Hershman, J. D. Wagner, J. F. Kennedy, C. S. Kwon, J. Pfluger, Y. Su, and D. Wagner
Unique, Shared, and Redundant Roles for the Arabidopsis SWI/SNF Chromatin Remodeling ATPases BRAHMA and SPLAYED
PLANT CELL, February 1, 2007; 19(2): 403 - 416.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
J. C. Preston and E. A. Kellogg
Reconstructing the Evolutionary History of Paralogous APETALA1/FRUITFULL-Like Genes in Grasses (Poaceae)
Genetics, September 1, 2006; 174(1): 421 - 437.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
T. H. Oakley, B. Ostman, and A. C. V. Wilson
Repression and loss of gene expression outpaces activation and gain in recently duplicated fly genes
PNAS, August 1, 2006; 103(31): 11637 - 11641.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
M. Benderoth, S. Textor, A. J. Windsor, T. Mitchell-Olds, J. Gershenzon, and J. Kroymann
Positive selection driving diversification in plant secondary metabolism
PNAS, June 13, 2006; 103(24): 9118 - 9123.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
J. Petersen, R. Teich, B. Becker, R. Cerff, and H. Brinkmann
The GapA/B Gene Duplication Marks the Origin of Streptophyta (Charophytes and Land Plants)
Mol. Biol. Evol., June 1, 2006; 23(6): 1109 - 1118.
[Abstract] [Full Text] [PDF]

Home page
 Plant Physiol.Home page
A. J. Windsor, M. E. Schranz, N. Formanova, S. Gebauer-Jung, J. G. Bishop, D. Schnabelrauch, J. Kroymann, and T. Mitchell-Olds
Partial Shotgun Sequencing of the Boechera stricta Genome Reveals Extensive Microsynteny and Promoter Conservation with Arabidopsis.
Plant Physiology, April 1, 2006; 140(4): 1169 - 1182.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
G. Zhang, M. M. Miyamoto, and M. J. Cohn
Lamprey type II collagen and Sox9 reveal an ancient origin of the vertebrate collagenous skeleton
PNAS, February 28, 2006; 103(9): 3180 - 3185.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
B. A. Chapman, J. E. Bowers, F. A. Feltus, and A. H. Paterson
Buffering of crucial functions by paleologous duplicated genes may contribute cyclicality to angiosperm genome duplication
PNAS, February 21, 2006; 103(8): 2730 - 2735.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
S.-H. Shiu, J. K. Byrnes, R. Pan, P. Zhang, and W.-H. Li
Role of positive selection in the retention of duplicate genes in mammalian genomes
PNAS, February 14, 2006; 103(7): 2232 - 2236.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
M. Lynch
The Origins of Eukaryotic Gene Structure
Mol. Biol. Evol., February 1, 2006; 23(2): 450 - 468.
[Abstract] [Full Text] [PDF]

Home page
 Nucleic Acids ResHome page
I. Paulsen and A. von Haeseler
INVHOGEN: a database of homologous invertebrate genes
Nucleic Acids Res., January 1, 2006; 34(suppl_1): D349 - D353.
[Abstract] [Full Text] [PDF]

Home page
 Protein Sci.Home page
M. Lynch
Simple evolutionary pathways to complex proteins
Protein Sci., September 1, 2005; 14(9): 2217 - 2225.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
A. L. Hughes
Gene duplication and the origin of novel proteins
PNAS, June 21, 2005; 102(25): 8791 - 8792.
[Full Text] [PDF]

Home page
 BioinformaticsHome page
J.-F. Dufayard, L. Duret, S. Penel, M. Gouy, F. Rechenmann, and G. Perriere
Tree pattern matching in phylogenetic trees: automatic search for orthologs or paralogs in homologous gene sequence databases
Bioinformatics, June 1, 2005; 21(11): 2596 - 2603.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
C. D. Jones, A. W. Custer, and D. J. Begun
Origin and Evolution of a Chimeric Fusion Gene in Drosophila subobscura, D. madeirensis and D. guanche
Genetics, May 1, 2005; 170(1): 207 - 219.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
A. Force, W. A. Cresko, F. B. Pickett, S. R. Proulx, C. Amemiya, and M. Lynch
The Origin of Subfunctions and Modular Gene Regulation
Genetics, May 1, 2005; 170(1): 433 - 446.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
M. Lynch, D. G. Scofield, and X. Hong
The Evolution of Transcription-Initiation Sites
Mol. Biol. Evol., April 1, 2005; 22(4): 1137 - 1146.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
C. Dale, T. Jones, and M. Pontes
Degenerative Evolution and Functional Diversification of Type-III Secretion Systems in the Insect Endosymbiont Sodalis glossinidius
Mol. Biol. Evol., March 1, 2005; 22(3): 758 - 766.
[Abstract] [Full Text] [PDF]

Home page
 J. Biol. Chem.Home page
A. S. Rahman, J. Hothersall, J. Crosby, T. J. Simpson, and C. M. Thomas
Tandemly Duplicated Acyl Carrier Proteins, Which Increase Polyketide Antibiotic Production, Can Apparently Function Either in Parallel or in Series
J. Biol. Chem., February 25, 2005; 280(8): 6399 - 6408.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
K. Thornton and M. Long
Excess of Amino Acid Substitutions Relative to Polymorphism Between X-Linked Duplications in Drosophila melanogaster
Mol. Biol. Evol., February 1, 2005; 22(2): 273 - 284.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
R. C. Moore, S. R. Grant, and M. D. Purugganan
Molecular Population Genetics of Redundant Floral-Regulatory Genes in Arabidopsis thaliana
Mol. Biol. Evol., January 1, 2005; 22(1): 91 - 103.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
C. Guillet-Claude, N. Isabel, B. Pelgas, and J. Bousquet
The Evolutionary Implications of knox-I Gene Duplications in Conifers: Correlated Evidence from Phylogeny, Gene Mapping, and Analysis of Functional Divergence
Mol. Biol. Evol., December 1, 2004; 21(12): 2232 - 2245.
[Abstract] [Full Text] [PDF]

Home page
 ScienceHome page
M. Lynch and J. S. Conery
Response to Comment on "The Origins of Genome Complexity"
Science, November 5, 2004; 306(5698): 978b - 978b.
[Full Text] [PDF]

Home page
 Infect. Immun.Home page
L. Giacani, E. S. Sun, K. Hevner, B. J. Molini, W. C. Van Voorhis, S. A. Lukehart, and A. Centurion-Lara
Tpr Homologs in Treponema paraluiscuniculi Cuniculi A Strain
Infect. Immun., November 1, 2004; 72(11): 6561 - 6576.
[Abstract] [Full Text] [PDF]

Home page
 Protein Sci.Home page
M. J. Behe and D. W. Snoke
Simulating evolution by gene duplication of protein features that require multiple amino acid residues
Protein Sci., October 22, 2004; 13(10): 2651 - 2664.
[Abstract] [Full Text] [PDF]

Home page
 Genome ResHome page
L. Huminiecki and K. H. Wolfe
Divergence of Spatial Gene Expression Profiles Following Species-Specific Gene Duplications in Human and Mouse
Genome Res., October 1, 2004; 14(10a): 1870 - 1879.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
C.-T. Ting, S.-C. Tsaur, S. Sun, W. E. Browne, Y.-C. Chen, N. H. Patel, and C.-I Wu
Gene duplication and speciation in Drosophila: Evidence from the Odysseus locus
PNAS, August 17, 2004; 101(33): 12232 - 12235.
[Abstract] [Full Text] [PDF]

Home page
 Plant Physiol.Home page
R. D'Ovidio, A. Raiola, C. Capodicasa, A. Devoto, D. Pontiggia, S. Roberti, R. Galletti, E. Conti, D. O'Sullivan, and G. De Lorenzo
Characterization of the Complex Locus of Bean Encoding Polygalacturonase-Inhibiting Proteins Reveals Subfunctionalization for Defense against Fungi and Insects
Plant Physiology, August 1, 2004; 135(4): 2424 - 2435.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
R. Friedman and A. L. Hughes
Two Patterns of Genome Organization in Mammals: the Chromosomal Distribution of Duplicate Genes in Human and Mouse
Mol. Biol. Evol., June 1, 2004; 21(6): 1008 - 1013.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
M. J. Clauss and T. Mitchell-Olds
Functional Divergence in Tandemly Duplicated Arabidopsis thaliana Trypsin Inhibitor Genes
Genetics, March 1, 2004; 166(3): 1419 - 1436.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
R. C. Moore and M. D. Purugganan
The early stages of duplicate gene evolution
PNAS, December 23, 2003; 100(26): 15682 - 15687.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
V. Katju and M. Lynch
The Structure and Early Evolution of Recently Arisen Gene Duplicates in the Caenorhabditis elegans Genome
Genetics, December 1, 2003; 165(4): 1793 - 1803.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
J. Kroymann, S. Donnerhacke, D. Schnabelrauch, and T. Mitchell-Olds
Evolutionary dynamics of an Arabidopsis insect resistance quantitative trait locus
PNAS, November 25, 2003; 100(suppl_2): 14587 - 14592.
[Abstract] [Full Text]

Home page
 ScienceHome page
M. Lynch and J. S. Conery
The Origins of Genome Complexity
Science, November 21, 2003; 302(5649): 1401 - 1404.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
L. P. Martinez-Castilla and E. R. Alvarez-Buylla
Adaptive evolution in the Arabidopsis MADS-box gene family inferred from its complete resolved phylogeny
PNAS, November 11, 2003; 100(23): 13407 - 13412.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
F. Rodriguez-Trelles, R. Tarrio, and F. J. Ayala
Convergent neofunctionalization by positive Darwinian selection after ancient recurrent duplications of the xanthine dehydrogenase gene
PNAS, November 11, 2003; 100(23): 13413 - 13417.
[Abstract] [Full Text] [PDF]

Home page
 Genome ResHome page
D. P. Mortlock, C. Guenther, and D. M. Kingsley
A General Approach for Identifying Distant Regulatory Elements Applied to the Gdf6 Gene
Genome Res., September 1, 2003; 13(9): 2069 - 2081.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
C. G. Kurland, B. Canback, and O. G. Berg
Horizontal gene transfer: A critical view
PNAS, August 19, 2003; 100(17): 9658 - 9662.
[Abstract] [Full Text] [PDF]

Home page
 J. Immunol.Home page
C. K. Doyle, B. K. Davis, R. G. Cook, R. R. Rich, and J. R. Rodgers
Hyperconservation of the N-Formyl Peptide Binding Site of M3: Evidence that M3 Is an Old Eutherian Molecule with Conserved Recognition of a Pathogen-Associated Molecular Pattern
J. Immunol., July 15, 2003; 171(2): 836 - 844.
[Abstract] [Full Text] [PDF]

Home page
 Genome ResHome page
A. L. Hughes and R. Friedman
Parallel Evolution by Gene Duplication in the Genomes of Two Unicellular Fungi
Genome Res., May 1, 2003; 13(5): 794 - 799.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
K. L. Adams, R. Cronn, R. Percifield, and J. F. Wendel
Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing
PNAS, April 15, 2003; 100(8): 4649 - 4654.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
L. C. Hileman and D. A. Baum
Why Do Paralogs Persist? Molecular Evolution of CYCLOIDEA and Related Floral Symmetry Genes in Antirrhineae (Veronicaceae)
Mol. Biol. Evol., April 1, 2003; 20(4): 591 - 600.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
R. Friedman and A. L. Hughes
The Temporal Distribution of Gene Duplication Events in a Set of Highly Conserved Human Gene Families
Mol. Biol. Evol., January 1, 2003; 20(1): 154 - 161.
[Abstract] [Full Text] [PDF]

Home page
 Plant CellHome page
S. Ferrari, D. Vairo, F. M. Ausubel, F. Cervone, and G. De Lorenzo
Tandemly Duplicated Arabidopsis Genes That Encode Polygalacturonase-Inhibiting Proteins Are Regulated Coordinately by Different Signal Transduction Pathways in Response to Fungal Infection
PLANT CELL, January 1, 2003; 15(1): 93 - 106.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
O. G. Berg and C. G. Kurland
Evolution of Microbial Genomes: Sequence Acquisition and Loss
Mol. Biol. Evol., December 1, 2002; 19(12): 2265 - 2276.
[Abstract] [Full Text] [PDF]

Home page
 Genome ResHome page
V. Nembaware, K. Crum, J. Kelso, and C. Seoighe
Impact of the Presence of Paralogs on Sequence Divergence in a Set of Mouse-Human Orthologs
Genome Res., September 1, 2002; 12(9): 1370 - 1376.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
M. Lynch
Intron evolution as a population-genetic process
PNAS, April 30, 2002; 99(9): 6118 - 6123.
[Abstract] [Full Text] [PDF]