Role of selection in fixation of gene duplications
Abstract
New genes commonly appear through complete or partial duplications of pre-existing genes. Duplications of long DNA segments are constantly produced by rare mutations, may become fixed in a population by selection or random drift, and are subject to divergent evolution of the paralogous sequences after fixation, although gene conversion can impede this process. New data shed some light on each of these processes. Mutations which involve duplications can occur through at least two different mechanisms, backward strand slippage during DNA replication and unequal crossing-over. The background rate of duplication of a complete gene in humans is 10(-9)-10(-10) per generation, although many genes located within hot-spots of large-scale mutation are duplicated much more often. Many gene duplications affect fitness strongly, and are responsible, through gene dosage effects, for a number of genetic diseases. However, high levels of intrapopulation polymorphism caused by presence or absence of long, gene-containing DNA segments imply that some duplications are not under strong selection. The polymorphism to fixation ratios appear to be approximately the same for gene duplications and for presumably selectively neutral nucleotide substitutions, which, according to the McDonald-Kreitman test, is consistent with selective neutrality of duplications. However, this pattern can also be due to negative selection against most of segregating duplications and positive selection for at least some duplications which become fixed. Patterns in post-fixation evolution of duplicated genes do not easily reveal the causes of fixations. Many gene duplications which became fixed recently in a variety of organisms were positively selected because the increased expression of the corresponding genes was beneficial. The effects of gene dosage provide a unified framework for studying all phases of the life history of a gene duplication. Application of well-known methods of evolutionary genetics to accumulating data on new, polymorphic, and fixed duplication will enhance our understanding of the role of natural selection in the evolution by gene duplication.
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In S. cerevisiae, cobalt resistance also improved tolerance for other metal ions, and pulsed cobalt stress exposure during laboratory evolution resulted in evolutionary cross-protection to thermal and oxidative stress.
“Examples for adaptive cross-protection are also available for S. cerevisiae where cobalt resistance also improved tolerance for other metal ions and pulsed cobalt stress exposure during laboratory evolution even resulted in evolutionary cross-protection to thermal and oxidative stress [114].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [114]
Other studies used ethylmethanesulfonate (EMS) treated Bacillus boroniphilus to select for increased boron resistance or EMS-treated S. cerevisiae in order to achieve increased nutrient utilization and stress resistance.
“Other studies used ethylmethanesulfonate (EMS) treated Bacillus boroniphilus to select for increased boron resistance [88] or EMS-treated S. cerevisiae in order to achieve increased nutrient utilization and stress resistance [95,113,114].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [114]
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The evolution of gene duplications: classifying and distinguishing between models
Innan, H., & Kondrashov, F. (2010) · Nature reviews genetics · doi:10.1038/nrg2689 · Cited by 1,320 · see citing works
“However, as data from eukaryotes became more widely available, authors started to relate dosage and gene duplications in multicellular organism”
BackgroundSelf-citationTurning a hobby into a job: How duplicated genes find new functions
Conant, G. C., & Wolfe, K. H. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2482 · Cited by 1,281 · see citing works
“Duplicate gene pairs can also be preserved by selection for increased gene dosag”
BackgroundAdaptive laboratory evolution—Principles and applications for biotechnology
Dragosits, M., & Mattanovich, D. (2013) · Microbial Cell Factories · doi:10.1186/1475-2859-12-64 · Cited by 827 · see citing works
“Whereas there is an ongoing debate about the long-term fixation of gene duplications, either by their selective advantage under selection pressure, or by selective neutrality and fixation by random drift, they are a prerequisite for the development of novel molecular functions [129-131].”
BackgroundGene duplication as a mechanism of genomic adaptation to a changing environment
Kondrashov, F. A. (2012) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2012.1108 · Cited by 639 · see citing works
Self-citationDistinguishing Among Evolutionary Models for the Maintenance of Gene Duplicates
Hahn, M. W. (2009) · Journal of Heredity · doi:10.1093/jhered/esp047 · Cited by 415 · see citing works
“Multiple authors have also recently proposed that this is a major force in duplicate gene retention (Kondrashov et al. 2002; Kondrashov and Kondrashov 2006; Sugino and Innan 2006).”
BackgroundGene and genome duplications: the impact of dosage-sensitivity on the fate of nuclear genes
Edger, P. P., & Pires, J. C. (2009) · Chromosome Research · doi:10.1007/s10577-009-9055-9 · Cited by 389 · see citing works
“This is the theoretical basis of the Increased Gene Dosage Hypothesis (Seoighe and Wolfe 1999; Kondrashov and Kondrashov 2006; Conant and Wolfe 2007; Conant and Wolfe 2008).”
BackgroundGene retention, fractionation and subgenome differences in polyploid plants
Cheng, F., Wu, J., Cai, X., Liang, J., Freeling, M., & Wang, X. (2018) · Nature Plants · doi:10.1038/s41477-018-0136-7 · Cited by 391 · see citing works
The gain and loss of genes during 600 million years of vertebrate evolution
Blomme, T., Vandepoele, K., Bodt, S. D., Simillion, C., Maere, S., & de Peer, Y. V. (2006) · Genome biology · doi:10.1186/gb-2006-7-5-r43 · Cited by 383 · see citing works
“A general overview of the mechanisms of gene duplication and retention can be found in [42,43].”
BackgroundConant, G. C., Birchler, J. A., & Pires, J. C. (2014) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2014.05.008 · Cited by 303 · see citing works
“Sequence divergence [52,53], between duplicates has been attributed to altered function models [54]; however, divergence is also compatible with dosage hypotheses because new effective balances or advantageous absolute dosages could evolve.”
BackgroundRarely successful polyploids and their legacy in plant genomes
Arrigo, N., & Barker, M. S. (2012) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2012.03.010 · Cited by 260 · see citing works
“Alternatively, there may be selection for increases or decreases in raw copy number of particular gene families that lead to biased patterns of retention and loss [64,65].”
BackgroundBias of Selection on Human Copy-Number Variants
Nguyen, D.-Q., Webber, C., & Ponting, C. P. (2006) · PLoS Genetics · doi:10.1371/journal.pgen.0020020 · Cited by 255 · see citing works
Natural Selection Shapes Genome-Wide Patterns of Copy-Number Polymorphism in Drosophila melanogaster
Emerson, J. J., Cardoso-Moreira, M., Borevitz, J., & Long, M. (2008) · Science · doi:10.1126/science.1158078 · Cited by 250 · see citing works
Retention of duplicated genes in evolution
Kuzmin, E., Taylor, J. S., & Boone, C. M. (2021) · Trends in Genetics · doi:10.1016/j.tig.2021.06.016 · Cited by 227 · see citing works
Multiple large-scale gene and genome duplications during the evolution of hexapods
Li, Z., Tiley, G. P., Galuska, S. R., Reardon, C. R., Kidder, T. I., Rundell, R. J., & Barker, M. S. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1710791115 · Cited by 197 · see citing works
“Although neo- and subfunctionalization are also important in duplicate gene retention, only the DBH predicts a convergent pattern of gene retention following polyploidy across multiple species (44, 45).”
BackgroundLow pesticide rates may hasten the evolution of resistance by increasing mutation frequencies
Gressel, J. (2010) · Pest Management Science · doi:10.1002/ps.2071 · Cited by 195 · see citing works
Patterns and Processes of Diploidization in Land Plants
Li, Z., McKibben, M. T. W., Finch, G., Blischak, P. D., Sutherland, B. L., & Barker, M. S. (2021) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-050718-100344 · Cited by 186 · see citing works
Pervasive and Persistent Redundancy among Duplicated Genes in Yeast
Dean, E., Davis, J. C., Davis, R. W., & Petrov, D. A. (2008) · PLoS Genetics · doi:10.1371/journal.pgen.1000113 · Cited by 173 · see citing works
“why does subfunctionalization not proceed to completion)? One possibility is that functional similarity within the duplicate pair is maintained by selection for its effect on the level, rate, dynamics, or noisiness of expression [32–39].”
BackgroundCopy number variation in the bovine genome
Fadista, J., Thomsen, B., Holm, L., & Bendixen, C. (2010) · BMC Genomics · doi:10.1186/1471-2164-11-284 · Cited by 168 · see citing works
“This result, as for the over represented set of 'environmental response' genes, might indicate a relaxation of constrains due to the redundancy expected from the variable number of gene copies [58-61].”
Functional Analysis of Gene Duplications in Saccharomyces cerevisiae
Guan, Y., Dunham, M. J., & Troyanskaya, O. G. (2006) · Genetics · doi:10.1534/genetics.106.064329 · Cited by 163 · see citing works
Chang, D., & Duda, T. F. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss068 · Cited by 157 · see citing works
Backup without redundancy: genetic interactions reveal the cost of duplicate gene loss
Ihmels, J., Collins, S. R., Schuldiner, M., Krogan, N. J., & Weissman, J. S. (2007) · Molecular Systems Biology · doi:10.1038/msb4100127 · Cited by 151 · see citing works
“…data are available, the observation that the relationship between coexpression, abundance and abundance similarity holds on a genomic scale supports the role of dosage amplification for a significant subset of duplicates in the genome (Seoighe and Wolfe, 1999; Kondrashov and Kondrashov, 2006).”
BackgroundDragosits, M., Mozhayskiy, V., Quiñones-Soto, S., Park, J., & Tagkopoulos, I. (2013) · Molecular Systems Biology · doi:10.1038/msb.2012.76 · Cited by 145 · see citing works
“evolution of novel functions (Kondrashov and Kondrashov, 2006; Bergthorsson et al, 2007).”
ResultBekaert, M., Edger, P. P., Pires, J. C., & Conant, G. C. (2011) · The Plant Cell · doi:10.1105/tpc.110.081281 · Cited by 140 · see citing works
“Such selection has been observed for duplicate genes froma variety of organisms (Kondrashov and Kondrashov, 2006), including plants (vanHoof et al., 2001;Widholm et al., 2001).”
BackgroundA portrait of copy-number polymorphism in Drosophila melanogaster
Dopman, E. B., & Hartl, D. L. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0709888104 · Cited by 136 · see citing works
Sezutsu, H., Goff, G. L., & Feyereisen, R. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0428 · Cited by 124 · see citing works
Retroposition and evolution of the DNA-binding motifs of YY1, YY2 and REX1
Kim, J. D., Faulk, C. D., & Kim, J.-H. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm235 · Cited by 122 · see citing works
“Successful gene duplication is still regarded as a rare evolutionary event (37), which is further supported by the single-copy status of YY1 in the majority of animal lineages.”
Palacios, Ò., Pagani, M. A., Pérez‐Rafael, S., Egg, M., Höckner, M., Kloss‐Brandstätter, A., Capdevila, M., Atrian, S., & Dallinger, R. (2011) · BMC Biology · doi:10.1186/1741-7007-9-4 · Cited by 118 · see citing works
“towards evolution of specific features [42].”
Mandáková, T. M., Li, Z., Barker, M. S., & Lysák, M. A. (2017) · The Plant Journal · doi:10.1111/tpj.13553 · Cited by 113 · see citing works
“Among the many hypotheses for duplicate gene retention (Kondrashov and Kondrashov, 2006; Freeling, 2009), the DBH is the only hypothesis that explicitly predicts the parallel retention and loss of functionally related genes across species following WGD (Freeling and Thomas, 2006; Freeling, 2009; Conant et al.”
BackgroundExploring whole-genome duplicate gene retention with complex genetic interaction analysis
Kuzmin, E., VanderSluis, B., Ba, A. N. N., Wang, W., Koch, E. N., Ušaj, M., Khmelinskii, A., Ušaj, M. M., van Leeuwen, J. S., Kraus, O. Z., et al. (2020) · Science · doi:10.1126/science.aaz5667 · Cited by 109 · see citing works
Genetic interactions reveal the evolutionary trajectories of duplicate genes
VanderSluis, B., Bellay, J., Musso, G., Costanzo, M., Papp, B., Vizeacoumar, F. J., Baryshnikova, A., Andrews, B., Boone, C., & Myers, C. L. (2010) · Molecular Systems Biology · doi:10.1038/msb.2010.82 · Cited by 110 · see citing works
“…because of their functional divergence (Ohno, 1970; Hughes, 1994; Force et al, 1999; Conant and Wolfe, 2008; Marques et al, 2008) from those pairs retained because increased gene dosage is beneficial to the organism (Kondrashov and Kondrashov, 2006; Conant and Wolfe, 2007; Ihmels et al, 2007).”
BackgroundLevasseur, A., & Pontarotti, P. (2011) · Biology Direct · doi:10.1186/1745-6150-6-11 · Cited by 107 · see citing works
“However, the rate of fixation of duplications cannot be used a priori to estimate rate of mutational origin [14].”
BackgroundMolecular mechanisms of paralogous compensation and the robustness of cellular networks
Diss, G., Ascencio, D., DeLuna, A., & Landry, C. R. (2013) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.22555 · Cited by 105 · see citing works
“Some duplicate pairs may be retained even as fully functionally redundant duplicates because of beneficial dosage amplification effects (Kondrashov et al., 2002; Kondrashov and Kondrashov, 2006; Tang and Amon, 2013).”
Tetrahymena Metallothioneins Fall into Two Discrete Subfamilies
Díaz, S., Amaro, F., Rico, D., Campos, V., Benı́tez, L., Martín‐González, A., Hamilton, E. P., Orias, E., & Gutiérrez, J. C. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000291 · Cited by 100 · see citing works
Multilevel populations and the evolution of antibiotic resistance through horizontal gene transfer
Andam, C. P., Fournier, G. P., & Gogarten, J. P. (2011) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2011.00274.x · Cited by 95 · see citing works
“Redundant genes found in the same genome are likely a result of recent duplication or horizontal acquisition and may be maintained if there is selective advantage to retain both copies (Kondrashov & Kondrashov, 2006).”
BackgroundConstructive Neutral Evolution 20 Years Later
Muñoz-Gómez, S. A., Bilolikar, G., Wideman, J. G., & Geiler‐Samerotte, K. (2021) · Journal of Molecular Evolution · doi:10.1007/s00239-021-09996-y · Cited by 94 · see citing works
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Gene duplication and the evolution of moonlighting proteins
Espinosa‐Cantú, A., Ascencio, D., Barona‐Gómez, F., & DeLuna, A. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00227 · Cited by 84 · see citing works
Tracking the evolution of a cold stress associated gene family in cold tolerant grasses
Sandve, S. R., Rudi, H., Asp, T., & Rognli, O. A. (2008) · BMC Evolutionary Biology · doi:10.1186/1471-2148-8-245 · Cited by 85 · see citing works
“The evolution of gene families per se is in itself a much debated topic, and gene family expansion and subsequent functional diversification is thought to have been a significant factor contributing to adaptations to new environments [16,17].”
BackgroundGene Dosage and Gene Duplicability
Qian, W., & Zhang, J. (2008) · Genetics · doi:10.1534/genetics.108.090936 · Cited by 83 · see citing works
“Recently, it was proposed that the fixation process is frequently driven by positive selection for enhanced gene dosage brought about by gene duplication (Kondrashov and Koonin 2004; Kondrashov and Kondrashov 2006).”
BackgroundAssogba, B. S., Milesi, P., Djogbénou, L., Berthomieu, A., Makoundou, P., Baba-Moussa, L. S., Fiston-Lavier, A.-S., Belkhir, K., Labbé, P., & Weill, M. (2016) · PLoS Biology · doi:10.1371/journal.pbio.2000618 · Cited by 77 · see citing works
“However, homogeneous duplications are also often associated with deleterious pleiotropic effects (or selective costs), probably due to the disruption of biochemical balance or overproduction costs ([12], e.”
BackgroundEvolutionary biology through the lens of budding yeast comparative genomics
Marsit, S., Leducq, J., Durand, É., Marchant, A., Filteau, M., & Landry, C. R. (2017) · Nature Reviews Genetics · doi:10.1038/nrg.2017.49 · Cited by 72 · see citing works
Protein engineering: opportunities and challenges
LEISOLA, M. S. A., & Turunen, O. (2007) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-007-0964-2 · Cited by 72 · see citing works
“Positive selection may be needed to retain the duplicated genes in the population (Ohta 2002; Kondrashov and Kondrashov 2006; Shiu et al. 2006).”
BackgroundEvidence for the fixation of gene duplications by positive selection in DrosophilaPreprint
Cardoso-Moreira, M., Arguello, J. R., Gottipati, S., Harshman, L. G., Grenier, J. K., & Clark, A. G. (2016) · Genome Research · doi:10.1101/gr.199323.115 · Cited by 71 · see citing works
Sandve, S. R., & Fjellheim, S. (2010) · Molecular Ecology · doi:10.1111/j.1365-294x.2010.04629.x · Cited by 71 · see citing works
“Selection for lineage specific expansion of individual gene families can also play an important role in adaptive evolution (Kondrashov & Kondrashov 2006; Chen et al. 2008; Zou et al. 2009).”
BackgroundMultiple chaperonins in bacteria—novel functions and non-canonical behaviors
Kumar, C. M. S., Mande, S. C., & Mahajan, G. (2015) · Cell Stress and Chaperones · doi:10.1007/s12192-015-0598-8 · Cited by 63 · see citing works
“The organism expressing multiple GroELs might benefit either from the dosage effect of multiple chaperonins (Kondrashov and Kondrashov 2006) or from the functional divergence of different chaperonins (Goyal et al. 2006).”
Evolutionary novelties: the making and breaking of pleiotropic constraints
Galis, F. F., & Metz, J. A. J. (2007) · Integrative and Comparative Biology · doi:10.1093/icb/icm081 · Cited by 64 · see citing works
Metabolic peculiarities of Aspergillus niger disclosed by comparative metabolic genomics
Sun, J., Lü, X., Rinas, U., & Zeng, A. (2007) · Genome biology · doi:10.1186/gb-2007-8-9-r182 · Cited by 64 · see citing works
“Additional or different copies of genes can strengthen certain pathways or enhance the robustness of the regulation to adapt to different environments [25,26].”
BackgroundProtein subcellular relocalization: a new perspective on the origin of novel genes
McKay, S., & Geeta, R. (2007) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2007.05.002 · Cited by 61 · see citing works
Escape from Adaptive Conflict follows from weak functional trade-offs and mutational robustness
Sikosek, T., Chan, H. S., & Bornberg‐Bauer, E. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1115620109 · Cited by 61 · see citing works
“Under such a positive dosage model (38, 39), gene duplication is beneficial, especially when suboptimal (promiscuous) functions are involved (40).”
BackgroundRapid repetitive element-mediated expansion of piRNA clusters in mammalian evolution
Assis, R., & Kondrashov, A. S. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900523106 · Cited by 60 · see citing works
“More generally, long insertions are unlikely to be selectively neutral, and only beneficial ones can be fixed (19).”
BackgroundSelf-citationLopes‐Marques, M., Kabeya, N., Yu, Q., Ruivo, R., Santos, M. M., Venkatesh, B., Tocher, D. R., Castro, L. F. C., & Monroig, Ó. (2018) · BMC Evolutionary Biology · doi:10.1186/s12862-018-1271-5 · Cited by 57 · see citing works
Why did the acquired immune system of vertebrates evolve?
Rolff, J. (2006) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2006.08.009 · Cited by 57 · see citing works
“Whilst this is plausible, recent theoretical work suggests that genome duplications arise not through neutral processes, but are much more likely to be driven by selection acting shortly before, during, and immediately after duplication events [22,23].”
BackgroundEvolutionary and Functional Features of Copy Number Variation in the Cattle Genome1
Keel, B. N., Lindholm‐Perry, A. K., & Snelling, W. M. (2016) · Frontiers in Genetics · doi:10.3389/fgene.2016.00207 · Cited by 53 · see citing works
“It has been argued in previous studies that copy number variation is the result of positive selection for a diverse set of proteins that canmeet the challenges of a constantly changing environment (Kondrashov and Kondrashov, 2006).”
BackgroundTandem duplications lead to novel expression patterns through exon shuffling in Drosophila yakuba
Rogers, R. L., Shao, L., & Thornton, K. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006795 · Cited by 53 · see citing works
“Pesticide resistance genes have been reported to have changes in gene dosage after duplication (reviewed in [6]).”
BackgroundResultInfluentialIdentification of genome-wide copy number variations among diverse pig breeds by array CGH
Li, Y., Mei, S., Zhang, X., Peng, X., Liu, G., Tao, H., Wu, H., Jiang, S., Xiong, Y., & Li, F. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-725 · Cited by 49 · see citing works
“It might indicate a relaxation of purifying selection due to the redundancy fragments generated during the formation process of the variable number of genes [39-42].”
BackgroundYang, X., Zhao, X., Li, C., Liu, J., Qiu, Z., Dong, Y., & Wang, Y. (2015) · PLANT PHYSIOLOGY · doi:10.1104/pp.15.01181 · Cited by 46 · see citing works
“…retain a considerable degree of expressional or functional similarity over very long periods, which is usually assumed due to purifying selection maintaining the ancestral function in both duplicates (Lynch and Conery, 2000; Kondrashov and Kondrashov, 2006; Dean et al., 2008; Vavouri et al., 2008).”
BackgroundZhu, H., Han, X., Lv, J., Zhao, L., Xu, X., Zhang, T., & Guo, W. (2011) · BMC Plant Biology · doi:10.1186/1471-2229-11-40 · Cited by 46 · see citing works
“Second, the multiple copies can contribute to an increase in the gene expression level [42,43] or both copies can suffer mutations but the combined action of both gene copies is necessary to maintain original function and expression levels (subfunctionalization) [40,44,45].”
BackgroundIntegrating Networks, Phylogenomics, and Population Genomics for the Study of Polyploidy
Blischak, P. D., Mabry, M. E., Conant, G. C., & Pires, J. C. (2018) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-121415-032302 · Cited by 44 · see citing works
Genome-wide copy number variations in Oryza sativa L.
Yu, P., Wang, C., Xu, Q. J., Feng, Y., Yuan, X., Yu, H., Wang, Y.-P., Tang, S.-X., & Wei, X. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-649 · Cited by 43 · see citing works
“This result, as for the over-represented set of disease resistance genes, might indicate a relaxation of constraints because of the redundancy expected from the variable number of gene copies [77,78].”
BackgroundCridland, J. M., & Thornton, K. (2010) · Genome Biology and Evolution · doi:10.1093/gbe/evq001 · Cited by 43 · see citing works
Differential Retention of Metabolic Genes Following Whole-Genome Duplication
Goût, J.-F., Duret, L., & Kahn, D. (2009) · Molecular Biology and Evolution · doi:10.1093/molbev/msp026 · Cited by 42 · see citing works
GENE-DOSAGE EFFECTS ON FITNESS IN RECENT ADAPTIVE DUPLICATIONS:ace-1IN THE MOSQUITOCULEX PIPIENS
Labbé, P., Milesi, P., Yébakima, A., Pasteur, N., Weill, M., & Lenormand, T. (2014) · Evolution · doi:10.1111/evo.12372 · Cited by 41 · see citing works
“Several authors suggested that selection plays a role in early duplication evolution, that is, in their initial fixation (segregation avoidance models; Haldane 1954; Spofford 1969) rather than chance (Ohno 1970; Walsh 1995; Zhang 2003; Kondrashov and Kondrashov 2006).”
BackgroundRegulatory back-up circuit of medaka Wt1 co-orthologs ensures PGC maintenance
Klüver, N., Herpin, A., Braasch, I., Drieβle, J., & Schartl, M. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.10.009 · Cited by 40 · see citing works
“Nevertheless, in many cases where both copies of a duplicated gene have still been retained, it is assumed that a duplication is preserved due to a direct impact on fitness or partially redundant function(s) (Kondrashov and Kondrashov, 2006; Ohno, 1970).”
BackgroundEvolution of Gene Regulatory Networks by Fluctuating Selection and Intrinsic Constraints
Tsuda, M. E., & Kawata, M. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000873 · Cited by 36 · see citing works
“Several studies have proposed that gene deletion rates could be several times higher than gene duplication rates [47,48].”
BackgroundAcharya, D., & Ghosh, T. C. (2016) · BMC Genomics · doi:10.1186/s12864-016-2392-0 · Cited by 36 · see citing works
“The retention of duplicates might be initially favourable due to circumstances like increased gene dosage advantage, where the duplication and subsequent increase in the gene product may be advantageous to the organism [5, 8].”
BackgroundAncient Gene Paralogy May Mislead Inference of Plastid Phylogeny
Qiu, H., Yang, E. C., Bhattacharya, D., & Yoon, H. S. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss137 · Cited by 36 · see citing works
“This evolutionary strategy is consistent with the gene dosage hypothesis, whereby duplicated genes are retained to enhance the dosage of a critical gene product (Kondrashov and Koonin 2004; Kondrashov and Kondrashov 2006; Hahn 2009).”
ResultGene Age Predicts the Strength of Purifying Selection Acting on Gene Expression Variation in Humans
Popadin, K. Y., Gutiérrez‐Arcelus, M., Lappalainen, T., Buil, A., Steinberg, J., Nikolaev, S. I., Lukowski, S. W., Bazykin, G. A., Seplyarskiy, V. B., Ioannidis, P., et al. (2014) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2014.11.003 · Cited by 35 · see citing works
The evolutionary significance of copy number variation in the human genome
Perry, G. H. (2008) · Cytogenetic and Genome Research · doi:10.1159/000184719 · Cited by 33 · see citing works
“Therefore, CNVs have the potential to affect downstream phenotypes and, ultimately, reproductive fitness (Kondrashov and Kondrashov, 2006; Hurles et al., 2008).”
Oliva, R. F., Cano, L. M., Raffaele, S., Win, J., Bozkurt, T. O., Belhaj, K., Oh, S., Thines, M., & Kamoun, S. (2015) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi-12-14-0393-r · Cited by 33 · see citing works
“Gene duplications are thought to be beneficial in eukaryotic and prokaryotic genes that mediate interaction with the environment (Kondrashov and Kondrashov 2006; Kondrashov et al. 2002; Romero and Palacios 1997).”
BackgroundParallel Concerted Evolution of Ribosomal Protein Genes in Fungi and Its Adaptive Significance
Mullis, A., Lu, Z., Zhan, Y., Wang, T., Rodríguez, J. S., Rajeh, A. A., Chatrath, A., & Lin, Z. (2019) · Molecular Biology and Evolution · doi:10.1093/molbev/msz229 · Cited by 32 · see citing works
“Similar to other types of mutations, only a small portion of duplicate genes can be eventually fixed in a population, and the survivors are usually advantageous to the organisms (Zhang 2003; Kondrashov and Kondrashov 2006).”
BackgroundMANTIS: a phylogenetic framework for multi-species genome comparisons
Tzika, A. C., Helaers, R., de Peer, Y. V., & Milinkovitch, M. C. (2007) · Bioinformatics · doi:10.1093/bioinformatics/btm567 · Cited by 32 · see citing works
“Finally, lineage-specific positive selection might also play a significant role in the retention of duplicates (Hurles, 2004; Kondrashov and Kondrashov, 2006; Shiu et al., 2006).”
Karn, R. C., & Laukaitis, C. M. (2009) · Genome Biology and Evolution · doi:10.1093/gbe/evp049 · Cited by 31 · see citing works
Predominant Gain of Promoter TATA Box after Gene Duplication Associated with Stress Responses
Zou, Y., Huang, W. Y., Gu, Z., & Gu, X. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr116 · Cited by 30 · see citing works
Sutter, M., McGuire, S. T., Ferlez, B. H., & Kerfeld, C. A. (2019) · ACS Synthetic Biology · doi:10.1021/acssynbio.9b00011 · Cited by 31 · see citing works
The Neutral Coalescent Process for Recent Gene Duplications and Copy-Number Variants
Thornton, K. (2007) · Genetics · doi:10.1534/genetics.107.074948 · Cited by 32 · see citing works
“While CNVs have been implicated in several diseases (Sharp et al. 2006; Sebat et al. 2007; reviewed in Kondrashov and Kondrashov 2006), they are also of significant evolutionary interest, as they will likely provide valuable insight into the earliest stages of the evolution of new genes.”
BackgroundHirase, S., Ozaki, H., & Iwasaki, W. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-735 · Cited by 30 · see citing works
“In particular, gene copy number variations (GCNVs), which change the numbers of gene loci in genomes, can significantly alter gene functions and dosages [17,18].”
BackgroundTwo chaperonin systems in bacterial genomes with distinct ecological roles
Williams, T. A., Codoñer, F. M., Toft, C., & Fares, M. A. (2009) · Trends in Genetics · doi:10.1016/j.tig.2009.11.009 · Cited by 29 · see citing works
Selection for Higher Gene Copy Number after Different Types of Plant Gene Duplications
Hudson, C. M., Puckett, E. E., Bekaert, M., Pires, J. C., & Conant, G. C. (2011) · Genome Biology and Evolution · doi:10.1093/gbe/evr115 · Cited by 29 · see citing works
Adaptive deletion in resistance gene duplications in the malaria vector Anopheles gambiae
Assogba, B. S., Alout, H., KOFFI, A. A., Pennetier, C., Djogbénou, L., Makoundou, P., Weill, M., & Labbé, P. (2018) · Evolutionary Applications · doi:10.1111/eva.12619 · Cited by 28 · see citing works
“…through structural problems (breakpoints), hitch- hiking deleterious mutations, metabolic overproduction costs, and/or due to the disruption of biochemical balances for the products of the duplicated genes (Kondrashov & Kondrashov, 2006; Labbé, Berticat et al., 2007; Milesi, Assogba et al., 2017).”
BackgroundDuplicate Retention After Small‐ and Large‐Scale Duplications
Maere, S., & de Peer, Y. V. (2010) · Wiley eBooks · doi:10.1002/9780470619902.ch3 · Cited by 27 · see citing works
The Origin and Evolution of New Genes
Cardoso-Moreira, M., & Long, M. (2012) · Methods in molecular biology · doi:10.1007/978-1-61779-585-5_7 · Cited by 27 · see citing works
Whole-Genome Duplication and Yeast’s Fruitful Way of Life
Escalera‐Fanjul, X., Quezada, H., Riego‐Ruiz, L. R., & González, A. (2018) · Trends in Genetics · doi:10.1016/j.tig.2018.09.008 · Cited by 27 · see citing works
Venom Gene Sequence Diversity and Expression Jointly Shape Diet Adaptation in Pitvipers
Mason, A. J., Holding, M. L., Rautsaw, R. M., Rokyta, D. R., Parkinson, C. L., & Gibbs, H. L. (2022) · Molecular Biology and Evolution · doi:10.1093/molbev/msac082 · Cited by 26 · see citing works
Polyploidy and the Evolution of Complex Traits
Huminiecki, Ł., & Conant, G. C. (2012) · International Journal of Evolutionary Biology · doi:10.1155/2012/292068 · Cited by 24 · see citing works
“At first blush, this result could be explained in terms of selection for high copy number [59] and the dosage balance hypothesis.”
BackgroundThe Role of Retrotransposons in Gene Family Expansions in the Human and Mouse Genomes
Janoušek, V., Laukaitis, C. M., Yanchukov, A., & Karn, R. C. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw192 · Cited by 26 · see citing works
“The snowball effect (Kondrashov and Kondrashov 2006) amounts to a rapid, local increase in gene duplications caused by a high rate of LINE accumulation, subsequent Genome Biol.”
BackgroundYang, H. Z., Gu, W. J., Chen, W. Q., Hwang, J., & Wang, L. (2019) · Chemosphere · doi:10.1016/j.chemosphere.2019.06.097 · Cited by 26 · see citing works
Martins, W. F. S., Subramaniam, K. S., Steen, K., Mawejje, H. D., Liloglou, T., Donnelly, M. J., & Wilding, C. S. (2017) · Scientific Reports · doi:10.1038/s41598-017-06080-8 · Cited by 24 · see citing works
Scienski, K., Fay, J. C., & Conant, G. C. (2015) · Genome Biology and Evolution · doi:10.1093/gbe/evv216 · Cited by 24 · see citing works
Ast, J. C., Urbanczyk, H., & Dunlap, P. V. (2007) · Journal of Bacteriology · doi:10.1128/jb.00672-07 · Cited by 23 · see citing works
“In this regard, it is known that selection can protect both copies of duplicated genes under conditions in which expression benefits the cell (25) and that selection for increased levels of gene products can lead to the retention of duplicated genes (see, e.”
BackgroundNonadaptive processes in primate and human evolution
Harris, E. E. (2010) · American Journal of Physical Anthropology · doi:10.1002/ajpa.21439 · Cited by 23 · see citing works
Copy Number Alterations among Mammalian Enzymes Cluster in the Metabolic Network
Bekaert, M., & Conant, G. C. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq296 · Cited by 22 · see citing works
Denekamp, N. Y., Reinhardt, R., Albrecht, M. W., Drungowski, M., Kube, M., & Lubzens, E. (2010) · Hydrobiologia · doi:10.1007/s10750-010-0518-y · Cited by 21 · see citing works
“It has been proposed that functionality of duplicated genes can be maintained through variability in spatial and temporal expression patterns, but subfunctionality or neofunctionality are also an option (Force et al., 1999; Lynch & Force, 2000; Kondrashov & Kondrashov, 2006).”
BackgroundMa, F., Lau, C. Y., & Zheng, C. (2023) · Cell Genomics · doi:10.1016/j.xgen.2023.100467 · Cited by 20 · see citing works
Fattorini, R., Khojayori, F. N., Mellers, G., Moyroud, E., Herrero, E., Kellenberger, R. T., Walker, R. H., Wang, Q., Hill, L. M., & Glover, B. J. (2024) · New Phytologist · doi:10.1111/nph.19804 · Cited by 20 · see citing works
EARLY EVOLUTION OF THE GENETIC BASIS FOR SOMA IN THE VOLVOCACEAE
Hanschen, E. R., Ferris, P. J., & Michod, R. E. (2014) · Evolution · doi:10.1111/evo.12416 · Cited by 20 · see citing works
“The regA cluster is likely the result of tandem duplications, perhaps by repeated unequal crossing over or backward strand slippage (Chen et al. 2005; Kondrashov and Kondrashov 2006).”
BackgroundDoty, K. A., Wilburn, D. B., Bowen, K. E., Feldhoff, P. W., & Feldhoff, R. C. (2015) · Journal of Proteomics · doi:10.1016/j.jprot.2015.09.019 · Cited by 20 · see citing works
Ancient origin of the divergent forms of leucyl-tRNA synthetases in the Halobacteriales
Andam, C. P., Harlow, T. J., Papke, R. T., & Gogarten, J. P. (2012) · BMC Evolutionary Biology · doi:10.1186/1471-2148-12-85 · Cited by 19 · see citing works
“In bacteria, differential sensitivity of multiple copies of aaRS with redundant functions may benefit the organism against naturally occurring antibiotics [27].”
BackgroundContainment of Extended Length Polymorphisms in Silk Proteins
Chinali, A., Vater, W., Rudakoff, B., Sponner, A., Unger, E., Große, F., Guehrs, K.-H., & Weißhart, K. (2010) · Journal of Molecular Evolution · doi:10.1007/s00239-010-9326-2 · Cited by 18 · see citing works
“Multiple genes within a genome would have the benefit to enhance transcript levels when being commonly expressed ( Kondrashov and Kondrashov 2006 ).”
BackgroundSpecialization of a polyphenism switch gene following serial duplications in Pristionchus nematodes
Ragsdale, E. J., & Ivers, N. A. (2016) · Evolution · doi:10.1111/evo.13011 · Cited by 18 · see citing works
“A speculative possibility is the immediate fitness advantages of gene amplification, allowing selection for higher enzyme dosage (Mouches et al. 1986; Kondrashov and Kondrashov 2006).”
BackgroundCluster expansion of apolipoprotein D (ApoD) genes in teleost fishes
Gu, L., & Xia, C. (2019) · BMC Evolutionary Biology · doi:10.1186/s12862-018-1323-x · Cited by 13 · see citing works
- Authors
- Kondrashov, F. A., & Kondrashov, A. S.
- Affiliations
- National Center for Biotechnology Information (US)
- Corresponding author
- Kondrashov, Fyodor A.
- Kondrashov, Alexey S.
- Venue
- Journal of Theoretical Biology
- Publisher
- Elsevier BV
- Published
- 2006-03
- Volume
- 239
- Issue
- 2
- Pages
- 141-151
- ISSN
- 0022-5193 (ISSN-L)
- OpenAlex
- W2018486257
- Cited by
- 195
- References
- 150
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 3 · 2023: 6 · 2022: 9 · 2021: 4 · 2020: 6 · 2019: 7 · 2018: 10 · 2017: 12 · 2016: 6 · 2015: 11 · 2014: 11 · 2013: 10 · 2012: 13
- FWCI
- 1.01
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Theoretical Biology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genome Rearrangement Algorithms
- Keywords
- gene duplication, natural selection, paralogs, gene conversion, unequal crossover, replication slippage, McDonald-Kreitman test, gene dosage effect, positive selection
- MeSH terms
- Animals, Humans, Mutation, Selection, Genetic, Genome, Gene Dosage, Evolution, Molecular, Gene Duplication
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