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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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“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]
In the citing paper
“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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“…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).”
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Differential Retention of Metabolic Genes Following Whole-Genome Duplication
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“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).”
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“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
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“Several studies have proposed that gene deletion rates could be several times higher than gene duplication rates [47,48].”
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“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].”
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“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 37
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 35
“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
“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 31
“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
“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 32
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
Sutter, M., McGuire, S. T., Ferlez, B. H., & Kerfeld, C. A. (2019) · ACS Synthetic Biology · doi:10.1021/acssynbio.9b00011 · Cited by 31
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
“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 32
“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
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
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 26
“…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
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
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 28
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
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
“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 25
“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
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
Scienski, K., Fay, J. C., & Conant, G. C. (2015) · Genome Biology and Evolution · doi:10.1093/gbe/evv216 · Cited by 24
Ast, J. C., Urbanczyk, H., & Dunlap, P. V. (2007) · Journal of Bacteriology · doi:10.1128/jb.00672-07 · Cited by 23
“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
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
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
“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 18
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
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
“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
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 20
“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
“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
“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
Metadata
- 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 › Biochemistry, Genetics and Molecular Biology › Genetics › 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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