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Ohno's dilemma: Evolution of new genes under continuous selection
Open accessAbstract
New genes with novel functions arise by duplication and divergence, but the process poses a problem. After duplication, an extra gene copy must rise to sufficiently high frequency in the population and remain free of common inactivating lesions long enough to acquire the rare mutations that provide a new selectable function. Maintaining a duplicated gene by selection for the original function would restrict the freedom to diverge. (We refer to this problem as Ohno's dilemma). A model is described by which selection continuously favors both maintenance of the duplicate copy and divergence of that copy from the parent gene. Before duplication, the original gene has a trace side activity (the innovation) in addition to its original function. When an altered ecological niche makes the minor innovation valuable, selection favors increases in its level (the amplification), which is most frequently conferred by increased dosage of the parent gene. Selection for the amplified minor function maintains the extra copies and raises the frequency of the amplification in the population. The same selection favors mutational improvement of any of the extra copies, which are not constrained to maintain their original function (the divergence). The rate of mutations (per genome) that improve the new function is increased by the multiplicity of target copies within a genome. Improvement of some copies relaxes selection on others and allows their loss by mutation (becoming pseudogenes). Ultimately one of the extra copies is able to provide all of the new activity.
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“As such, ALE studies highlight that duplications and large scale genomic variations, although they can lead to significant issues such as genomic instability [152], play a major role in e.g. yeast evolution; this is also indicated by data on wine yeasts, galactose utilization, comparative genomics and drug resistance [115,153-156].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [115]
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“Several studies support the idea that high-level amplification of the lac operon and the increased number of potentially revertible lac target genes explains this fast reversion (Hendricksson et al. 2002; Roth and Andersson 2004; Kugelberg et al. 2006 ).”
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BackgroundGenotype network intersections promote evolutionary innovation
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BackgroundAn update on evolutionary, structural, and functional studies of receptor-like kinases in plants
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Brückner, A., & Parker, J. (2020) · Journal of Experimental Biology · doi:10.1242/jeb.211938 · Cited by 42
“The fates of duplicated genes have been widely debated by molecular evolutionists, with a number of competing models proposed for how duplicated loci are not simply lost via genetic drift, but instead become visible to natural selection by impacting the phenotype (Bergthorsson et al., 2007; Force et al., 1999; Lynch a…”
BackgroundGene copy number and malaria biology
Anderson, T., Patel, J., & Ferdig, M. T. (2009) · Trends in Parasitology · doi:10.1016/j.pt.2009.04.005 · Cited by 41
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“shuffling, mobile element transposition, genome rearrangement, and even de novo selection from previously noncoding DNA [5–7] have all been suggested to play a role – the EAD model is very general, applying equally to both prokaryotes and eukaryotes, and among the most commonly cited explanations for the origin, as op…”
GENE-DOSAGE EFFECTS ON FITNESS IN RECENT ADAPTIVE DUPLICATIONS:ace-1IN THE MOSQUITOCULEX PIPIENS
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“Understanding the gene-dosage impact on the fate of duplication is thus fairly straightforward when the two duplicates are identical to start with: in these cases, the evolution of new function requires subsequent divergence of the duplicates (Force et al. 1999; Lynch and Conery 2000; Otto and Yong 2002; Zhang 2003; T…”
BackgroundInfluentialTranscription, Translation, and the Evolution of Specialists and Generalists
Zhong, S., Miller, S. P., Dykhuizen, D. E., & Dean, A. M. (2009) · Molecular Biology and Evolution · doi:10.1093/molbev/msp187 · Cited by 40
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Voß, M., Xiang, C., Esque, J., Nobili, A., Menke, M. J., André, I., Höhne, M., & Bornscheuer, U. T. (2020) · ACS Chemical Biology · doi:10.1021/acschembio.9b00888 · Cited by 32
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BackgroundSelf-citationThe origin and evolution of human glutaminases and their atypical C-terminal ankyrin repeats
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“Genetic evolutionary models often predict an increase in the gene copy number prior to the specialization or gain of new functions, with a momentary intermediate state of specialization with an overlap of functions (38).”
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“Among these, the Innovation-AmplificationDivergence model (Bergthorsson et al., 2007) is the one that better fits the evolutionary history of the CrCO, PpCOLs, and AtCOLs genes inferred in this work using gene co-expression networks.”
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BackgroundAntifreeze protein gene amplification facilitated niche exploitation and speciation in wolffish
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“Thereby gene function is improved stepwise and even the neo-functionalization of genes is fostered while the original function of the gene is retained on other copies [20], a hypothesis that has recently been strengthened with experimental evidence [21].”
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Metadata
- Authors
- Bergthorsson, U., Andersson, D. I., & Roth, J. R.
- Affiliations
- University of New Mexico (US)
- Uppsala University (SE)
- University of California, Davis (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2007-10-23
- Volume
- 104
- Issue
- 43
- Pages
- 17004-17009
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2040452
- OpenAlex
- W2051768616
- Cited by
- 405
- References
- 96
- Citations by year
- 2026: 17 · 2025: 17 · 2024: 53 · 2023: 16 · 2022: 14 · 2021: 14 · 2020: 21 · 2019: 13 · 2018: 14 · 2017: 22 · 2016: 28 · 2015: 20 · 2014: 28 · 2013: 23 · 2012: 32
- FWCI
- 9.64
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of General Medical Sciences (GM27068, R01GM027068)
- National Center for Research Resources (P20-RR18754, P20RR018754)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
- Social Sciences › Arts and Humanities › History and Philosophy of Science › Philosophy of Biology and Scientific Explanation
- Keywords
- gene duplication, gene divergence, continuous selections, pseudogenes, gene copy number
- MeSH terms
- Biological Evolution, Gene Amplification, Gene Frequency, Models, Genetic, Recombination, Genetic, Selection, Genetic, Genetic Variation, Point Mutation, Gene Duplication, Gene Transfer, Horizontal
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