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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Duplications and large scale genomic variations, although they can lead to significant issues such as genomic instability, play a major role in yeast evolution.
“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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Elde, N. C., Child, S. J., Eickbush, M. T., Kitzman, J. O., Rogers, K. S., Shendure, J., Geballe, A. P., & Malik, H. S. (2012) · Cell · doi:10.1016/j.cell.2012.05.049 · Cited by 357 · see citing works
“Whereas rapid evolution of copy number variation is known for some nonvirus microbial populations, including Plasmodium, yeast, and a variety of bacteria (Bergthorsson et al., 2007; Demuth and Hahn, 2009; Dunham et al., 2002; Kugelberg et al., 2010; Nair et al., 2008; Pränting and Andersson, 2011; Stambuk et al., 2009…”
Bacterial gene amplification: implications for the evolution of antibiotic resistance
Sandegren, L., & Andersson, D. I. (2009) · Nature Reviews Microbiology · doi:10.1038/nrmicro2174 · Cited by 355 · see citing works
“jpg" NDATA ITEM> ]> Gene amplification is found in all three kingdoms of life and is important both from a fundamental evolutionary perspectiv”
BackgroundSelf-citationRauwerdink, A. M., & Kazlauskas, R. J. (2015) · ACS Catalysis · doi:10.1021/acscatal.5b01539 · Cited by 354 · see citing works
Gene amplification and adaptive evolution in bacteria.
Andersson, D., & Hughes, D. (2009) · Annual Review of Genetics · doi:10.1146/annurev-genet-102108-134805 · Cited by 308 · see citing works
Self-citationNew Gene Evolution: Little Did We Know
Long, M., VanKuren, N. W., Chen, S., & Vibranovski, M. D. (2013) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133301 · Cited by 307 · see citing works
“IAD and EAC, in contrast, propose that ancestral loci develop novel beneficial secondary functions before duplication (9, 36).”
BackgroundReal-Time Evolution of New Genes by Innovation, Amplification, and Divergence
Näsvall, J., Sun, L., Roth, J. R., & Andersson, D. I. (2012) · Science · doi:10.1126/science.1226521 · Cited by 282 · see citing works
Self-citationThe population genetics of mutations: good, bad and indifferent
Loewe, L., & Hill, W. G. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0317 · Cited by 259 · see citing works
“1990), and (v) mutations that enable a species to start expanding into a new ecological niche (e.g. Elena & Lenski 2003; Bergthorsson et al. 2007).”
BackgroundFrom bacteria to human: A journey into the world of chitinases
Adrangi, S., & Faramarzi, M. A. (2013) · Biotechnology Advances · doi:10.1016/j.biotechadv.2013.09.012 · Cited by 235 · see citing works
Extensive Functional Diversification of the Populus Glutathione S -Transferase Supergene Family
Lan, T., Yang, Z., Yang, X. N., Liu, Y., Wang, X., & Zeng, Q. (2009) · The Plant Cell · doi:10.1105/tpc.109.070219 · Cited by 224 · see citing works
“genome-wide nucleotide substitution analyses suggests that retention of paralogs driven by positive selection accounts for only a fraction of the expansion of gene families (Bergthorsson et al., 2007; Demuth and Hahn, 2009).”
BackgroundCoevolution of retroelements and tandem zinc finger genesPreprint
Thomas, J. H., & Schneider, S. (2011) · Genome Research · doi:10.1101/gr.121749.111 · Cited by 218 · see citing works
“This pattern of duplicate evolution corresponds in many ways to that proposed for bacterial genes (Bergthorsson et al. 2007).”
BackgroundVoordeckers, K., Brown, C. A., Vanneste, K., van der Zande, E., Voet, A. R. D., Maere, S., & Verstrepen, K. J. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001446 · Cited by 201 · see citing works
“Examples of such co-option models include the ‘‘gene sharing’’ or ‘‘Escape from Adaptive Conflict’’ (EAC) model [5,16–19] and the related ‘‘Innovation, Amplification and Divergence’’ (IAD) model [20–22].”
Shining a light on enzyme promiscuity
Copley, S. D. (2017) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2017.11.001 · Cited by 200 · see citing works
“When an environmental change makes a promiscuous activity important for fitness, gene duplication followed by divergence can allow evolution of a new enzyme while the original activity is maintained [2,3].”
Moonlighting is mainstream: Paradigm adjustment required
Copley, S. D. (2012) · BioEssays · doi:10.1002/bies.201100191 · Cited by 199 · see citing works
Casewell, N. R., Wagstaff, S. C., Harrison, R. A., Renjifo, C., & Wüster, W. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr091 · Cited by 193 · see citing works
“It has since been proposed that genes may develop one or more discrete or neutral secondary functions prior to gene duplication, with subsequent mutations (Hughes 1994) or further gene amplification prior to mutation (Bergthorsson et al. 2007), allowing selective pressures to maintain duplicates with divergent functio…”
BackgroundEvolution of New Functions De Novo and from Preexisting GenesPreprint
Andersson, D. I., Jerlström-Hultqvist, J., & Näsvall, J. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a017996 · Cited by 185 · see citing works
“Susumu Ohno further developed this idea in his seminal book Evolution by Gene Duplication (Ohno 1970) and later work modified and refined his model (Jensen 1976; Piatigorsky 1991; Hughes 1994; Force et al. 1999; Lynch and Conery 2000; Lynch and Force 2000; Kondrashovet al. 2002; Bergthorsson et al. 2007; Näsvall et al…”
BackgroundSelf-citationPoole, S. J., Diner, E. J., Aoki, S. K., Braaten, B. A., de Roodenbeke, C. T., Low, D. A., & Hayes, C. S. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002217 · Cited by 184 · see citing works
“would be present [22,23].”
The Importance of Genetic Redundancy in Evolution
Láruson, Á. J., Yeaman, S., & Lotterhos, K. E. (2020) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2020.04.009 · Cited by 181 · see citing works
The Deep Origin and Recent Loss of Venom Toxin Genes in Rattlesnakes
Dowell, N. L., Giorgianni, M. W., Kassner, V. A., Selegue, J. E., Sanchez, E. E., & Carroll, S. B. (2016) · Current Biology · doi:10.1016/j.cub.2016.07.038 · Cited by 177 · see citing works
RECENT ADVANCES IN RATIONAL APPROACHES FOR ENZYME ENGINEERING
Steiner, K., & Schwab, H. (2012) · Computational and Structural Biotechnology Journal · doi:10.5936/csbj.201209010 · Cited by 179 · see citing works
An evolutionary biochemist's perspective on promiscuity
Copley, S. D. (2015) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2014.12.004 · Cited by 173 · see citing works
Genesis, effects and fates of repeats in prokaryotic genomes
Treangen, T. J., Abraham, A., Touchon, M., & Rocha, E. P. C. (2009) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2009.00169.x · Cited by 172 · see citing works
“On the other hand, if there is strong selection for both copies at the time of amplification, then the amplification will be stable and mutational processes could have much more time to diversify the function of the genes (Francino, 2005; Bergthorsson et al., 2007).”
BackgroundCopy-number changes in evolution: rates, fitness effects and adaptive significance
Katju, V., & Bergthorsson, U. (2013) · Frontiers in Genetics · doi:10.3389/fgene.2013.00273 · Cited by 172 · see citing works
“…biologically valuable, selection for increase in gene dosage would help the spread and maintenance of a duplicated gene in the population until subsequent beneficial mutations result in a novel gene (Roth et al., 1996; Hendrickson et al., 2002; Hooper and Berg, 2003; Bergthorsson et al., 2007).”
BackgroundSelf-citationGenetic conflicts: the usual suspects and beyond
McLaughlin, R. N., & Malik, H. S. (2017) · Journal of Experimental Biology · doi:10.1242/jeb.148148 · Cited by 167 · see citing works
“Similar copy number expansions have been observed in many ‘slowly evolving’ organisms including bacteria, yeast, Plasmodium and even mammalian cells (Bergthorsson et al., 2007; Demuth and Hahn, 2009; Dunham et al., 2002; Kugelberg et al., 2010; Nair et al., 2008; Pränting and Andersson, 2011;…”
BackgroundBornscheuer, U. T. (2016) · Science · doi:10.1126/science.aaf2853 · Cited by 159 · see citing works
Chang, D., & Duda, T. F. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss068 · Cited by 157 · see citing works
“Model of Conotoxin Gene Family Evolution Redundant gene copies produced by gene duplication mutation can be either neutral and fixed by genetic drift (Ohno 1970) or beneficial and fixed by selection (Francino 2005; Kondrashov and Kondrashov 2006; Bergthorsson et al. 2007).”
BackgroundEvolutionary dynamics of natural product biosynthesis in bacteria
Chevrette, M. G., Gutiérrez-García, K., Mojica, N. S., Aguilar, C., Yañez-Olvera, A. G., Ramos-Aboites, H. E., Hoskisson, P. A., & Barona‐Gómez, F. (2019) · Natural Product Reports · doi:10.1039/c9np00048h · Cited by 153 · see citing works
Evolution of new enzymes by gene duplication and divergence
Copley, S. D. (2020) · FEBS Journal · doi:10.1111/febs.15299 · Cited by 148 · see citing works
Dragosits, 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
“Our observations are in accordance with recent theoretical analyses on the role of gene duplication in adaptation and evolution of novel functions (Kondrashov and Kondrashov, 2006; Bergthorsson et al, 2007).”
Resultvon Reumont, B. M., Anderluh, G., Antunes, A., Ayvazyan, N. M., Beis, D., Çalışkan, F., Crnković, A., Damm, M., Dutertre, S., Ellgaard, L., et al. (2022) · GigaScience · doi:10.1093/gigascience/giac048 · Cited by 131 · see citing works
“Previous knowledge of gene evolution can help to infer the most likely evolutionary history of a given gene [177, 180– 183].”
Convergent evolution of caffeine in plants by co-option of exapted ancestral enzymes
Huang, R., O’Donnell, A. J., Barboline, J. J., & Barkman, T. J. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1602575113 · Cited by 131 · see citing works
“model of protein functional change (30) and those that have emerged from protein engineering studies (31) in that promiscuous enzyme activities are nearly universal properties of modern-day enzymes and have been shown to serve as the basis for evolution of specialized, novel enzyme activities.”
BackgroundBeyond Paralogs: The Multiple Layers of Redundancy in Bacterial Pathogenesis
Ghosh, S., & O’Connor, T. J. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00467 · Cited by 120 · see citing works
Reams, A. B., Kofoid, E., Savageau, M. A., & Roth, J. R. (2010) · Genetics · doi:10.1534/genetics.109.111963 · Cited by 126 · see citing works
“A proposal for rapid evolution of new genes by means of selective gene amplification has been described previously (Bergthorsson et al. 2007).”
Self-citationAccelerated Evolution after Gene Duplication: A Time-Dependent Process Affecting Just One Copy
Pegueroles, C., Laurie, S., & Albà, M. M. (2013) · Molecular Biology and Evolution · doi:10.1093/molbev/mst083 · Cited by 125 · see citing works
High Spontaneous Rate of Gene Duplication in Caenorhabditis elegans
Lipinski, K. J., Farslow, J. C., Fitzpatrick, K. A., Lynch, M., Katju, V., & Bergthorsson, U. (2011) · Current Biology · doi:10.1016/j.cub.2011.01.026 · Cited by 125 · see citing works
“populations have often involved an increase in gene dosage through gene duplication and amplification rather than regulatory base substitutions [29–31].”
BackgroundSelf-citationEvolution of a New Function by Degenerative Mutation in Cephalochordate Steroid Receptors
Bridgham, J. T., Brown, J. E., Rodríguez‐Marí, A., Catchen, J., & Thornton, J. W. (2008) · PLoS Genetics · doi:10.1371/journal.pgen.1000191 · Cited by 122 · see citing works
“The plausibility of the classic model as a general explanation for the evolution of new functions has therefore been called into question[16,17].”
BackgroundSoo, V. W. C., Hanson‐Manful, P., & Patrick, W. M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1012108108 · Cited by 116 · see citing works
“This model, termed adaptive radiation (10) or the innovation, amplification, and divergence (IAD) model (11), is rooted in the notion that many existing proteins display broad specificity and secondary activities in addition to the function that they evolved to carry out (12).”
BackgroundMethodResultInfluentialAdler, M., Anjum, M., Berg, O. G., Andersson, D. I., & Sandegren, L. (2014) · Molecular Biology and Evolution · doi:10.1093/molbev/msu111 · Cited by 103 · see citing works
“Finally, the neofunctionalization model involves the development of a new function in one of the duplicated copies while maintaining the old function in another copy (Ohno 1970; Bergthorsson et al. 2007; Dittmar and Liberles 2011; Näsvall et al. 2012).”
BackgroundMethodInfluentialSelf-citationEmerging chemicals and the evolution of biodegradation capacities and pathways in bacteria
Kolvenbach, B. A., Helbling, D. E., Kohler, H. E., & Corvini, P. F.-X. (2013) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2013.08.017 · Cited by 101 · see citing works
An evolutionary perspective on protein moonlighting
Copley, S. D. (2014) · Biochemical Society Transactions · doi:10.1042/bst20140245 · Cited by 98 · see citing works
Multicopy plasmids allow bacteria to escape from fitness trade-offs during evolutionary innovation
Rodríguez-Beltrán, J., Hernandez‐Beltran, J. C. R., DelaFuente, J., Escudero, J. A., Fuentes-Hernández, A., MacLean, R. C., Peña‐Miller, R., & Millán, Á. S. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0529-z · Cited by 99 · see citing works
“Most of these models are based on the emergence of genetic amplifications that provide genetic redundancy1,8–11.”
Jackson, T., Koludarov, I., Ali, S. A., Dobson, J. S., Zdenek, C. N., Dashevsky, D., den Brouw, B. O., Masci, P. P., Nouwens, A. S., Josh, P. F., et al. (2016) · Toxins · doi:10.3390/toxins8110309 · Cited by 95 · see citing works
Selection of Orphan Rhs Toxin Expression in Evolved Salmonella enterica Serovar Typhimurium
Koskiniemi, S., Garza-Sánchez, F., Sandegren, L., Webb, J. S., Braaten, B., Poole, S., Andersson, D., Hayes, C. S., & Low, D. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004255 · Cited by 78 · see citing works
“However, there is a cost to maintaining amplified regions, and gene duplications are lost during segregation at frequencies up to 10% per generation [16,17].”
BackgroundSelf-citationThe predictability of molecular evolution during functional innovation
Blank, D., Wolf, L., Ackermann, M., & Silander, O. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1318797111 · Cited by 91 · see citing works
“It has previously been proposed that gene duplications play a critical role in functional innovation (39, 40); more recently, C ar bo n”
BackgroundEnzyme functional evolution through improved catalysis of ancestrally nonpreferred substrates
Huang, R., Hippauf, F., Rohrbeck, D., Haustein, M., Wenke, K., Feike, J., Sorrelle, N. B., Piechulla, B., & Barkman, T. J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019605109 · Cited by 89 · see citing works
“In the cases of duplication–degeneration–complementation (DDC) (2) and escape from adaptive conflict (EAC) (3–6), multiple ancestral functions are selectively maintained in the single progenitor protein but for innovation–amplification– divergence (IAD) (7, 8), one ancestral function is under selection, whereas others…”
BackgroundInfluentialEnzyme evolution: innovation is easy, optimization is complicated
Newton, M., Arcus, V. L., Gerth, M. L., & Patrick, W. M. (2017) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2017.11.007 · Cited by 87 · see citing works
“[17,18]) are centred on the importance of gene duplication and divergence as the evolutionary route to new enzymes.”
Copley, S. D., Rokicki, J., Turner, P., Daligault, H. E., Nolan, M., & Land, M. (2011) · Genome Biology and Evolution · doi:10.1093/gbe/evr137 · Cited by 85 · see citing works
“New genes that can help microbes survive and grow in the face of selective pressure from environmental toxins can also arise by gene duplication and divergence (Hughes 1994; Bergthorsson et al. 2007).”
BackgroundCompensatory gene amplification restores fitness after inter‐species gene replacements
Lind, P. A., Tobin, C., Berg, O. G., Kurland, C. G., & Andersson, D. I. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.07030.x · Cited by 85 · see citing works
“…increased target size for beneficial mutations can also speed up the selective fine-tuning required for optimal function, and potentially the selective stabilization of the amplification may contribute to the evolution of genes with novel function by diverging mutations (Bergthorsson et al., 2007).”
BackgroundInfluentialSelf-citationZhao, L., Lv, Y., Cai, C., Xiangchao, T., Xiangdong, C., Zhang, W., Hao, D., Xiuhua, G., & Wangzhen, G. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-539 · Cited by 84 · see citing works
“Ultimately, these duplicated sequences and their functions are maintained intact or undergo long-term evolutionary changes via sequence elimination [69,70], sequence rearrangement [71], gene silencing [72], or acquisition of new function [73].”
Toward a General Theory of Adaptive Radiation
Kassen, R. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04574.x · Cited by 78 · see citing works
“Models for the evolution of new gene functions (Francino 2005; Bergthorsson et al. 2007) provide a starting place for thinking about the sorts of genes or genetic systems involved in overcoming the first two challenges—small population size and limited extant genetic variation—faced by a population when it invades a n…”
BackgroundHow enzyme promiscuity and horizontal gene transfer contribute to metabolic innovation
Glasner, M. E., Truong, D. P., & Morse, B. C. (2019) · FEBS Journal · doi:10.1111/febs.15185 · Cited by 77 · see citing works
Shi, A., Fan, F., & Broach, J. R. (2021) · Journal of Industrial Microbiology & Biotechnology · doi:10.1093/jimb/kuab076 · Cited by 77 · see citing works
“Gene duplications are pervasive (Bergthorsson et al., 2007) and provide opportunities for increasing expression of a gene and for introducing genomic variability, which in turn facilitates adaptation to various environments.”
Copy Number Change: Evolving views on Gene Amplification
Elliott, K. T., Cuff, L. E., & Neidle, E. L. (2013) · Future Microbiology · doi:10.2217/fmb.13.53 · Cited by 78 · see citing works
“Amplification, diversification & evolution GDA (at levels beyond two gene copies) is increasingly being incorporated into evolutionary models [13,58,59].”
BackgroundInfluentialAssogba, 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
“Increasing numbers of studies also suggest that CNVs may play a role in adaptation to environmental changes at the micro-evolutionary scale (for a review, [3]; see also [4,5]).”
BackgroundToward a Systems Biology Perspective on Enzyme Evolution
Copley, S. D. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.r111.254714 · Cited by 74 · see citing works
Shukla, A., Chatterjee, A., & Kondabagil, K. R. (2017) · Virus Evolution · doi:10.1093/ve/vex039 · Cited by 74 · see citing works
Murakami, T., Burian, J., Yanai, K., Bibb, M. J., & Thompson, C. J. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1108124108 · Cited by 73 · see citing works
Montanier, C., Money, V. A., Pires, V. M. R., Flint, J. E., Pinheiro, B., Goyal, A., Prates, J. A. M., Izumi, A., Stålbrand, H., Morland, C., et al. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000071 · Cited by 71 · see citing works
“[28] and others argue that Ohno’s model poses a dilemma, because it requires that the duplicated copy of the gene, which incurs an energetic cost, must be retained within a population prior to acquiring the mutations that confer the new activity.”
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
“Selection for increased dosage does not necessarily have to be for the gene’s primary activity; it could also be for trace side activity that becomes beneficial after an environmental change (Bergthorsson et al. 2007).”
BackgroundBershtein, S., & Tawfik, D. S. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn174 · Cited by 69 · see citing works
“Duplication is known to occur under such selection pressures and under this scenario, both duplicates will be maintained under selection to maintain both the primary function and the minor one (Bergthorsson et al. 2007).”
BackgroundMethodInfluentialThe Ingenuity of Bacterial Genomes
Kirchberger, P. C., Schmidt, M. L., & Ochman, H. (2020) · Annual Review of Microbiology · doi:10.1146/annurev-micro-020518-115822 · Cited by 68 · see citing works
Regulation of Clostridium difficile spore germination by the CspA pseudoprotease domain
Kevorkian, Y. L., Shirley, D. J., & Shen, A. (2015) · Biochimie · doi:10.1016/j.biochi.2015.07.023 · Cited by 67 · see citing works
“Since copy number variation frequently indicates that genes are under selective pressure [68, 75], the high frequency of csp gene duplications in Peptostreptococcaceae family members strongly suggests that unknown selective pressures are driving the diversification of these loci.”
BackgroundKujala, K., Drake, H. L., & Horn, M. A. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.00254-09 · Cited by 67 · see citing works
“, in species in which multiple gene copies are present) rather than by horizontal gene transfer (1).”
BackgroundPatterns and Evolutionary Consequences of Pleiotropy
Zhang, J. (2023) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-022323-083451 · Cited by 66 · 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
“Future work will need to address other factors such as gene expression (61), the interactions within gene regulatory (62) and metabolic networks (63), the possibility of multiple duplications of the same gene in rapid succession (40), and cases of smaller μN (46).”
BackgroundBarsottini, M. R. D. O., de Oliveira, J. F., Adamóski, D., Teixeira, P. J. P. L., do Prado, P. F. V., Tiezzi, H. D. O., Sforça, M. L., Cassago, A., Portugal, R. V., de Oliveira, P. S. L., et al. (2013) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi-05-13-0148-r · Cited by 60 · see citing works
“Different genetic evolutionary models predict an expansion in a gene’s copy 339 number before their specialization or the rise of new functions, also accounting for an overlap of functions 340 due to a momentary intermediate state of specialization (Bergthorsson et al. 2007).”
BackgroundHellgren, O., & Ekblom, R. (2010) · Immunome Research · doi:10.1186/1745-7580-6-3 · Cited by 60 · see citing works
Functional innovation through new genes as a general evolutionary process
Xia, S., Chen, J., Arsala, D., Emerson, J. J., & Long, M. (2025) · Nature Genetics · doi:10.1038/s41588-024-02059-0 · Cited by 61 · see citing works
Bunsupa, S., Hanada, K., Maruyama, A., Aoyagi, K., Komatsu, K., Ueno, H., Yamashita, M., Sasaki, R., Oikawa, A., Saito, K., et al. (2016) · PLANT PHYSIOLOGY · doi:10.1104/pp.16.00639 · Cited by 57 · see citing works
“This evolutionary process has been proposed as the innovation, amplification, and divergence model (Bergthorsson et al., 2007).”
BackgroundAccelerating pathway evolution by increasing the gene dosage of chromosomal segments
Tumen-Velasquez, M. P., Johnson, C. W., Ahmed, A. R., Dominick, G., Fulk, E. M., Khanna, P., Lee, S. A., Schmidt, A. L., Linger, J. G., Eiteman, M. A., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1803745115 · Cited by 56 · see citing works
“During continued selection for Gua growth, gcoAB copies are expected to diverge (5).”
BackgroundOrigin and Functional Diversification of an Amphibian Defense Peptide Arsenal
Roelants, K., Fry, B. G., Ye, L., Stijlemans, B., Brys, L., Kok, P. J. R., Clynen, E., Schoofs, L., Cornélis, P., & Bossuyt, F. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003662 · Cited by 56 · see citing works
“[74,76,77].”
The evolution of metabolism: How to test evolutionary hypotheses at the genomic level
Scossa, F., & Fernie, A. R. (2020) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2020.02.009 · Cited by 56 · see citing works
“The patchwork hypothesis, on the other hand, is consistent with the various models of protein functional evolution following gene duplications [24,96,164,194,266], and with the evidences coming from directed evolution experiments on the evolution of promiscuous activities [1].”
ResultFunctional Divergence for Every Paralog
Soria, P. S., McGary, K. L., & Rokas, A. (2014) · Molecular Biology and Evolution · doi:10.1093/molbev/msu050 · Cited by 53 · see citing works
“More recent models have focused on the role of positive selection in gene duplication, due to escape from adaptive conflict (Hittinger and Carroll 2007) or selection of a new weak secondary function that drives gene duplication and subsequent divergence (Bergthorsson et al. 2007; Elde et al. 2012).”
BackgroundMicrobial co-habitation and lateral gene transfer: what transposases can tell us
Hooper, S. D., Mavromatis, K., & Kyrpides, N. C. (2009) · Genome biology · doi:10.1186/gb-2009-10-4-r45 · Cited by 56 · see citing works
“A further advantage of transposases over other protein-coding genes is lower degree of selection effects such as conservation, recombination [12], adaptive radiation [13] or counter-selection [14].”
The Evolutionary Potential of Phenotypic Mutations
Yanagida, H., Gispan, A., Kadouri, N., Rozen, S., Sharon, M., Barkai, N., & Tawfik, D. S. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005445 · Cited by 54 · see citing works
“Divergence before duplication, and a subsequent sub-functionalization to two paralogues, demands the appearance of the new trait within the ancestral, pre-duplicated gene while maintaining its original function [14,23,24,25].”
BackgroundMargres, M. J., Bigelow, A. T., Lemmon, E. M., Lemmon, A. R., & Rokyta, D. R. (2017) · Genetics · doi:10.1534/genetics.117.202655 · Cited by 54 · see citing works
“…thepositive dosagemodel, the frequency of this specific process relative to others, particularly for models requiring sequence variation (Francino 2005; Bergthorsson et al. 2007), is unclear because of the lack of data on copy number variation at the population level (Innan and Kondrashov 2010).”
BackgroundReams, A. B., Kofoid, E., Kugelberg, E., & Roth, J. R. (2012) · Genetics · doi:10.1534/genetics.112.142570 · Cited by 50 · see citing works
Self-citationMicroevolution of Cryptococcus neoformans Driven by Massive Tandem Gene Amplification
Chow, E. W. L., Morrow, C. A., Djordjevic, J. T., Wood, I., & Fraser, J. A. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss066 · Cited by 52 · see citing works
“cerevisiae, amplified gene arrays are found in multiple subtelomeres (Brown et al. 1998; Bergthorsson et al. 2007; Wu et al. 2009; Brown et al. 2010).”
Positive and strongly relaxed purifying selection drive the evolution of repeats in proteins
Persi, E., Wolf, Y. I., & Koonin, E. V. (2016) · Nature Communications · doi:10.1038/ncomms13570 · Cited by 49 · see citing works
Abiotic selection of microbial genome size in the global ocean
Ngugi, D. K., Acinas, S. G., Sánchez, P., Gasol, J. M., Agustı́, S., Karl, D. M., & Duarte, C. M. (2023) · Nature Communications · doi:10.1038/s41467-023-36988-x · Cited by 51 · see citing works
Baquero, F. (2011) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkr214 · Cited by 50 · see citing works
van der Nest, M. A., Steenkamp, E. T., McTaggart, A. R., Trollip, C., Godlonton, T., Sauerman, E., Roodt, D., Naidoo, K., Coetzee, M. P. A., Wilken, P. M., et al. (2015) · BMC Evolutionary Biology · doi:10.1186/s12862-015-0550-7 · Cited by 50 · see citing works
“In fungi, changes in the repertoire of GH32 functional products are thought to influence the efficiency at which sucrolytic compounds are exploited [79].”
BackgroundLight-Emitting Dehalogenases: Reconstruction of Multifunctional Biocatalysts
Chaloupková, R., Lišková, V., Toul, M., Marková, K., Šebestová, E., Hernychová, L., Marek, M., Pinto, G., Pluskal, D., Waterman, J., et al. (2019) · ACS Catalysis · doi:10.1021/acscatal.9b01031 · Cited by 50 · see citing works
Enzyme function and evolution through the lens of bioinformatics
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“Additionally, increased mutation rates or genomic reticulations could lead to the exaptation of genes through duplication, domain shuffling, and altered regulation (True and Carroll, 2002; Zhang, 2003; Taylor and Raes, 2004; Bergthorsson et al., 2007; Pigliucci, 2008).”
BackgroundSignificance and Biological Consequences of Polyploidization in Land Plant Evolution
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“More recently, two models have been proposed that combine aspects of sub- and neofunctionalization, namely the ‘Escape from Adaptive Conflict’ (EAC) model (Hittinger and Carroll 2007; Des Marais and Rausher 2008) and the ‘Innovation, Amplification, Divergence’ (IAD) model (Hendrickson et al. 2002; Francino 2005; Bergt…”
BackgroundDiscovery and Design of Family VIII Carboxylesterases as Highly Efficient Acyltransferases
Müller, H., Godehard, S. P., Palm, G. J., Berndt, L., Badenhorst, C. P. S., Becker, A., Lammers, M., & Bornscheuer, U. T. (2020) · Angewandte Chemie International Edition · doi:10.1002/anie.202014169 · Cited by 48 · see citing works
How the Toxin got its Toxicity
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Self-citation
- 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 › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Social Sciences › Arts and Humanities › History and Philosophy of Science › Philosophy and History of Science
- 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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