Viruses and mobile elements as drivers of evolutionary transitions
Open accessAbstract
The history of life is punctuated by evolutionary transitions which engender emergence of new levels of biological organization that involves selection acting at increasingly complex ensembles of biological entities. Major evolutionary transitions include the origin of prokaryotic and then eukaryotic cells, multicellular organisms and eusocial animals. All or nearly all cellular life forms are hosts to diverse selfish genetic elements with various levels of autonomy including plasmids, transposons and viruses. I present evidence that, at least up to and including the origin of multicellularity, evolutionary transitions are driven by the coevolution of hosts with these genetic parasites along with sharing of ‘public goods’. Selfish elements drive evolutionary transitions at two distinct levels. First, mathematical modelling of evolutionary processes, such as evolution of primitive replicator populations or unicellular organisms, indicates that only increasing organizational complexity, e.g. emergence of multicellular aggregates, can prevent the collapse of the host–parasite system under the pressure of parasites. Second, comparative genomic analysis reveals numerous cases of recruitment of genes with essential functions in cellular life forms, including those that enable evolutionary transitions. This article is part of the themed issue ‘The major synthetic evolutionary transitions’.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In silico coevolution models, in vitro evolution and genomic analyses have shown that parasites actively promote diversity and evolvability.
“In silico coevolution models [333,334], in vitro evolution [335,336] and genomic analyses [337,338] have shown that parasites actively promote diversity and evolvability, as illustrated by the phylogenetic trees in figure 9a,b.”
From Fundamental constraints to the logic of living systems (2024) · cites this paper as [338]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The origins of genome complexity
Lynch, M., & Conery, J. S. (2003) · Science · doi:10.1126/science.1089370 · Cited by 1,698 · see citing works
Complex archaea that bridge the gap between prokaryotes and eukaryotes
Spang, A., Saw, J. H., Jørgensen, S. L., Zaremba-Niedzwiedzka, K., Martijn, J., Lind, A. E., van Eijk, R., Schleper, C., Guy, L., & Ettema, T. J. G. (2015) · Nature · doi:10.1038/nature14447 · Cited by 1,324 · see citing works
Eukaryotic evolution, changes and challenges
Embley, T. M., & Martin, W. (2006) · Nature · doi:10.1038/nature04546 · Cited by 867 · see citing works
Endosymbiosis and Eukaryotic Cell Evolution
Archibald, J. M. (2015) · Current Biology · doi:10.1016/j.cub.2015.07.055 · Cited by 654 · see citing works
Group selection of early replicators and the origin of life
Szathmáry, E., & Demeter, L. (1987) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(87)80191-1 · Cited by 407 · see citing works
On the origin of genomes and cells within inorganic compartments
Koonin, E. V., & Martin, W. (2005) · Trends in Genetics · doi:10.1016/j.tig.2005.09.006 · Cited by 406 · see citing works
Self-citationWolf, Y. I., & Koonin, E. V. (2007) · Biology Direct · doi:10.1186/1745-6150-2-14 · Cited by 235 · see citing works
Self-citationTakeuchi, N., Kaneko, K., & Koonin, E. V. (2014) · G3 Genes|Genomes|Genetics · doi:10.1534/g3.113.009845 · Cited by 125 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 173
- [2]Dobzhansky T 1937 Genetics and the origin of species. New York, NY: Columbia University Press.
- [4]Szathmáry E, Maynard Smith J 1997 From replicators to reproducers: the first major transitions leading to life. J. Theor. Biol. 187, 555– 571. (10.1006/jtbi.1996.0389) 9299299 · DOI · Paper page
- [6]Maynard Smith J 1998 The units of selection. Novartis Found Symp. 213, 203– 211; discussion 211–207. 9653725
- [7]Szathmáry E 2001 Biological information, kin selection, and evolutionary transitions. Theor. Popul. Biol. 59, 11– 14. (10.1006/tpbi.2000.1503) 11243923 · DOI
- [8]Szathmáry E 2015 Toward major evolutionary transitions theory 2.0. Proc. Natl Acad. Sci. USA 112, 10 104– 10 111. (10.1073/pnas.1421398112) 25838283 PMC4547294 · DOI · Paper page
- [9]Queller DC 1997 Cooperators since life began. Q. Rev. Biol. 72, 184– 188. (10.1086/419766) · DOI
- [10]Bass LW 1988 The evolution of individuality. Princeton, NJ: Princeton University Press.
- [11]Michod RE 1999 Darwinian dynamics: evolutionary transitions in fitness and individuality. Princeton, NY: Princeton University Press.
- [12]Corning PA, Szathmáry E 2015 ‘Synergistic selection’: a Darwinian frame for the evolution of complexity. J. Theor. Biol. 371, 45– 58. (10.1016/j.jtbi.2015.02.002) 25681798 · DOI
- [13]Turchin VF 1977 The phenomenon of science: a cybernetic approach to human evolution. New York, NY: Columbia University Press.
- [14]Koonin EV, Dolja VV 2013 A virocentric perspective on the evolution of life. Curr. Opin. Virol. 3, 546– 557. (10.1016/j.coviro.2013.06.008) 23850169 PMC4326007 · DOI
- [15]May RM, Anderson RM 1990 Parasite–host coevolution. Parasitology 100(Suppl. 1), S89– S101. (10.1017/S0031182000073042) 2122393 · DOI
- [16]Messinger SM, Ostling A 2009 The consequences of spatial structure for the evolution of pathogen transmission rate and virulence. Am. Nat. 174, 441– 454. (10.1086/605375) 19691436 · DOI
- [17]Koskella B, Brockhurst MA 2014 Bacteria–phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol. Rev. 38, 916– 931. (10.1111/1574-6976.12072) 24617569 PMC4257071 · DOI
- [18]Leggett HC, Brown SP, Reece SE 2014 War and peace: social interactions in infections. Phil. Trans. R. Soc. B 369, 20130365 (10.1098/rstb.2013.0365) 24686936 PMC3982666 · DOI
- [19]Gorter FA, Hall AR, Buckling A, Scanlan PD 2015 Parasite host range and the evolution of host resistance. J. Evol. Biol. 28, 1119– 1130. (10.1111/jeb.12639) 25851735 · DOI
- [20]Forterre P, Prangishvili D 2009 The great billion-year war between ribosome- and capsid-encoding organisms (cells and viruses) as the major source of evolutionary novelties. Annu. NY Acad. Sci. 1178, 65– 77. (10.1111/j.1749-6632.2009.04993.x) 19845628 · DOI
- [21]Forterre P, Prangishvili D 2013 The major role of viruses in cellular evolution: facts and hypotheses. Curr. Opin. Virol. 3, 558– 565. (10.1016/j.coviro.2013.06.013) 23870799 · DOI
- [22]Edgell DR, Chalamcharla VR, Belfort M 2011 Learning to live together: mutualism between self-splicing introns and their hosts. BMC Biol. 9, 22 (10.1186/1741-7007-9-22) 21481283 PMC3073962 · DOI
- [24]Bao X, Roossinck MJ 2013 A life history view of mutualistic viral symbioses: quantity or quality for cooperation? Curr. Opin. Microbiol. 16, 514– 518. (10.1016/j.mib.2013.05.007) 23796963 · DOI
- [25]Shirogane Y, Watanabe S, Yanagi Y 2013 Cooperation: another mechanism of viral evolution. Trends Microbiol. 21, 320– 324. (10.1016/j.tim.2013.05.004) 23764388 · DOI
- [26]Kazazian HH Jr 2004 Mobile elements: drivers of genome evolution. Science 303, 1626– 1632. (10.1126/science.1089670) 15016989 · DOI · Paper page
- [27]Goodier JL, Kazazian HH Jr 2008 Retrotransposons revisited: the restraint and rehabilitation of parasites. Cell 135, 23– 35. (10.1016/j.cell.2008.09.022) 18854152 · DOI
- [28]Hua-Van A, Le Rouzic A, Maisonhaute C, Capy P 2005 Abundance, distribution and dynamics of retrotransposable elements and transposons: similarities and differences. Cytogenet. Genome Res. 110, 426– 440. (10.1159/000084975) 16093695 · DOI
- [29]Jurka J, Kapitonov VV, Kohany O, Jurka MV 2007 Repetitive sequences in complex genomes: structure and evolution. Annu. Rev. Genomics Hum. Genet. 8, 241– 259. (10.1146/annurev.genom.8.080706.092416) 17506661 · DOI
- [30]Huda A, Jordan IK 2009 Epigenetic regulation of Mammalian genomes by transposable elements. Annu. NY Acad. Sci. 1178, 276– 284. (10.1111/j.1749-6632.2009.05007.x) 19845643 · DOI
- [31]Werren JH 2011 Selfish genetic elements, genetic conflict, and evolutionary innovation. Proc. Natl Acad. Sci. USA 108(Suppl 2), 10 863– 10 870. (10.1073/pnas.1102343108) PMC3131821 21690392 · DOI
- [32]López-Flores I, Garrido-Ramos MA 2012 The repetitive DNA content of eukaryotic genomes. Genome Dyn. 7, 1– 28. (10.1159/000337118) 22759811 · DOI
- [33]Miller WJ, Capy P 2004 Mobile genetic elements as natural tools for genome evolution. Methods Mol. Biol. 260, 1– 20. 15020798
- [34]Levin HL, Moran JV 2011 Dynamic interactions between transposable elements and their hosts. Nat. Rev. Genet. 12, 615– 627. (10.1038/nrg3030) 21850042 PMC3192332 · DOI · Paper page
- [35]Sullivan MB, Lindell D, Lee JA, Thompson LR, Bielawski JP, Chisholm SW 2006 Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol. 4, e234 (10.1371/journal.pbio.0040234) 16802857 PMC1484495 · DOI
- [36]Lindell D et al. 2007 Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449, 83– 86. (10.1038/nature06130) 17805294 · DOI
- [37]Lang AS, Zhaxybayeva O, Beatty JT 2012 Gene transfer agents: phage-like elements of genetic exchange. Nat. Rev. Microbiol. 10, 472– 482. 22683880 PMC3626599
- [38]Cortez D, Forterre P, Gribaldo S 2009 A hidden reservoir of integrative elements is the major source of recently acquired foreign genes and ORFans in archaeal and bacterial genomes. Genome Biol. 10, R65 (10.1186/gb-2009-10-6-r65) 19531232 PMC2718499 · DOI
- [39]Jalasvuori M 2012 Vehicles, replicators, and intercellular movement of genetic information: evolutionary dissection of a bacterial cell. Int. J. Evol. Biol. 2012, 874153 (10.1155/2012/874153) 22567533 PMC3332184 · DOI
- [40]Jalasvuori M, Koonin EV 2015 Classification of prokaryotic genetic replicators: between selfishness and altruism. Annu. NY Acad. Sci. 1341, 96– 105. (10.1111/nyas.12696) PMC4390439 25703428 · DOI
- [41]Koonin EV, Starokadomskyy P 2016 Are viruses alive? The replicator paradigm sheds a decisive light on an old but misguided question. Stud. Hist. Philos. Biol. Biomed. Sci. (10.1016/j.shpsc.2016.02.016) PMC5406846 26965225 · DOI
- [42]Koonin EV, Dolja VV 2014 Virus world as an evolutionary network of viruses and capsidless selfish elements. Microbiol. Mol. Biol. Rev. 78, 278– 303. (10.1128/MMBR.00049-13) 24847023 PMC4054253 · DOI
- [43]Canchaya C, Fournous G, Chibani-Chennoufi S, Dillmann M-L, Brüssow H 2003 Phage as agents of lateral gene transfer. Curr. Opin. Microbiol. 6, 417– 424. (10.1016/S1369-5274(03)00086-9) 12941415 · DOI
- [44]Łoś M, We¸grzyn G 2012 Pseudolysogeny. Adv. Virus Res. 82, 339– 349. (10.1016/B978-0-12-394621-8.00019-4) 22420857 · DOI
- [45]Sherwood R, Casjens SR, Hendrix RW 2015 Bacteriophage lambda: early pioneer and still relevant. Virology 479–480, 310– 330. (10.1016/j.virol.2015.02.010) PMC4424060 25742714 · DOI
- [46]Mayer J, Meese E 2005 Human endogenous retroviruses in the primate lineage and their influence on host genomes. Cytogenet. Genome Res. 110, 448– 456. (10.1159/000084977) 16093697 · DOI
- [47]Friedli M, Trono D 2015 The developmental control of transposable elements and the evolution of higher species. Annu. Rev. Cell Dev. Biol. 31, 429– 451. (10.1146/annurev-cellbio-100814-125514) 26393776 · DOI
- [48]Briani F, Dehò G, Forti F, Ghisotti D 2001 The plasmid status of satellite bacteriophage P4. Plasmid 45, 1– 17. (10.1006/plas.2000.1497) 11319927 · DOI
- [49]Suttle CA 2005 Viruses in the sea. Nature 437, 356– 361. (10.1038/nature04160) 16163346 · DOI
- [50]Suttle CA 2007 Marine viruses--major players in the global ecosystem. Nat. Rev. Microbiol. 5, 801– 812. (10.1038/nrmicro1750) 17853907 · DOI
- [51]Rohwer F, Thurber RV 2009 Viruses manipulate the marine environment. Nature 459, 207– 212. (10.1038/nature08060) 19444207 · DOI
- [52]Ignacio-Espinoza JC, Solonenko SA, Sullivan MB 2013 The global virome: not as big as we thought? Curr. Opin. Virol. 3, 566– 571. (10.1016/j.coviro.2013.07.004) 23896279 · DOI
- [53]Forterre P 2011 Manipulation of cellular syntheses and the nature of viruses: the virocell concept. C R Chim. 14, 392– 399. (10.1016/j.crci.2010.06.007) · DOI
- [54]Forterre P 2013 The virocell concept and environmental microbiology. ISME J. 7, 233– 236. (10.1038/ismej.2012.110) 23038175 PMC3554396 · DOI
- [56]Szathmáry E 1992 Viral sex, levels of selection, and the origin of life. J. Theor. Biol. 159, 99– 109. (10.1016/S0022-5193(05)80770-2) 1291813 · DOI
- [58]Takeuchi N, Hogeweg P 2012 Evolutionary dynamics of RNA-like replicator systems: a bioinformatic approach to the origin of life. Phys. Life Rev. 9, 219– 263. (10.1016/j.plrev.2012.06.001) 22727399 PMC3466355 · DOI
- [59]Haruna I, Spiegelman S 1965 Autocatalytic synthesis of a viral RNA in vitro. Science 150, 884– 886. (10.1126/science.150.3698.884) 5835788 · DOI
- [60]Spiegelman S, Haruna I, Pace NR, Mills DR, Bishop DHL, Claybrook JR, Peterson R 1967 Studies in the replication of viral RNA. J. Cell. Physiol. 70(Suppl. 1), 35– 64. (10.1002/jcp.1040700405) 5582808 · DOI
- [61]Spiegelman S 1971 An approach to the experimental analysis of precellular evolution. Q. Rev. Biophys. 4, 213– 253. (10.1017/S0033583500000639) 5134462 · DOI
- [62]Mills DR, Kramer FR, Spiegelman S 1973 Complete nucleotide sequence of a replicating RNA molecule. Science 180, 916– 927. (10.1126/science.180.4089.916) 4706684 · DOI
- [63]Koonin EV, Senkevich TG, Dolja VV 2006 The ancient Virus World and evolution of cells. Biol. Direct 1, 29 (10.1186/1745-6150-1-29) 16984643 PMC1594570 · DOI
- [64]Koonin EV 2009 On the origin of cells and viruses: primordial virus world scenario. Annu. NY Acad. Sci. 1178, 47– 64. (10.1111/j.1749-6632.2009.04992.x) PMC3380365 19845627 · DOI
- [65]Koonin EV 2014 The origins of cellular life. Antonie Van Leeuwenhoek 106, 27– 41. (10.1007/s10482-014-0169-5) 24756907 PMC7087693 · DOI · Paper page
- [66]Takeuchi N, Hogeweg P 2007 The role of complex formation and deleterious mutations for the stability of RNA-like replicator systems. J. Mol. Evol. 65, 668– 686. (10.1007/s00239-007-9044-6) 17955153 · DOI
- [67]Higgs PG, Lehman N 2015 The RNA world: molecular cooperation at the origins of life. Nat. Rev. Genet. 16, 7– 17. (10.1038/nrg3841) 25385129 · DOI · Paper page
- [68]Takeuchi N, Hogeweg P, Koonin EV 2011 On the origin of DNA genomes: evolution of the division of labor between template and catalyst in model replicator systems. PLoS Comput. Biol. 7, e1002024 (10.1371/journal.pcbi.1002024) 21455287 PMC3063752 · DOI
- [69]Shay JA, Huynh C, Higgs PG 2015 The origin and spread of a cooperative replicase in a prebiotic chemical system. J. Theor. Biol. 364, 249– 259. (10.1016/j.jtbi.2014.09.019) 25245369 · DOI
- [70]Jalasvuori M, Bamford JKH 2008 Structural co-evolution of viruses and cells in the primordial world. Orig. Life Evol. Biosph. 38, 165– 181. (10.1007/s11084-008-9121-x) 18228159 · DOI
- [71]Jalasvuori M, Mattila S, Hoikkala V 2015 Chasing the origin of viruses: capsid-forming genes as a life-saving preadaptation within a community of early replicators. PLoS ONE 10, e0126094 (10.1371/journal.pone.0126094) 25955384 PMC4425637 · DOI
- [72]Atkins JF, Gesteland RF, Cech TR (eds). 2010 RNA worlds: from life's origins to diversity in gene regulation, 3rd edn Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
- [73]Bernhardt HS 2012 The RNA world hypothesis: the worst theory of the early evolution of life (except for all the others). Biol. Direct 7, 23 (10.1186/1745-6150-7-23) 22793875 PMC3495036 · DOI
- [75]Forterre P 2006 The origin of viruses and their possible roles in major evolutionary transitions. Virus Res. 117, 5– 16. (10.1016/j.virusres.2006.01.010) 16476498 · DOI · Paper page
- [76]Forterre P 2006 Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: a hypothesis for the origin of cellular domain. Proc. Natl Acad. Sci. USA 103, 3669– 3674. (10.1073/pnas.0510333103) 16505372 PMC1450140 · DOI
- [77]Stewart FM, Levin BR 1984 The population biology of bacterial viruses: why be temperate. Theor. Popul. Biol. 26, 93– 117. (10.1016/0040-5809(84)90026-1) 6484871 · DOI
- [78]Maslov S, Sneppen K 2015 Well-temperate phage: optimal bet-hedging against local environmental collapses. Sci. Rep. 5, 10523 (10.1038/srep10523) 26035282 PMC4451807 · DOI
- [79]Villarreal LP, DeFilippis VR 2000 A hypothesis for DNA viruses as the origin of eukaryotic replication proteins. J. Virol. 74, 7079– 7084. (10.1128/JVI.74.15.7079-7084.2000) 10888648 PMC112226 · DOI
- [81]Koonin EV 2011 The logic of chance: the nature and origin of biological evolution. Upper Saddle River, NJ: FT press.
- [84]Koonin EV 2009 Evolution of genome architecture. Int. J. Biochem. Cell Biol. 41, 298– 306. (10.1016/j.biocel.2008.09.015) 18929678 PMC3272702 · DOI
- [85]Lane N, Martin W 2010 The energetics of genome complexity. Nature 467, 929– 934. (10.1038/nature09486) 20962839 · DOI · Paper page
- [86]Palazzo AF, Gregory TR 2014 The case for junk DNA. PLoS Genet. 10, e1004351 (10.1371/journal.pgen.1004351) 24809441 PMC4014423 · DOI
- [87]Elliott TA, Gregory TR 2015 What's in a genome? The C-value enigma and the evolution of eukaryotic genome content. Phil. Trans. R. Soc. B 370, 20140331 (10.1098/rstb.2014.0331) 26323762 PMC4571570 · DOI · Paper page
- [88]Rogozin IB, Carmel L, Csuros M, Koonin EV 2012 Origin and evolution of spliceosomal introns. Biol. Direct 7, 11 (10.1186/1745-6150-7-11) 22507701 PMC3488318 · DOI
- [89]Koonin EV, Csuros M, Rogozin IB 2013 Whence genes in pieces: reconstruction of the exon-intron gene structures of the last eukaryotic common ancestor and other ancestral eukaryotes. Wiley Interdiscip. Rev. RNA 4, 93– 105. (10.1002/wrna.1143) 23139082 · DOI
- [90]Martin W, Koonin EV 2006 Introns and the origin of nucleus-cytosol compartmentation. Nature 440, 41– 45. (10.1038/nature04531) 16511485 · DOI
- [91]Koonin EV 2006 The origin of introns and their role in eukaryogenesis: a compromise solution to the introns-early versus introns-late debate? Biol. Direct 1, 22 (10.1186/1745-6150-1-22) 16907971 PMC1570339 · DOI
- [92]López-García P, Moreira D 2006 Selective forces for the origin of the eukaryotic nucleus. Bioessays 28, 525– 533. (10.1002/bies.20413) 16615090 · DOI
- [94]Embley TM, Williams TA 2015 Evolution: steps on the road to eukaryotes. Nature 521, 169– 170. (10.1038/nature14522) 25945740 · DOI
- [95]Koonin EV 2015 Archaeal ancestors of eukaryotes: not so elusive any more. BMC Biol. 13, 84 (10.1186/s12915-015-0194-5) 26437773 PMC4594999 · DOI
- [96]Godfrey-Smith P 2015 Reproduction, symbiosis, and the eukaryotic cell. Proc. Natl Acad. Sci. USA 112, 10 120– 10 125. (10.1073/pnas.1421378112) 26286983 PMC4547265 · DOI
- [97]Forterre P 2013 The common ancestor of archaea and eukarya was not an archaeon. Archaea 2013, 372396 (10.1155/2013/372396) 24348094 PMC3855935 · DOI
- [98]López-García P, Moreira D 2015 Open Questions on the Origin of Eukaryotes. Trends Ecol. Evol. 30, 697– 708. (10.1016/j.tree.2015.09.005) 26455774 PMC4640172 · DOI · Paper page
- [99]Koonin EV 2015 Energetics and population genetics at the root of eukaryotic cellular and genomic complexity. Proc. Natl Acad. Sci. USA 112, 15 777– 15 778. (10.1073/pnas.1520869112) PMC4703004 26699503 · DOI
- [100]Lynch M 2007 The frailty of adaptive hypotheses for the origins of organismal complexity. Proc. Natl Acad. Sci. USA 104(Suppl 1), 8597– 8604. (10.1073/pnas.0702207104) 17494740 PMC1876435 · DOI
- [103]Lambowitz AM, Belfort M 2015 Mobile bacterial group II introns at the crux of eukaryotic evolution. Microbiol. Spectr. 3, MDNA3-0050-2014. (10.1128/microbiolspec.MDNA3-0050-2014) PMC4394904 26104554 · DOI
- [104]Dlakic M, Mushegian A 2011 Prp8, the pivotal protein of the spliceosomal catalytic center, evolved from a retroelement-encoded reverse transcriptase. RNA 17, 799– 808. (10.1261/rna.2396011) 21441348 PMC3078730 · DOI
- [105]de Lange T 2015 A loopy view of telomere evolution. Front. Genet. 6, 321 (10.3389/fgene.2015.00321) 26539211 PMC4612135 · DOI
- [106]Gladyshev EA, Arkhipova IR 2011 A widespread class of reverse transcriptase-related cellular genes. Proc. Natl Acad. Sci. USA 108, 20 311– 20 316. (10.1073/pnas.1100266108) PMC3251080 21876125 · DOI
- [107]Filée J, Forterre P 2005 Viral proteins functioning in organelles: a cryptic origin? Trends Microbiol. 13, 510– 513. (10.1016/j.tim.2005.08.012) 16157484 · DOI
- [108]Shutt TE, Gray MW 2006 Bacteriophage origins of mitochondrial replication and transcription proteins. Trends Genet. 22, 90– 95. (10.1016/j.tig.2005.11.007) 16364493 · DOI
- [109]Shutt TE, Gray MW 2006 Twinkle, the mitochondrial replicative DNA helicase, is widespread in the eukaryotic radiation and may also be the mitochondrial DNA primase in most eukaryotes. J. Mol. Evol. 62, 588– 599. (10.1007/s00239-005-0162-8) 16612544 · DOI
- [110]Ramesh MA, Malik SB, Logsdon JM Jr 2005 A phylogenomic inventory of meiotic genes; evidence for sex in Giardia and an early eukaryotic origin of meiosis. Curr. Biol. 15, 185– 191. 15668177
- [111]Goodenough U, Heitman J 2014 Origins of eukaryotic sexual reproduction. Cold Spring Harb. Perspect. Biol. 6, a016154 (10.1101/cshperspect.a016154) 24591519 PMC3949356 · DOI
- [112]Speijer D, Lukes J, Elias M 2015 Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life. Proc. Natl Acad. Sci. USA 112, 8827– 8834. (10.1073/pnas.1501725112) 26195746 PMC4517231 · DOI
- [113]Bernstein H, Byerly HC, Hope FA, Michod RE 1985 The evolutionary role of recombinational repair and sex. Int. Rev. Cytol. 96, 1– 28. (10.1016/S0074-7696(08)60592-6) 2416705 · DOI
- [114]Kondrashov AS 1988 Deleterious mutations and the evolution of sexual reproduction. Nature 336, 435– 440. (10.1038/336435a0) 3057385 · DOI
- [115]Kondrashov AS 2001 Sex and U. Trends Genet. 17, 75– 77. (10.1016/S0168-9525(00)02188-0) 11173114 · DOI
- [117]Hickey DA 1992 Evolutionary dynamics of transposable elements in prokaryotes and eukaryotes. Genetica 86, 269– 274. (10.1007/BF00133725) 1334911 · DOI
- [118]Hickey DA 1993 Molecular symbionts and the evolution of sex. J. Hered. 84, 410– 414. 8409362
- [119]Iyer LM, Makarova KS, Koonin EV, Aravind L 2004 Comparative genomics of the FtsK–HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res. 32, 5260– 5279. (10.1093/nar/gkh828) 15466593 PMC521647 · DOI
- [120]Ruiz-Trillo I, Burger G, Holland PWH, King N, Lang BF, Roger AJ, Gray MW 2007 The origins of multicellularity: a multi-taxon genome initiative. Trends Genet. 23, 113– 118. (10.1016/j.tig.2007.01.005) 17275133 · DOI
- [121]Rokas A 2008 The molecular origins of multicellular transitions. Curr. Opin. Genet. Dev. 18, 472– 478. (10.1016/j.gde.2008.09.004) 18926910 · DOI
- [122]Michod RE 2007 Evolution of individuality during the transition from unicellular to multicellular life. Proc. Natl Acad. Sci. USA 104(Suppl 1), 8613– 8618. (10.1073/pnas.0701489104) 17494748 PMC1876437 · DOI · Paper page
- [123]Niklas KJ, Newman SA 2013 The origins of multicellular organisms. Evol. Dev. 15, 41– 52. (10.1111/ede.12013) 23331916 · DOI
- [124]Umen JG 2014 Green algae and the origins of multicellularity in the plant kingdom. Cold Spring Harb. Perspect. Biol. 6, a016170 (10.1101/cshperspect.a016170) 25324214 PMC4413236 · DOI
- [125]Maliet O, Shelton DE, Michod RE 2015 A model for the origin of group reproduction during the evolutionary transition to multicellularity. Biol. Lett. 11, 20150157 (10.1098/rsbl.2015.0157) 26063749 PMC4528466 · DOI
- [126]Brown MW, Kolisko M, Silberman JD, Roger AJ 2012 Aggregative multicellularity evolved independently in the eukaryotic supergroup Rhizaria. Curr. Biol. 22, 1123– 1127. (10.1016/j.cub.2012.04.021) 22608512 · DOI
- [127]Du Q, Kawabe Y, Schilde C, Chen Z-H, Schaap P 2015 The evolution of aggregative multicellularity and cell–cell communication in the Dictyostelia. J. Mol. Biol. 427, 3722– 3733. (10.1016/j.jmb.2015.08.008) 26284972 PMC5055082 · DOI
- [128]Kaiser D 2001 Building a multicellular organism. Annu. Rev. Genet. 35, 103– 123. (10.1146/annurev.genet.35.102401.090145) 11700279 · DOI
- [129]Schirrmeister BE, Antonelli A, Bagheri HC 2011 The origin of multicellularity in cyanobacteria. BMC Evol. Biol. 11, 45 (10.1186/1471-2148-11-45) 21320320 PMC3271361 · DOI
- [130]Kaiser D 2013 Are Myxobacteria intelligent? Front. Microbiol. 4, 335 (10.3389/fmicb.2013.00335) 24273536 PMC3824092 · DOI
- [131]Miller MB, Bassler BL 2001 Quorum sensing in bacteria. Annu. Rev. Microbiol. 55, 165– 199. (10.1146/annurev.micro.55.1.165) 11544353 · DOI
- [132]Boyer M, Wisniewski-Dyé F 2009 Cell-cell signalling in bacteria: not simply a matter of quorum. FEMS Microbiol. Ecol. 70, 1– 19. (10.1111/j.1574-6941.2009.00745.x) 19689448 · DOI
- [133]Leist M, Jäättelä M 2001 Four deaths and a funeral: from caspases to alternative mechanisms. Nat. Rev. Mol. Cell Biol. 2, 589– 598. (10.1038/35085008) 11483992 · DOI
- [134]Baehrecke EH 2002 How death shapes life during development. Nat. Rev. Mol. Cell Biol. 3, 779– 787. (10.1038/nrm931) 12360194 · DOI
- [135]Ameisen JC 2002 On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death Differ. 9, 367– 393. (10.1038/sj.cdd.4400950) 11965491 · DOI
- [136]Ameisen JC 2004 Looking for death at the core of life in the light of evolution. Cell Death Differ. 11, 4– 10. (10.1038/sj.cdd.4401356) 14647240 · DOI
- [137]Twomey C, McCarthy JV 2005 Pathways of apoptosis and importance in development. J. Cell Mol. Med. 9, 345– 359. (10.1111/j.1582-4934.2005.tb00360.x) 15963254 PMC6740094 · DOI
- [138]Nedelcu AM, Driscoll WW, Durand PM, Herron MD, Rashidi A 2011 On the paradigm of altruistic suicide in the unicellular world. Evolution 65, 3– 20. (10.1111/j.1558-5646.2010.01103.x) 20722725 · DOI
- [139]Taylor-Brown E, Hurd H 2013 The first suicides: a legacy inherited by parasitic protozoans from prokaryote ancestors. Parasite Vectors 6, 108 (10.1186/1756-3305-6-108) PMC3640913 23597031 · DOI
- [140]Proto WR, Coombs GH, Mottram JC 2013 Cell death in parasitic protozoa: regulated or incidental? Nat. Rev. Microbiol. 11, 58– 66. (10.1038/nrmicro2929) 23202528 · DOI
- [141]Iranzo J, Lobkovsky AE, Wolf YI, Koonin EV 2014 Virus-host arms race at the joint origin of multicellularity and programmed cell death. Cell Cycle 13, 3083– 3088. (10.4161/15384101.2014.949496) 25486567 PMC4615056 · DOI
- [142]Bourke AF 2014 Hamilton's rule and the causes of social evolution. Phil. Trans. R. Soc. B 369, 20130362 (10.1098/rstb.2013.0362) 24686934 PMC3982664 · DOI
- [143]Gilbert OM, Foster KR, Mehdiabadi NJ, Strassmann JE, Queller DC 2007 High relatedness maintains multicellular cooperation in a social amoeba by controlling cheater mutants. Proc. Natl Acad. Sci. USA 104, 8913– 8917. (10.1073/pnas.0702723104) 17496139 PMC1885602 · DOI
- [144]Kuzdzal-Fick JJ, Fox SA, Strassmann JE, Queller DC 2011 High relatedness is necessary and sufficient to maintain multicellularity in Dictyostelium. Science 334, 1548– 1551. (10.1126/science.1213272) 22174251 · DOI
- [145]Ho H-I, Hirose S, Kuspa A, Shaulsky G 2013 Kin recognition protects cooperators against cheaters. Curr. Biol. 23, 1590– 1595. (10.1016/j.cub.2013.06.049) 23910661 PMC3759992 · DOI
- [146]Gerdes K, Christensen SK, Løbner-Olesen A 2005 Prokaryotic toxin-antitoxin stress response loci. Nat. Rev. Microbiol. 3, 371– 382. (10.1038/nrmicro1147) 15864262 · DOI
- [147]Makarova KS, Wolf YI, Koonin EV 2009 Comprehensive comparative-genomic analysis of Type 2 toxin-antitoxin systems and related mobile stress response systems in prokaryotes. Biol. Direct 4, 19 (10.1186/1745-6150-4-19) 19493340 PMC2701414 · DOI
- [148]Van Melderen L, Saavedra De Bast M 2009 Bacterial toxin-antitoxin systems: more than selfish entities? PLoS Genet. 5, e1000437 (10.1371/journal.pgen.1000437) 19325885 PMC2654758 · DOI
- [149]Leplae R, Geeraerts D, Hallez R, Guglielmini J, Drèze P, Van Melderen L 2011 Diversity of bacterial type II toxin-antitoxin systems: a comprehensive search and functional analysis of novel families. Nucleic Acids Res. 39, 5513– 5525. (10.1093/nar/gkr131) 21422074 PMC3141249 · DOI
- [150]Guglielmini J, Van Melderen L 2011 Bacterial toxin-antitoxin systems: Translation inhibitors everywhere. Mob. Genet. Elements 1, 283– 290. (10.4161/mge.18477) 22545240 PMC3337138 · DOI
- [151]Rankin DJ, Turner LA, Heinemann JA, Brown SP 2012 The coevolution of toxin and antitoxin genes drives the dynamics of bacterial addiction complexes and intragenomic conflict. Proc. R. Soc. B 279, 3706– 3715. (10.1098/rspb.2012.0942) PMC3415908 22787022 · DOI
- [152]Mochizuki A, Yahara K, Kobayashi I, Iwasa Y 2006 Genetic addiction: selfish gene's strategy for symbiosis in the genome. Genetics 172, 1309– 1323. (10.1534/genetics.105.042895) 16299387 PMC1456228 · DOI
- [153]Naito T, Kusano K, Kobayashi I 1995 Selfish behavior of restriction-modification systems. Science 267, 897– 899. (10.1126/science.7846533) 7846533 · DOI
- [154]Kobayashi I 2001 Behavior of restriction–modification systems as selfish mobile elements and their impact on genome evolution. Nucleic Acids Res. 29, 3742– 3756. (10.1093/nar/29.18.3742) 11557807 PMC55917 · DOI · Paper page
- [155]Van Melderen L 2010 Toxin–antitoxin systems: why so many, what for? Curr. Opin. Microbiol. 13, 781– 785. (10.1016/j.mib.2010.10.006) 21041110 · DOI
- [156]Makarova KS, Wolf YI, Koonin EV 2013 Comparative genomics of defense systems in archaea and bacteria. Nucleic Acids Res. 41, 4360– 4377. (10.1093/nar/gkt157) 23470997 PMC3632139 · DOI
- [157]Christensen-Dalsgaard M, Overgaard M, Winther KS, Gerdes K 2008 RNA decay by messenger RNA interferases. Methods Enzymol. 447, 521– 535. (10.1016/S0076-6879(08)02225-8) 19161859 · DOI
- [158]Cook GM, Robson JR, Frampton RA, McKenzie J, Przybilski R, Fineran PC, Arcus VL 2013 Ribonucleases in bacterial toxin-antitoxin systems. Biochim. Biophys. Acta 1829, 523– 531. (10.1016/j.bbagrm.2013.02.007) 23454553 · DOI
- [159]Dy RL, Przybilski R, Semeijn K, Salmond GP, Fineran PC 2014 A widespread bacteriophage abortive infection system functions through a Type IV toxin–antitoxin mechanism. Nucleic Acids Res. 42, 4590– 4605. (10.1093/nar/gkt1419) 24465005 PMC3985639 · DOI
- [160]Bickle TA, Kruger DH 1993 Biology of DNA restriction. Microbiol. Rev. 57, 434– 450. 8336674 PMC372918
- [161]Vasu K, Nagaraja V 2013 Diverse functions of restriction-modification systems in addition to cellular defense. Microbiol. Mol. Biol. Rev. 77, 53– 72. (10.1128/MMBR.00044-12) 23471617 PMC3591985 · DOI
- [162]Naito Y, Naito T, Kobayashi I 1998 Selfish restriction modification genes: resistance of a resident R/M plasmid to displacement by an incompatible plasmid mediated by host killing. Biol. Chem. 379, 429– 436. (10.1515/bchm.1998.379.4-5.429) 9628334 · DOI
- [163]Handa N, Kobayashi I 1999 Post-segregational killing by restriction modification gene complexes: observations of individual cell deaths. Biochimie 81, 931– 938. (10.1016/S0300-9084(99)00201-1) 10572308 · DOI
- [164]Shah SA, Garrett RA 2011 CRISPR/Cas and Cmr modules, mobility and evolution of adaptive immune systems. Res. Microbiol. 162, 27– 38. (10.1016/j.resmic.2010.09.001) 20863886 · DOI
- [165]Makarova KS et al. 2015 An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol. 13, 722– 736. (10.1038/nrmicro3569) 26411297 PMC5426118 · DOI
- [166]Krupovic M, Makarova KS, Forterre P, Prangishvili D, Koonin EV 2014 Casposons: a new superfamily of self-synthesizing DNA transposons at the origin of prokaryotic CRISPR-Cas immunity. BMC Biol. 12, 36 (10.1186/1741-7007-12-36) 24884953 PMC4046053 · DOI
- [167]Koonin EV, Krupovic M 2015 Evolution of adaptive immunity from transposable elements combined with innate immune systems. Nat. Rev. Genet. 16, 184– 192. (10.1038/nrg3859) 25488578 PMC5898214 · DOI
- [168]Nunez JK, Lee AS, Engelman A, Doudna JA 2015 Integrase-mediated spacer acquisition during CRISPR-Cas adaptive immunity. Nature 519, 193– 198. (10.1038/nature14237) 25707795 PMC4359072 · DOI
- [169]Noto T, Kataoka K, Suhren JH, Hayashi A, Woolcock KJ, Gorovsky MA, Mochizuki K 2015 Small-RNA-mediated genome-wide trans-recognition network in tetrahymena DNA elimination. Mol. Cell 59, 229– 242. (10.1016/j.molcel.2015.05.024) 26095658 PMC4518040 · DOI
- [170]Shmakov S et al. 2015 Discovery and functional characterization of diverse class 2 CRISPR-Cas systems. Mol. Cell 60, 385– 397. (10.1016/j.molcel.2015.10.008) 26593719 PMC4660269 · DOI
- [171]Seed KD, Lazinski DW, Calderwood SB, Camilli A 2013 A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature 494, 489– 491. (10.1038/nature11927) 23446421 PMC3587790 · DOI
- [172]Koonin EV 2014 The double-edged sword of Lamarck: comment on ‘Diversity, evolution, and therapeutic applications of small RNAs in prokaryotic and eukaryotic immune systems’ by Edwin L. Cooper and Nicola Overstreet. Phys. Life Rev. 11, 141– 143; discussion 149–151 (10.1016/j.plrev.2013.12.002) 24365235 PMC5875914 · DOI
- [173]Aravind L, Anantharaman V, Zhang D, de Souza RF, Iyer LM 2012 Gene flow and biological conflict systems in the origin and evolution of eukaryotes. Front. Cell Infect. Microbiol. 2, 89 (10.3389/fcimb.2012.00089) 22919680 PMC3417536 · DOI
- [174]Toro N, Nisa-Martinez R 2014 Comprehensive phylogenetic analysis of bacterial reverse transcriptases. PLoS ONE 9, e114083 (10.1371/journal.pone.0114083) 25423096 PMC4244168 · DOI
- [175]Schmitz-Linneweber C, Lampe MK, Sultan LD, Ostersetzer-Biran O 2015 Organellar maturases: A window into the evolution of the spliceosome. Biochim. Biophys. Acta 1847, 798– 808. (10.1016/j.bbabio.2015.01.009) 25626174 · DOI
- [176]Basu MK, Rogozin IB, Deusch O, Dagan T, Martin W, Koonin EV 2008 Evolutionary dynamics of introns in plastid-derived genes in plants: saturation nearly reached but slow intron gain continues. Mol. Biol. Evol. 25, 111– 119. (10.1093/molbev/msm234) 17974547 · DOI
- [177]Nunn CL, Craft ME, Gillespie TR, Schaller M, Kappeler PM 2015 The sociality–health–fitness nexus: synthesis, conclusions and future directions. Phil. Trans. R. Soc. B 370, 20140115 (10.1098/rstb.2014.0115) 25870401 PMC4410381 · DOI
- [178]Kappeler PM, Cremer S, Nunn CL 2015 Sociality and health: impacts of sociality on disease susceptibility and transmission in animal and human societies. Phil. Trans. R. Soc. B 370, 20140116 (10.1098/rstb.2014.0116) 25870402 PMC4410382 · DOI
- [179]Brunet TD, Doolittle WF 2015 Multilevel selection theory and the evolutionary functions of transposable elements. Genome Biol. Evol. 7, 2445– 2457. (10.1093/gbe/evv152) 26253318 PMC4558868 · DOI
- [180]Kapitonov VV, Jurka J 2005 RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol. 3, e181 (10.1371/journal.pbio.0030181) 15898832 PMC1131882 · DOI · Paper page
- [181]Kapitonov VV, Koonin EV 2015 Evolution of the RAG1-RAG2 locus: both proteins came from the same transposon. Biol. Direct 10, 20 (10.1186/s13062-015-0055-8) 25928409 PMC4411706 · DOI
- [182]Dupressoir A, Lavialle C, Heidmann T 2012 From ancestral infectious retroviruses to bona fide cellular genes: role of the captured syncytins in placentation. Placenta 33, 663– 671. (10.1016/j.placenta.2012.05.005) 22695103 · DOI · Paper page
- [183]Lavialle C, Cornelis G, Dupressoir A, Esnault C, Heidmann O, Vernochet C, Heidmann T 2013 Paleovirology of 'syncytins’, retroviral env genes exapted for a role in placentation. Phil. Trans. R. Soc. B 368, 20120507 (10.1098/rstb.2012.0507) 23938756 PMC3758191 · DOI · Paper page
- [184]Imakawa K, Nakagawa S, Miyazawa T 2015 Baton pass hypothesis: successive incorporation of unconserved endogenous retroviral genes for placentation during mammalian evolution. Genes Cells 20, 771– 788. (10.1111/gtc.12278) 26442811 · DOI
- [185]McInerney JO, Pisani D, Bapteste E, O'Connell MJ 2011 The public goods hypothesis for the evolution of life on Earth. Biol. Direct 6, 41 (10.1186/1745-6150-6-41) 21861918 PMC3179745 · DOI
- [186]McInerney J, Cummins C, Haggerty L 2011 Goods-thinking vs. tree-thinking: finding a place for mobile genetic elements. Mob. Genet. Elements 1, 304– 308. (10.4161/mge.19153) 22545244 PMC3337142 · DOI
- [188]Martin WF, Garg S, Zimorski V 2015 Endosymbiotic theories for eukaryote origin. Phil. Trans. R. Soc. B 370, 20140330 (10.1098/rstb.2014.0330) 26323761 PMC4571569 · DOI · Paper page
Cited by
Sorted by citations
From telomere to telomere: The transcriptional and epigenetic state of human repeat elements
Hoyt, S. J., Storer, J. M., Hartley, G. A., Grady, P. G. S., Gershman, A., de Lima, L. G., Limouse, C., Halabian, R., Wojenski, L., Rodriguez, M., et al. (2022) · Science · doi:10.1126/science.abk3112 · Cited by 411 · see citing works
Transposon-associated TnpB is a programmable RNA-guided DNA endonuclease
Karvelis, T., Druteika, G., Bigelyte, G., Budre, K., Zedaveinyte, R., Silanskas, A., Kazlauskas, D., Venclovas, Č., & Siksnys, V. (2021) · Nature · doi:10.1038/s41586-021-04058-1 · Cited by 348 · see citing works
Inevitability of Genetic Parasites
Iranzo, J., Puigbò, P., Lobkovsky, A. E., Wolf, Y. I., & Koonin, E. V. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw193 · Cited by 90 · see citing works
“Thus, the primordial parasite-host arms race could have been a key driver of the evolution of biological complexity (Koonin 2016).”
BackgroundSelf-citationKoonin, E. V., Wolf, Y. I., & Katsnelson, M. I. (2017) · Biology Direct · doi:10.1186/s13062-017-0202-5 · Cited by 74 · see citing works
Self-citationFundamental constraints to the logic of living systems
Solé, R., Kempes, C. P., Corominas-Murtra, B., De Domenico, M., Kolchinsky, A., Lachmann, M., Libby, E., Saavedra, S., Smith, E., & Wolpert, D. (2024) · Interface Focus · doi:10.1098/rsfs.2024.0010 · Cited by 34 · see citing works
- Authors
- Koonin, E. V.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Koonin, Eugene V.
- ORCID
- Koonin, Eugene V.
- Venue
- Philosophical Transactions of the Royal Society B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2016-08-19
- Volume
- 371
- Issue
- 1701
- Pages
- 20150442
- ISSN
- 0962-8436 (ISSN-L)
- 1471-2970
- PMC
- PMC4958936
- OpenAlex
- W2479867351
- Cited by
- 161
- References
- 8
- Citations by year
- 2026: 14 · 2025: 15 · 2024: 12 · 2023: 16 · 2022: 16 · 2021: 20 · 2020: 17 · 2019: 15 · 2018: 17 · 2017: 14 · 2016: 5
- FWCI
- 2.27
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- US Department of Health and Human Services (Intramural funds)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
- Social Sciences › Sociology and Political Science › Evolutionary Game Theory and Cooperation
- Keywords
- evolutionary transitions, viruses, mobile genetic elements, selfish genetic elements, host-parasite coevolution, multicellularity, eukaryotic origin, eusociality, plasmids, transposable elements, public goods, gene recruitment, organizational complexity
- MeSH terms
- Biological Evolution, Viruses, Interspersed Repetitive Sequences
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review