Cited by 161Evolution and Genetic DynamicsOrigins and Evolution of LifeEvolutionary Game Theory and Cooperation

Viruses and mobile elements as drivers of evolutionary transitions

Open access
Koonin, Eugene V.·2016·Philosophical Transactions of the Royal Society B: Biological Sciences

Abstract

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1098/rstb.2015.0442

Cites

8 of 8 references verified0 citation errors · 0 not checkable

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.

A few free checks a day · papers already verified open instantly · results are public

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

Flagged first, then by citations

Research works printed but not linked: 173

  1. [2]Dobzhansky T 1937 Genetics and the origin of species. New York, NY: Columbia University Press.
  2. [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
  3. [6]Maynard Smith J 1998 The units of selection. Novartis Found Symp. 213, 203– 211; discussion 211–207. 9653725
  4. [7]Szathmáry E 2001 Biological information, kin selection, and evolutionary transitions. Theor. Popul. Biol. 59, 11– 14. (10.1006/tpbi.2000.1503) 11243923 · DOI
  5. [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
  6. [9]Queller DC 1997 Cooperators since life began. Q. Rev. Biol. 72, 184– 188. (10.1086/419766) · DOI
  7. [10]Bass LW 1988 The evolution of individuality. Princeton, NJ: Princeton University Press.
  8. [11]Michod RE 1999 Darwinian dynamics: evolutionary transitions in fitness and individuality. Princeton, NY: Princeton University Press.
  9. [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
  10. [13]Turchin VF 1977 The phenomenon of science: a cybernetic approach to human evolution. New York, NY: Columbia University Press.
  11. [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
  12. [15]May RM, Anderson RM 1990 Parasite–host coevolution. Parasitology 100(Suppl. 1), S89– S101. (10.1017/S0031182000073042) 2122393 · DOI
  13. [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
  14. [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
  15. [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
  16. [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
  17. [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
  18. [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
  19. [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
  20. [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
  21. [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
  22. [26]Kazazian HH Jr 2004 Mobile elements: drivers of genome evolution. Science 303, 1626– 1632. (10.1126/science.1089670) 15016989 · DOI · Paper page
  23. [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
  24. [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
  25. [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
  26. [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
  27. [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
  28. [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
  29. [33]Miller WJ, Capy P 2004 Mobile genetic elements as natural tools for genome evolution. Methods Mol. Biol. 260, 1– 20. 15020798
  30. [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
  31. [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
  32. [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
  33. [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
  34. [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
  35. [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
  36. [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
  37. [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
  38. [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
  39. [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
  40. [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
  41. [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
  42. [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
  43. [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
  44. [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
  45. [49]Suttle CA 2005 Viruses in the sea. Nature 437, 356– 361. (10.1038/nature04160) 16163346 · DOI
  46. [50]Suttle CA 2007 Marine viruses--major players in the global ecosystem. Nat. Rev. Microbiol. 5, 801– 812. (10.1038/nrmicro1750) 17853907 · DOI
  47. [51]Rohwer F, Thurber RV 2009 Viruses manipulate the marine environment. Nature 459, 207– 212. (10.1038/nature08060) 19444207 · DOI
  48. [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
  49. [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
  50. [54]Forterre P 2013 The virocell concept and environmental microbiology. ISME J. 7, 233– 236. (10.1038/ismej.2012.110) 23038175 PMC3554396 · DOI
  51. [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
  52. [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
  53. [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
  54. [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
  55. [61]Spiegelman S 1971 An approach to the experimental analysis of precellular evolution. Q. Rev. Biophys. 4, 213– 253. (10.1017/S0033583500000639) 5134462 · DOI
  56. [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
  57. [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
  58. [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
  59. [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
  60. [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
  61. [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
  62. [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
  63. [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
  64. [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
  65. [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
  66. [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.
  67. [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
  68. [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
  69. [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
  70. [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
  71. [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
  72. [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
  73. [81]Koonin EV 2011 The logic of chance: the nature and origin of biological evolution. Upper Saddle River, NJ: FT press.
  74. [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
  75. [85]Lane N, Martin W 2010 The energetics of genome complexity. Nature 467, 929– 934. (10.1038/nature09486) 20962839 · DOI · Paper page
  76. [86]Palazzo AF, Gregory TR 2014 The case for junk DNA. PLoS Genet. 10, e1004351 (10.1371/journal.pgen.1004351) 24809441 PMC4014423 · DOI
  77. [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
  78. [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
  79. [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
  80. [90]Martin W, Koonin EV 2006 Introns and the origin of nucleus-cytosol compartmentation. Nature 440, 41– 45. (10.1038/nature04531) 16511485 · DOI
  81. [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
  82. [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
  83. [94]Embley TM, Williams TA 2015 Evolution: steps on the road to eukaryotes. Nature 521, 169– 170. (10.1038/nature14522) 25945740 · DOI
  84. [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
  85. [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
  86. [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
  87. [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
  88. [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
  89. [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
  90. [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
  91. [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
  92. [105]de Lange T 2015 A loopy view of telomere evolution. Front. Genet. 6, 321 (10.3389/fgene.2015.00321) 26539211 PMC4612135 · DOI
  93. [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
  94. [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
  95. [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
  96. [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
  97. [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
  98. [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
  99. [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
  100. [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
  101. [114]Kondrashov AS 1988 Deleterious mutations and the evolution of sexual reproduction. Nature 336, 435– 440. (10.1038/336435a0) 3057385 · DOI
  102. [115]Kondrashov AS 2001 Sex and U. Trends Genet. 17, 75– 77. (10.1016/S0168-9525(00)02188-0) 11173114 · DOI
  103. [117]Hickey DA 1992 Evolutionary dynamics of transposable elements in prokaryotes and eukaryotes. Genetica 86, 269– 274. (10.1007/BF00133725) 1334911 · DOI
  104. [118]Hickey DA 1993 Molecular symbionts and the evolution of sex. J. Hered. 84, 410– 414. 8409362
  105. [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
  106. [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
  107. [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
  108. [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
  109. [123]Niklas KJ, Newman SA 2013 The origins of multicellular organisms. Evol. Dev. 15, 41– 52. (10.1111/ede.12013) 23331916 · DOI
  110. [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
  111. [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
  112. [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
  113. [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
  114. [128]Kaiser D 2001 Building a multicellular organism. Annu. Rev. Genet. 35, 103– 123. (10.1146/annurev.genet.35.102401.090145) 11700279 · DOI
  115. [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
  116. [130]Kaiser D 2013 Are Myxobacteria intelligent? Front. Microbiol. 4, 335 (10.3389/fmicb.2013.00335) 24273536 PMC3824092 · DOI
  117. [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
  118. [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
  119. [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
  120. [134]Baehrecke EH 2002 How death shapes life during development. Nat. Rev. Mol. Cell Biol. 3, 779– 787. (10.1038/nrm931) 12360194 · DOI
  121. [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
  122. [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
  123. [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
  124. [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
  125. [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
  126. [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
  127. [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
  128. [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
  129. [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
  130. [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
  131. [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
  132. [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
  133. [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
  134. [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
  135. [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
  136. [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
  137. [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
  138. [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
  139. [153]Naito T, Kusano K, Kobayashi I 1995 Selfish behavior of restriction-modification systems. Science 267, 897– 899. (10.1126/science.7846533) 7846533 · DOI
  140. [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
  141. [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
  142. [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
  143. [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
  144. [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
  145. [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
  146. [160]Bickle TA, Kruger DH 1993 Biology of DNA restriction. Microbiol. Rev. 57, 434– 450. 8336674 PMC372918
  147. [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
  148. [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
  149. [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
  150. [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
  151. [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
  152. [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
  153. [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
  154. [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
  155. [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
  156. [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
  157. [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
  158. [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
  159. [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
  160. [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
  161. [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
  162. [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
  163. [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
  164. [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
  165. [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
  166. [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
  167. [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
  168. [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
  169. [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
  170. [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
  171. [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
  172. [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
  173. [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

Authors
Koonin, E. V.
Affiliations
National Institutes of Health (US)
Corresponding author
Koonin, Eugene V.
Venue
Philosophical Transactions of the Royal Society B: Biological Sciences
Published
2016-08-19
Volume
371
Issue
1701
Pages
20150442
ISSN
  • 0962-8436 (ISSN-L)
  • 1471-2970
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
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