The Biological Big Bang model for the major transitions in evolution.
BACKGROUND
Major transitions in biological evolution show the same pattern of sudden emergence of diverse forms at a new level of complexity. The relationships between major groups within an emergent new class of biological entities are hard to decipher and do not seem to fit the tree pattern that, following Darwin's original proposal, remains the dominant description of biological evolution. The cases in point include the origin of complex RNA molecules and protein folds; major groups of viruses; archaea and bacteria, and the principal lineages within each of these prokaryotic domains; eukaryotic supergroups; and animal phyla. In each of these pivotal nexuses in life's history, the principal "types" seem to appear rapidly and fully equipped with the signature features of the respective new level of biological organization. No intermediate "grades" or intermediate forms between different types are detectable. Usually, this pattern is attributed to cladogenesis compressed in time, combined with the inevitable erosion of the phylogenetic signal.


OBJECTIVE
I propose that most or all major evolutionary transitions that show the "explosive" pattern of emergence of new types of biological entities correspond to a boundary between two qualitatively distinct evolutionary phases. The first, inflationary phase is characterized by extremely rapid evolution driven by various processes of genetic information exchange, such as horizontal gene transfer, recombination, fusion, fission, and spread of mobile elements. These processes give rise to a vast diversity of forms from which the main classes of entities at the new level of complexity emerge independently, through a sampling process. In the second phase, evolution dramatically slows down, the respective process of genetic information exchange tapers off, and multiple lineages of the new type of entities emerge, each of them evolving in a tree-like fashion from that point on. This biphasic model of evolution incorporates the previously developed concepts of the emergence of protein folds by recombination of small structural units and origin of viruses and cells from a pre-cellular compartmentalized pool of recombining genetic elements. The model is extended to encompass other major transitions. It is proposed that bacterial and archaeal phyla emerged independently from two distinct populations of primordial cells that, originally, possessed leaky membranes, which made the cells prone to rampant gene exchange; and that the eukaryotic supergroups emerged through distinct, secondary endosymbiotic events (as opposed to the primary, mitochondrial endosymbiosis). This biphasic model of evolution is substantially analogous to the scenario of the origin of universes in the eternal inflation version of modern cosmology. Under this model, universes like ours emerge in the infinite multiverse when the eternal process of exponential expansion, known as inflation, ceases in a particular region as a result of false vacuum decay, a first order phase transition process. The result is the nucleation of a new universe, which is traditionally denoted Big Bang, although this scenario is radically different from the Big Bang of the traditional model of an expanding universe. Hence I denote the phase transitions at the end of each inflationary epoch in the history of life Biological Big Bangs (BBB).


CONCLUSIONS
A Biological Big Bang (BBB) model is proposed for the major transitions in life's evolution. According to this model, each transition is a BBB such that new classes of biological entities emerge at the end of a rapid phase of evolution (inflation) that is characterized by extensive exchange of genetic information which takes distinct forms for different BBBs. The major types of new forms emerge independently, via a sampling process, from the pool of recombining entities of the preceding generation. This process is envisaged as being qualitatively different from tree-pattern cladogenesis.
Koonin
Eugene V
EV
National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA. koonin@ncbi.nlm.nih.gov
D000818:Animals; D005075:Biological Evolution; D005057:Eukaryotic Cells; D019143:Evolution, Molecular; D022761:Gene Transfer, Horizontal; D008954:Models, Biological; D011387:Prokaryotic Cells; D011995:Recombination, Genetic
J Struct Biol. 2001 May-Jun;134(2-3):167-85
11551177
Annu Rev Microbiol. 2005;59:191-209
16153168
Biol Direct. 2006 Aug 14;1:22
16907971
Annu Rev Microbiol. 2001;55:709-42
11544372
Nature. 2006 Mar 2;440(7080):41-5
16511485
Nature. 1993 Nov 18;366(6452):223-7
8232582
BMC Evol Biol. 2005 May 31;5:34
15927057
Trends Genet. 1998 Aug;14(8):307-11
9724962
Sci Am. 2000 Feb;282(2):90-5
10710791
Science. 2002 Nov 22;298(5598):1547
12446888
Nature. 1998 Mar 5;392(6671):37-41
9510246
Philos Trans R Soc Lond B Biol Sci. 2006 Jun 29;361(1470):969-1006
16754610
Science. 1997 Apr 18;276(5311):338-41
9139351
Biol Bull. 2003 Apr;204(2):160-7
12700147
Biol Direct. 2007 May 31;2:15
17540027
Proc Natl Acad Sci U S A. 2007 May 29;104(22):9346-51
17494767
Science. 2005 Dec 23;310(5756):1933-8
16373569
Trends Cell Biol. 1999 Dec;9(12):M5-8
10611671
Gene. 2004 Jun 23;335:73-88
15194191
Stud Hist Philos Biol Biomed Sci. 2005 Mar;36(1):183-208
16120264
Symbiosis. 1987;4:185-98
11542098
Virus Res. 2006 Apr;117(1):156-84
16494962
Nat Rev Microbiol. 2007 Nov;5(11):892-9
17938630
Nature. 2006 Mar 30;440(7084):623-30
16572163
Science. 1999 Jun 25;284(5423):2124-9
10381871
Proc Natl Acad Sci U S A. 1986 Mar;83(5):1271-5
2419905
Am Nat. 1999 Oct;154(S4):S164-S177
10527925
Proc Natl Acad Sci U S A. 2007 May 29;104(22):9105-6
17519331
PLoS Biol. 2005 May;3(5):e130
15799709
Science. 2005 Feb 11;307(5711):884-90
15705842
Biol Direct. 2006 Sep 19;1:29
16984643
Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6764-71
8041695
PLoS Biol. 2006 Nov;4(11):e352
17105342
Mol Biol Evol. 2005 May;22(5):1299-308
15746017
Proc Natl Acad Sci U S A. 2005 May 3;102 Suppl 1:6595-9
15851673
BMC Evol Biol. 2001 Oct 20;1:8
11734060
Int J Dev Biol. 2003;47(7-8):505-15
14756326
Trans N Y Acad Sci. 1945 Dec;8:45-60
21012247
J Mol Biol. 2000 Jun 16;299(4):897-905
10843846
Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):6854-9
9618502
Trends Genet. 2005 Dec;21(12):647-54
16223546
Proc Natl Acad Sci U S A. 2002 Oct 29;99(22):14132-6
12384571
Crit Rev Biochem Mol Biol. 1993;28(5):375-430
8269709
Philos Trans R Soc Lond B Biol Sci. 2003 Jan 29;358(1429):59-83; discussion 83-5
12594918
Science. 2001 Jul 20;293(5529):438-9
11463899
Am J Bot. 2004 Oct;91(10):1481-93
21652304
Bioinformatics. 2007 Apr 1;23(7):815-24
17237036
Mol Biol Evol. 2007 Aug;24(8):1702-13
17488740
Curr Opin Struct Biol. 2002 Jun;12(3):392-9
12127460
Curr Biol. 2004 Jul 13;14(13):R514-6
15242632
Trends Biochem Sci. 2004 Sep;29(9):469-77
15337120
Science. 2006 May 19;312(5776):1011-4
16709776
Science. 1995 Nov 24;270(5240):1319-25
7481819
Bioessays. 1999 Aug;21(8):697-703
10440866
Proc Natl Acad Sci U S A. 2006 Aug 29;103(35):13080-5
16938841
Mol Biol Evol. 2005 Mar;22(3):387-90
15537810
J Bacteriol. 2004 Oct;186(19):6575-85
15375139
Trends Genet. 1998 Nov;14(11):442-4
9825671
Philos Trans R Soc Lond B Biol Sci. 2006 Jun 29;361(1470):1069-83
16754615
Science. 2005 Aug 12;309(5737):1022-3
16099967
Bioessays. 2004 Jan;26(1):50-60
14696040
Philos Trans R Soc Lond B Biol Sci. 2003 Jan 29;358(1429):109-33; discussion 133-4
12594921
Syst Biol. 2005 Aug;54(4):672-8
16126662
Biochemistry. 2003 Jul 29;42(29):8748-55
12873135
BMC Evol Biol. 2005 Jun 02;5:36
15932645
Proc Natl Acad Sci U S A. 2007 Feb 13;104(7):2043-9
17261804
Trends Genet. 2002 Sep;18(9):472-9
12175808
PLoS Genet. 2006 Dec;2(12):e220
17194223
Science. 2003 Jun 13;300(5626):1703-6
12805537
Proteins. 2002 Jan 1;46(1):61-71
11746703
Nucleic Acids Res. 2005 Aug 16;33(14):4626-38
16106042
Phys Rev Lett. 2006 Nov 10;97(19):191302
17155610
Trends Ecol Evol. 2005 Dec;20(12):670-6
16701456
Nucleic Acids Res. 1999 Sep 1;27(17):3389-401
10446225
Int J Syst Evol Microbiol. 2002 Mar;52(Pt 2):297-354
11931142
Science. 1999 May 21;284(5418):1305-7
10383313
J Virol. 2001 Dec;75(23):11720-34
11689653
J Eukaryot Microbiol. 2005 Sep-Oct;52(5):399-451
16248873
Curr Opin Genet Dev. 2000 Dec;10(6):596-601
11088007
Science. 2006 Feb 10;311(5762):796-800
16469913
Proc Natl Acad Sci U S A. 2002 Jun 25;99(13):8742-7
12077305
Symbiosis. 1985;1:101-24
11543608
Genome Biol. 2004;5(3):R17
15003120
Trends Ecol Evol. 1990 May;5(5):140-4
11538863
J Eukaryot Microbiol. 1999 Jul-Aug;46(4):347-66
18092388
Nature. 1999 May 27;399(6734):323-9
10360571
Nature. 2000 May 18;405(6784):299-304
10830951
Sci Am. 2004 Sep;291(3):78-87
15376755
Philos Trans R Soc Lond B Biol Sci. 2006 Jun 29;361(1470):1039-54
16754613
Science. 2007 Apr 27;316(5824):542-3; author reply 542-3
17463271
Cell. 1997 Jun 27;89(7):995-8
9215620
Mol Microbiol. 1997 Aug;25(4):619-37
9379893
Comput Appl Biosci. 1996 Aug;12(4):357-8
8902363
IUBMB Life. 2005 Aug;57(8):539-47
16118111
J Mol Biol. 1998 Dec 18;284(5):1301-5
9878351
J Struct Biol. 2001 May-Jun;134(2-3):191-203
11551179
Cell. 2000 Jun 9;101(6):573-6
10892642