31 октября самый цитируемый ученый русского происхождения, известный эволюционный биолог Евгений Кунин рассказал в Digital October о постмодернистском взгляде на эволюционные процессы. http://digitaloctober.ru/ru/events/knowledge_stream_evolyutsiya_po_sluchayu

1. Information
Comparative genomics rewrites
evolution textbooks: a
“postmodern synthesis” of
Evolutionary Biology?
Eugene V. Koonin
National Center for Biotechnology Information, NLM, NIH, Bethesda,
Maryland, USA
Moscow, Digital October, 31/10/2013

2. Information
The Modern Synthesis

3. Information
Nothing in biology makes sense except in the light of evolution
Evolutionary process represented as change in allele frequency
driven by natural selection

4. Information
The beginnings of comparative genomes
Haemophilus influenzae
Mycoplasma genitalium
Venter et al. 1995

5. Information

6. Exponential accumulation of prokaryotic genome sequences
1000
Information
No. of Sequenced Genomes
100
10
Bacteria
Archaea
1
7/3/1995
7/2/1997
7/2/1999
7/1/2001
7/1/2003
Date
6/30/2005
6/30/2007

7. 0%
Thermotoga maritima MSB8
Treponema pallidum subsp. pallidum str. Nichols
Leptospira interrogans serovar Copenhageni str. Fiocruz L1-…
Pseudomonas aeruginosa PAO1
Escherichia coli K12
Desulfovibrio vulgaris subsp. vulgaris str. Hildenborough
Burkholderia mallei ATCC 23344
Agrobacterium tumefaciens str. C58
Pirellula sp.
Fusobacterium nucleatum subsp. nucleatum ATCC 25586
Mesoplasma florum L1
Clostridium acetobutylicum ATCC 824
Lactococcus lactis subsp. lactis Il1403
Bacillus subtilis subsp. subtilis str. 168
Solibacter usitatus Ellin6076
Thermus thermophilus HB27
Deinococcus radiodurans R1
Prochlorococcus marinus subsp. marinus str. CCMP1375
Anabaena variabilis ATCC 29413
Synechocystis sp. PCC 6803
Dehalococcoides ethenogenes 195
Candidatus Protochlamydia amoebophila UWE25
Chlamydia muridarum Nigg
Chlorobium tepidum TLS
Salinibacter ruber DSM 13855
Bacteroides thetaiotaomicron VPI-5482
Aquifex aeolicus VF5
Bifidobacterium longum NCC2705
Streptomyces coelicolor A3(2)
Mycobacterium tuberculosis H37Rv
Nanoarchaeum equitans Kin4-M
Thermoplasma volcanium GSS1
Pyrococcus horikoshii OT3
Methanopyrus kandleri AV19
Methanosarcina acetivorans C2A
Methanocaldococcus jannaschii DSM 2661
Methanothermobacter thermautotrophicus str. Delta H
Halobacterium sp. NRC-1
Archaeoglobus fulgidus DSM 4304
Aeropyrum pernix K1
Information
Most (~70-80%) of genes in prokaryotic genomes are evolutionarily
conserved –belong to COGs – orthologous lineages - distinct units of evolution
100%
90%
80%
70%
60%
50%
40%
30%
20%
10%

8. Information
Understanding evolution in the
light of comparative genomics and
systems biology:
Is there a „postmodern synthesis‟
in sight?

9. Postmodern reassessment of some central propositions of
Darwin and the Modern Synthesis
Postmodern status
The material for evolution is
provided, primarily, by
random, heritable variation
(random local mutations, in
modern terms).
Information
Proposition
Only partly true. The repertoire of relevant changes greatly expanded to include duplication of
Fixation of (rare) beneficial changes by natural
selection is the main driving force of evolution.
Only partly true. Natural (positive) selection is important but is only one of several fundamental factors of
evolution and is not quantitatively dominant. Neutral processes combined with purifying selection dominate
evolution, and direct effects of environmental cues on the genome {(quasi)Lamarckian phenomena] are
important as well.
The variations fixed by natural selection are
“infinitesimally small”. Evolution adheres to
gradualism.
False. Even single gene duplications and HGT of single genes are by no means “infinitesimally small” let
alone deletion or acquisition of larger regions, genome rearrangements, whole-genome duplication, and most
dramatically, endosymbiosis. Gradualism is not the principal regime of evolution.
Uniformitarianism: evolutionary processes
remained, largely, the same throughout the
evolution of life.
Only partly true. Present day evolutionary processes were important since the origin of replication.
However, major transitions in the evolution like the origin of eukaryotes could be brought about by
(effectively) unique events such as endosymbiosis, and the earliest stages of evolution (pre-LUCA) partially
relied on distinct processes not involved in subsequent, “normal” evolution.
genes, genome regions, and entire genomes; loss of genes and, generally, genetic material; HGT
including massive gene flux in cases of endosymbiosis; invasion of mobile selfish elements and
recruitment of sequences from them; and more. More importantly, (quasi)directed, Lamarckian
variation is recognized as a major factor of evolution.

10. Information
The 3 modalities of evolution
Koonin, Wolf, Biol. Direct 2009

11. Information
NATURE REVIEWS | MICR
OBIOLOGY
VOLUME 9 | JUNE 2011 | 467

12. Information
Makarova et al. Nature Rev Microbiol 2011

13. Information
CRISPR/Cas: a case of bona fide Lamarckian evolution
…although elements of stochasticity and selection are always present
Koonin, Wolf, Biol. Direct 2009

14. Lamarck’s gift to biotechnology
Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. A programmable
dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science. 2012 Aug
17;337(6096):816-21
Information
Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang
W, Marraffini LA, Zhang F. Multiplex genome engineering using CRISPR/Cas
systems.Science. 2013 Feb 15;339(6121):819-23
Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM.
RNA-guided human genome engineering via Cas9. Science. 2013 Feb
15;339(6121):823-6.
Brouns SJ. Molecular biology. A Swiss army knife of immunity.
Science. 2012 Aug 17;337(6096):808-9
Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. Genome engineering
using the CRISPR-Cas9 system. Nat Protoc. 2013 Nov;8(11):2281-308

15. Diverse Lamarckian and quasi-Lamarckian phenomena
Phenomenon
Biological role/function
Phyletic spread
Lamarckian criteria
Genomic changes
caused by
environmental factor
Bona fide Lamarckian
Most of the
Yes
Archaea and
many bacteria
Changes are
specific to
relevant
genomic loci
Changes provide
adaptation to the
causative factor
Yes
Yes
Information
CRISPR/Cas
Defense against viruses
and other mobile elements
piRNA
Defense against
transposable elements in
germline
Animals
Yes
Yes
Yes
HGT (specific
cases)
Adaptation to new
environment, stress
response, resistance
Yes
Yes
HGT (general
phenomenon)
Diverse innovations
No
Yes/no
Stress-induced
mutagenesis
Stress response/resistance/
adaptation to new
conditions
Archaea,
Yes
bacteria,
unicellular
eukaryotes
Quasi-Lamarckian
Archaea,
Yes
bacteria,
unicellular
eukaryotes
Ubiquitous
Yes
No or
partially
Yes (but general
evolvability
enhanced as well)
Koonin, Wolf, Biol. Direct 2009

16. Postmodern reassessment of some central propositions of
Darwin and the Modern Synthesis
Postmodern status
The material for evolution is provided, primarily, by
random, heritable variation.
Information
Proposition
Only partly true. The repertoire of relevant random changes greatly expanded to include duplication of genes, genome
regions, and entire genomes; loss of genes and, generally, genetic material; HGT including massive gene flux in cases of
endosymbiosis; invasion of mobile selfish elements and recruitment of sequences from them; and more. More
importantly, (quasi)directed (Lamarckian) variation is recognized as a major factor of evolution.
The variations fixed by natural
selection are “infinitesimally small”.
Evolution strictly adheres to
gradualism.
False. Even single gene duplications and HGT of single genes are by no means “infinitesimally
Uniformitarianism: evolutionary processes remained,
largely, the same throughout the evolution of life.
Only partly true. Present day evolutionary processes were important since the origin of replication. However, major
transitions in the evolution like the origin of eukaryotes could be brought about by (effectively) unique events such as
endosymbiosis, and the earliest stages of evolution (pre-LUCA) partially relied on distinct processes not involved in
subsequent, “normal” evolution.
small” let alone deletion or acquisition of larger regions, genome rearrangements, whole-genome
duplication, and most dramatically, endosymbiosis. Gradualism is not the principal regime of
evolution.

17. The recurrent structure in the gene universe reflects dramatic genome
plasticity – extensive loss and gain of genes - at all levels
10000
Shell
Core
Cloud
1000
Shell
Core:
~70
Shell: ~5700
100
Cloud
DATA
Number of COGs
1000
Number of COGs
Core
Cloud:
~24000
10000
DATA
100
10
Information
10
1
1
0
50
100
150
200
250
300
350
0
400
338 Archaea and Bacteria
10000
DATA
Core
Accessory genome
Cloud
Shell
Number of COGs
1000
Core
genome
100
10
1
0
5
10
15
20
25
30
35
40
45
Number of Organisms
44 Escherichia and Salmonella
5
10
15
20
25
30
35
40
45
Number of Organisms
Number of Organisms
50
41 Archaea
Fractal (self-similar) structure of
the prokaryotic gene space Tripartite organization
of pangenomes at
all levels – major
differences in gene
repertoires
Koonin, Logic of Chance 2011

18. 1960-1990
PARADIGM SHIFT: from
GENOMES TO
PANGENOMES
Information
1990-2010
2010-2020
16S RNA
Genomes
Pangenomes

19. Information
Open (unlimited growth) vs closed pan-genome

20. Information
Mathematical modeling of pangenome evolution reveals closed
pangenomes and exponential growth of estimated pangenome
size with tree depth
Lobkovsky,
Wolf, Koonin,
in preparation
(Only) a million proteins for molecular biologists?

21. Postmodern reassessment of some central propositions of
Darwin and the Modern Synthesis
Postmodern status
The material for evolution is
provided, primarily, by random,
heritable variation.
Information
Proposition
Only partly true. The repertoire of relevant random changes greatly expanded to include duplication of
The variations fixed by natural selection are
“infinitesimally small”. Evolution adheres to
gradualism.
False. Even single gene duplications and HGT of single genes are by no means “infinitesimally small” let
alone deletion or acquisition of larger regions, genome rearrangements, whole-genome duplication, and most
dramatically, endosymbiosis. Gradualism is not the principal regime of evolution.
Fixation of (rare) beneficial
changes by natural selection is the
main driving force of evolution.
True only to a small extent. Natural (positive) selection is important but is only one of
Uniformitarianism: evolutionary processes
remained, largely, the same throughout the
evolution of life.
Only partly true. Present day evolutionary processes were important since the origin of replication. However,
major transitions in the evolution like the origin of eukaryotes could be brought about by (effectively) unique
events such as endosymbiosis, and the earliest stages of evolution (pre-LUCA) partially relied on distinct
processes not involved in subsequent, “normal” evolution.
genes, genome regions, and entire genomes; loss of genes and, generally, genetic material; HGT including
massive gene flux in cases of endosymbiosis; invasion of mobile selfish elements and recruitment of sequences
from them; and more. More importantly, (quasi)directed (Lamarckian) variation is recognized as a major factor
of evolution.
several fundamental factors of evolution and is not quantitatively dominant. Neutral
processes combined with purifying selection dominate evolution, and direct effects of
environmental cues on the genome - (quasi)Lamarckian phenomena - are important as well.
Universal patterns of evolution seem to emerge without natural selection

22. Information
The 3 modalities of evolution
Koonin, Wolf, Biol. Direct 2009

23. Selection and drift in classic population genetics
drift+selection – small Ne
Information
Sewall Wright
(1889-1988)
Selection - large Ne

24. Non-adaptive evolution of genomic complexity
Nothing makes sense in evolution except in light of population genetics
Lynch M. The frailty of adaptive hypotheses for the origins of organismal complexity. Proc Natl Acad Sci U S A. 2007
Lynch M, Conery JS.
The origins of genome complexity. Science. 2003 Nov 21;302(5649):1401-4.
Information
Complete genomic sequences from diverse phylogenetic lineages reveal notable increases in genome complexity from prokaryotes to
multicellular eukaryotes. The changes include gradual increases in gene number, resulting from the retention of duplicate genes, and
More abrupt increases in the abundance of spliceosomal introns and mobile genetic elements. We argue that many of these
modifications emerged passively in response to the long-term population-size reductions that accompanied increases in organism size.
According to this model, much of the restructuring of eukaryotic genomes was initiated by nonadaptive processes, and this in turn
provided novel substrates for the secondary evolution of phenotypic complexity by natural selection. The enormous long-term effective
population sizes of prokaryotes may impose a substantial barrier to the evolution of complex genomes and morphologies.

25. Information
Estimates of the composite parameter Neu for a phylogenetically
diverse assemblage of species
M Lynch, J S Conery Science 2003;302:1401-1404
Published by AAAS

26. Information
The major intrusion of stochasticity into Biology:
do statistical laws rule Life?

27. Information
Some key universals of genome/molecular phenome evolution
Karev et al. 2002; Jordan et al. 2004; Lobkovsky, Wolf, Koonin, 2010; Koonin, Wolf 2010

28. The major intrusion of stochasticity into Biology:
do statistical laws rule Life?
PLoS Comput Biol. 2011 Aug;7(8):e1002173.
Are there laws of genome evolution?
Information
Koonin EV.
Research in quantitative evolutionary genomics and systems biology led to the discovery of
several universal regularities connecting genomic and molecular phenomic variables. These
universals include the log-normal distribution of the evolutionary rates of orthologous genes; the
power law-like distributions of paralogous family size and node degree in various biological
networks; the negative correlation between a gene's sequence evolution rate and expression
level; and differential scaling of functional classes of genes with genome size.
The universals of genome evolution can be accounted for by simple mathematical models
similar to those used in statistical physics, such as the birth-death-innovation model.
These models do not explicitly incorporate selection; therefore, the observed universal
regularities do not appear to be shaped by selection but rather are emergent properties of
gene ensembles. Although a complete physical theory of evolutionary biology is inconceivable,
the universals of genome evolution might qualify as "laws of evolutionary genomics“ in the same
sense "law" is understood in modern physics.

29. Information
Laws and generative models in evolutionary genomics
Koonin, PLOS Comp Biol 2011

30. A general physical principle behind all universals?
Shannon entropy: H= - pilogpi
Max(H) – most random, least unexpected distribution
MaxEnt Principle: the probability distribution of any variable in
a large ensemble of data/measurements tends to the distribution
with Max(H) within the applicable constraints
Information
S
Frank SA. The common patterns of nature
J Evol Biol. 2009; 22:1563-85
E. T. Jaynes
Karev, Koonin: Parabolic Replicator Dynamics
and the Principle of Minimum Tsallis Information
Gain. Biology Direct 2013
The results of this analysis show that the general
MaxEnt principle is the underlying law for
the evolution of a broad class of replicator systems
including not only exponential but also parabolic
and hyperbolic systems.

31. Postmodern reassessment of some central propositions of Darwin and the Modern Synthesis
Postmodern status
The material for evolution is provided, primarily, by
random, heritable variation.
Information
Proposition
Only partly true. The repertoire of relevant random changes greatly expanded to include duplication of genes, genome
regions, and entire genomes; loss of genes and, generally, genetic material; HGT including massive gene flux in cases of
endosymbiosis; invasion of mobile selfish elements and recruitment of sequences from them; and more. More
importantly, (quasi)directed (Lamarckian) variation is recognized as a major factor of evolution.
Fixation of (rare) beneficial changes by natural
selection is the main driving force of evolution.
Only partly true. Natural (positive) selection is important but is only one of several fundamental factors of evolution
and is not quantitatively dominant. Neutral processes combined with purifying selection dominate evolution, and direct
effects of environmental cues on the genome {(quasi)Lamarckian phenomena] are important as well.
The variations fixed by natural selection are
“infinitesimally small”. Evolution adheres to
gradualism.
False. Even single gene duplications and HGT of single genes are by no means “infinitesimally small” let alone deletion
or acquisition of larger regions, genome rearrangements, whole-genome duplication, and most dramatically,
endosymbiosis. Gradualism is not the principal regime of evolution.
Uniformitarianism: evolutionary
processes remained, largely, the same
throughout the evolution of life.
Only partly true. Present day evolutionary processes were important since the origin of
replication. However, major transitions in the evolution like the origin of eukaryotes could be
brought about by (effectively) unique events such as endosymbiosis, and the earliest stages of
evolution (pre-LUCA) partially relied on distinct processes not involved in subsequent, “normal”
evolution.

32. Information
“Amitochondrial” eukaryotes
“In the mid-1990s, a somewhat pedestrian view of eukaryotic origins, the 'archezoa hypothesis', held sway.
This maintained that a protoeukaryote (with nucleus) engulfed the mitochondrial ancestor. Supporting the theory
were 'archezoa', anaerobic eukaryotes with no mitochondria. Archezoa apparently populated the oldest branches
of the eukaryote tree, suggesting that eukaryotes began diversifying before mitochondria entered the picture.”
Poole, Penny, Nature 447, 913 (21 June 2007)

33. Information
There are no (known) true amitochondrial eukaryotes
Animal mitochondrion
Hydrogenosome from an
anaerobic fungus
Mitosomes from Giardia
Van der Giezen, Tovar. Degenerate mitochondria. EMBO Rep. 2005 Jun;6(6):525-30.
All “archezoa” possess:
-mitochondrial genes in nuclear genomes
-degenerate derivatives of mitochondria
They are not archezoa at all!

34. “Symbiotic” hypotheses
Information
“Archezoan”
hypotheses
????
Hypotheses on the origin of eukaryotes
Embley, Martin, Nature 2006

35. Information
Adaptation to
survive the intron
invasion
Origin of nucleus
and
spliceosome
Dispersal of
introns, population
bottleneck
Non-adaptive process –
Attack on the host genome
Unidirectional flow of genes
and introns from symbiont to
host – ratchet due to
propagation/lysis of symbiont
Invasion
2 prokaryotes: archaeon
and a-proteobacterium
Martin, Koonin, 2006, Introns and the origin of nucleus-cytosol compartmentalization. Nature 440: 41-5

36. Information
The proposed chain of causes and effects in eukaryogenesis –
the pivotal roles of mitochondrial endosymbiosis and intron invasion
Koonin, The origin of introns and their role in eukaryogenesis: a compromise solution to the
introns-early versus introns-late debate? Biol Direct. 2006 Aug 14;1:22

37. Postmodern reassessment of some central propositions of
Darwin and the Modern Synthesis
Postmodern status
Evolution by natural selection tends
to produce increasingly complex
adaptive features of organisms; hence
progress as a general trend in
evolution.
Information
Proposition
False. Genomic complexity probably evolved as a “genomic syndrome” caused by weak purifying
The entire evolution of life can be depicted as a single
“big tree”.
False. The discovery of the fundamental contributions of HGT and mobile genetic elements to genome evolution
invalidate the TOL concept in its original sense. However, trees remain essential templates to represent evolution of
individual genes and many phases of evolution in groups of relatively close organisms. The possibility of salvaging the
TOL as a central trend of evolution remains.
All extant cellular life forms descend from very few,
and probably, one ancestral form (LUCA).
True. Comparative genomics leaves no doubt of the common ancestry of cellular life. However, it also yields indications
that LUCA(S) might have been very different from modern cells.
selection in small population and not as an adaptation. There is no consistent trend towards
increasing complexity in evolution, and the notion of evolutionary progress is unwarranted.

38. Non-adaptive evolution of genomic complexity
Nothing makes sense in evolution except in light of population genetics
Lynch M. The frailty of adaptive hypotheses for the origins of organismal complexity. Proc Natl Acad Sci U S A. 2007
Lynch M, Conery JS.
The origins of genome complexity. Science. 2003 Nov 21;302(5649):1401-4.
Information
Complete genomic sequences from diverse phylogenetic lineages reveal notable increases in genome complexity from prokaryotes to
multicellular eukaryotes. The changes include gradual increases in gene number, resulting from the retention of duplicate genes, and
More abrupt increases in the abundance of spliceosomal introns and mobile genetic elements. We argue that many of these
modifications emerged passively in response to the long-term population-size reductions that accompanied increases in organism size.
According to this model, much of the restructuring of eukaryotic genomes was initiated by nonadaptive processes, and this in turn
provided novel substrates for the secondary evolution of phenotypic complexity by natural selection. The enormous long-term effective
population sizes of prokaryotes may impose a substantial barrier to the evolution of complex genomes and morphologies.

39. Information
There is no general trend toward
increasing complexity in evolution…
actually, the opposite might be true

40. Information
Reconstruction of archaeal genome evolution:
reduction prevails
Wolf YI, Makarova KS, Yutin N, Koonin EV. Updated clusters of orthologous genes for Archaea: a complex ancestor of the Archaea and
the byways of horizontal gene transfer. Biol Direct. 2012 Dec 14;7:46

41. Information
Maximum Likelihood (MCMC) reconstruction of intron gain/loss during eukaryote evolution from comparativegenomic analysis of 100 genomes (mean/median+ confidence intervals)
•Pronounced excess of loss over gain: mostly a story of decreasing complexity
•Intron-rich ancestors
•Human-like intron-density in Last Eukaryotic Common Ancestor (LECA)
•No intron-poor stage from LECA to mammals – no stage of intense purifying selection
Csuros, Rogozin Koonin, PLOS Comp Biol 2011

42. log
complexity
Information
Punctuated model of evolution: long phases of reduction punctuated by bursts
time
Wolf, Koonin, BioEssays 2013

43. Postmodern reassessment of some central propositions of
Darwin and the Modern Synthesis
Postmodern status
Evolution by natural selection tends to produce
increasingly complex adaptive features of organisms;
hence progress as a general trend in evolution.
Information
Proposition
False. Genomic complexity probably evolved as a “genomic syndrome” caused by weak purifying selection in small
population and not as an adaptation. There is no consistent trend towards increasing complexity in evolution, and the
notion of evolutionary progress is unwarranted.
The entire evolution of life can be
depicted as a single “big tree”.
False. The discovery of the fundamental contributions of HGT and mobile genetic elements to
All extant cellular life forms descend from very few,
and probably, one ancestral form (LUCA).
True. Comparative genomics leaves no doubt of the common ancestry of cellular life. However, it also yields indications
that LUCA(S) might have been very different from modern cells.
genome evolution invalidate the TOL concept in its original sense. However, trees remain essential
templates to represent evolution of individual genes and many phases of evolution in groups of
relatively close organisms. The possibility of salvaging the TOL as a central trend of evolution
remains.

44. A brief history of TOL
Information
Thinking of the history of life in terms of phylogenetic trees is as old as
scientific biology (if not older)
Charles Darwin (1859) Origin of Species [one and only
illustration]: "descent with modification"
Ernst Haeckel (1879)
The Evolution of Man

45. A brief history of TOL
Information
Advent of molecular phylogenetics – expectations of objectively
reconstructed complete Tree of Life
Carl R. Woese (1928-2012)
Woese et al. (1990) Towards a natural system of organisms: proposal for the domains
Archaea, Bacteria, and Eucarya. PNAS 87, 4576-4579 [Figure 1, modified]

46. “Forest of Life” to replace Tree of Life
Puigbò P, Wolf YI, Koonin EV.
Information
Search for a 'Tree of Life' in the thicket of
the phylogenetic forest. J Biol. 2009;8(6):59
0.5
0.4
0.3
1
0.2
2
0.1
3
4
0
-0.6
-0.4
-0.2
-0.1
-0.2
-0.3
-0.4
-0.5
0
0.2
0.4
0.6
0.8
5
6
7
NUTs

47. Horizontal gene flow dominates
evolution, at least in prokaryotes
d’ =0
d’ = (d-Dr) / (Ds-Dr)
d’=1
NUTs
Information
0.63 +/- 0.35
Dr
d’=1
Ds
Dr = 0.67
Ds > Dr
d’ = 1 – ((d-Ds) / (Dr-Ds)) d’=0
FOL
Ds
Ds < Dr
Dr
0.39 +/- 0.31
Dr = 0.67
TNT (Tree/Net Trend): scoring tree-like and netlike evolution quantitatively
0: Network(green) – Neutral (black) – 1:Tree (red)
Puigbo, Wolf, Koonin, Genome Biol Evol 2010

48. Postmodern reassessment of some central propositions of
Darwin and the Modern Synthesis
Postmodern status
Evolution by natural selection tends to produce
increasingly complex adaptive features of organisms;
hence progress as a general trend in evolution.
Information
Proposition
False. Genomic complexity probably evolved as a “genomic syndrome” caused by weak purifying selection in small
population and not as an adaptation. There is no consistent trend towards increasing complexity in evolution, and the
notion of evolutionary progress is unwarranted.
The entire evolution of life can be depicted as a single
“big tree”.
False. The discovery of the fundamental contributions of HGT and mobile genetic elements to genome evolution
invalidate the TOL concept in its original sense. However, trees remain essential templates to represent evolution of
individual genes and many phases of evolution in groups of relatively close organisms. The possibility of salvaging the
TOL as a central trend of evolution remains.
All extant cellular life forms descend
from very few, and probably, one
ancestral form (LUCA).
True. Comparative genomics leaves no doubt of the common ancestry of cellular life. However, it
also yields indications that LUCA(S) might have been very different from modern cells.

49. LUCA: undeniable but elusive
Information
~100 universally conserved protein and RNA genes =
primarily translation system components
Koonin EV. Comparative genomics, minimal gene-sets and the last universal common ancestor. Nat Rev Microbiol. 2003

50. Information
Mulkidjanian AY, Bychkov AY, Dibrova DV, Galperin MY, Koonin EV. Origin of first cells at terrestrial, anoxic
geothermal fields. Proc Natl Acad Sci U S A. 2012 Apr 3;109(14):E821-30

51. CRISPR spacer acquisition
direct
adaptation
resistance plasmid
acquisition
strong
selection
horizontal gene transfer
deterministic
intermediate
selection
stress-induced mutagenesis
draft
genome
streamlining
degradation
ratchet
transposition-induced
weak
Junk
shuffling
selection
accumulation/
gene duplication
complexification
gene loss
drift
random mutation
random
generation of variation
fixation of variation/mode of genome evolution
random
Information
determini
stic
From randomness to determinism: evolution spans the whole range

52. Information
The biosphere as the world of
viruses

53. Viruses are the dominant entities in the biosphere – physically and
genetically – as shown by viral metagenomics – virome studies
1 cm3 of seawater contains 106-109 virus particles
Information
Suttle, C.A. (2005) Nature 437:356
There are millions of diverse bacteriophage species
in the water, soil, and gut
Edwards and Rohwer (2005) Nat. Rev. Microbiol. 3:504
•Viruses are the most abundant biological entities in
the biosphere: there are 10-100 virus particles per cell
•The pangenomes of viruses and cellular organisms
have [at least] comparable complexities

54. Information
Some of the largest viruses host their own parasites
La Scola et al. The virophage as a unique parasite of the giant mimivirus.
Nature. 2008 Sep 4;455(7209):100-4

55. Information
Philippe et al. Pandoraviruses:
Amoeba Viruses with Genomes Up to
2.5 Mb Reaching That of Parasitic Eukaryotes
Science 19 July 2013: Vol. 341 no. 6143 pp. 281-286

56. Information
(At least) two independent origins of giant viruses:
Pandoraviruses appear to be highly derived Phycodnaviruses
Smaller,
simpler
common
ancestor(?)
Mimi
Yutin, Koonin.
Biol. Direct 2013
Pandora

57. Information
The ancient Virus World
•Viruses and virus-like genetic elements are not “just” pathogens: they are dominant
entities in the biosphere
•Emergence of virus-like parasites is inevitable in any replicating system
•In the pre-cellular epoch, the genetic elements that later became viral and cellular
genomes comprised a single pool in which they mixed, matched, and evolved
new, increasingly complex gene ensembles
•Different replication strategies including RNA replication, reverse transcription,
and DNA replication evolved already in the primordial genetic pool
•With the emergence of prokaryotic cells, a distinct pool of viral genes formed that
retained its identity ever since as evidenced by the extant distribution of
viral hallmark genes: “virus world” or the virosphere
•The emergence of the eukaryotic cell was a second melting pot of virus evolution, from
which viruses of eukaryotes originated via recombination of genes from prokaryote
viruses, retroelements, and the evolving eukaryotic host
•Viruses make essential contributions to the evolution of the genomes of cellular
life forms, in particular, as vehicles of HGT: GTAs, transducing phages
Koonin EV, Senkevich TG, Dolja VV. The ancient Virus World and evolution of cells. Biol Direct. 2006

58. viroids
Information
dsDNA viruses
ssDNA viruses
Retroviruses/
elements
dsRNA viruses
(+)RNA viruses
Koonin, Logic of Chance 2011
Bacteria
KEukaryota
Archaea
(-)RNA viruses
Virus Empire
Cellular Empire

59. Virus
World
constructive neutral
evolution of
complexity
Selfish
gene
HGT
phylogeno
mics
Neutral theory
Quantitative
laws and
physical
principles
of evolution
Population genetics
Quantitative theory of selection
and drift
Darwinian theory
of natural
selection
evolution
of
evolvabilit
y
Information
Neo-Lamarckian
evolution models
Lamarckian
L'influence des
circonstances
Modified from: Koonin EV, Wolf YI. Evolution of microbes and viruses: a paradigm shift in evolutionary biology? Front Cell Infect Microbiol. 2012;2:119

60. Information
FT Press; 1 edition (September 10, 2011)
Marine Corps marathon 2011,
Washington, DC

61. Information
Acknowledgments
Bill Martin
Valerian Dolja
Didier Raoult