Transcript The Major Transitions in Evolution

The emergence and importance of
compartment models
Eörs Szathmáry
Collegium Budapest AND Eötvös University
Early origin-of-life models were
compartmental
• Oparin and coacervates
• Fox and microspheres
• The idea of naked replicators became
fashionable after the discovery of DNA
structure
• Even though DNA never self-replicates!
• Standard forms of the RNA world today
usually assume naked replicators
A lot of confusion arises when units
of evolution and units of life are
taken to be identical
• The problem of the virus
• Gánti’s analogy: the virus is the living cells
as a self-replicating programme is to the
computer
• Neither the virus nor the programme do not
do anything alone
Units of evolution (JMS)
1. multiplication
2. heredity
3. variation
hereditary traits affecting
survival and/or
reproduction
The simplest cells today are bacterial
• THUS we want to explain the origin of some
primitive bacterium-like cell
• Even present-day bacteria are far too complex
• The main problem is the genetic code
Units of evolution and units of life
viruses
memes
Units of evolution
bacteria,
protists,
etc.
mules
sterilized
workers
nondividing
cells
Units of life
(Szathmáry, 2001)
We need a modern picture of
compartmentation
• Molecular biology
• Cell biology
• Biochemistry
Gánti’s chemoton model (1974)
metabolism
template
copying
membrane
growth
ALL THREE SUBSYSTEMS ARE AUTOCATALYTIC
The fission of the chemoton
•
•
•
•
Membrane surface doubled
Quantity of internal materials doubled
Assume spherical shape
Concentration cannot be kept with a
growing sphere: volume increases with the
cubic of the radius
• Volume of sphere with a surface are
doubled would be more than doubled
Compartments are important,
because
• They prohibit constituents diffusing away
• Can increase local concentration
• Create a special microenvironment, e.g. by
keeping many molecules out
• For example, imagine when a poison cannot
enter the compartment
• The problem of the origin of life is
essentially that of metabolite channelling!
• Last but not least: a higher-level unit of
evolution
Mineral surfaces are a poor man’s
form of compartmentation (?)
• A passive form of localisation (limited diffusion in
2D)
• Thermodynamic effect (when leaving group also
leaves the surface)
• Kinetic effects: surface catalysis (cf. enzymes)
• How general and diverse are these effects?
• Good for polymerisation, not good for metabolism
(Orgel)
• What about catalysis by the inner surface of the
bilayer (composomes)?
Population dynamics on surfaces
• Reaction-diffusion on the surface (following
Hogeweg and Boerlijst, 1991)
• One tends to interact with one’s neighbours
• This is important, because lesson from
theoretical ecology indicates that such
conditions promote coexistence of
competitors
• Important effect on the dynamics of the
primordial genome (cf. Eigen’s paradox)
Surface metabolism catalysed by
replicators (Czárán & Szathmáry, 2000)
I1-I3: metabolic
replicators
(template and
enzyme)
I1
P
M
I3
I2
M: metabolism (not
detailed)
P: parasite (only
template)
Elements of the model
i-2
i-1
i
j -2
j-1
j
j+1
j+2
S
X
i+1
i+2
• A cellular automaton model
simulating replication and dispersal
in 2D
• ALL genes must be present in a
limited METABOLIC
neighbourhood for replication to
occur
• Replication needs a template next
door
• Replication probability proportional
to rate constant (allowing for
replication)
• Diffusion
Robust conclusions
• Protected polymorphism of competitive replicators
(cost of commonness and advantage of rarity)
• This does NOT depend on mesoscopic structures
(such as spirals, etc.)
• Parasites cannot drive the system to extinction
• Unless the neighbourhood is too large (approaches
a well-stirred system)
• Parasites can evolve into metabolic replicators
• System survives perturbation (e.g. when death
rates are different in adjacent cells), exactly
because no mesocopic structure is needed.
An interesting twist
• This system survives with arbitrary
diffusion rates
• But metabolic neighbourhood size must
remain small
• Why does excessive dispersal not ruin the
system?
• Because it convergences to a trait-group
model!
The trait group model (Wilson, 1980)
Mixed global pool
Random dispersal
Harvest
Mixed global pool
Applied to early coexistence: Szathmáry (1992)
Why does the trait group work?
• It works only for cases when the “red hair
theorem” applies
• People with red hair overestimate the
frequency of people with red hair,
essentially because they know this about
themselves
• “average subjective frequency”
• In short, molecules must be able to scratch
their own back!
Nature 420, 360-363 (2002).
• 2D Reaction-diffusion system: molecules
are bound to the surface, and can only
interact with their neighbours
• Replicating molecules have template and
replicase functions (auto- and
heterocatalytic effects)
Maximum as a function of
molecule length
• Target and
replicase
efficiency
• Copying fidelity
• Trade-off among
all three traits:
worst case
Evolution of replicases on the
rocks
• All functions coevolve
and improve despite
the tradeoffs
• Increased diffusion
destroys the system
• Reciprocal altruism on
the rocks
Evolving population
Error rate
Replicase
activity
The stochastic corrector model
for compartmentalized genomes
Szathmáry, E. &
Demeter L. (1987)
Group selection of early
replicators and the
origin of life. J. theor
Biol. 128, 463-486.
Grey, D., Hutson, V. &
Szathmáry, E. (1995) A
re-examination of the
stochastic corrector
model. Proc. R. Soc.
Lond. B 262, 29-35.
The stochastic corrector model
(1986, ’87, ’95, 2002)
metabolic
gene
replicas
e
membrane
Dynamics of the SC model
• Independently reassorting genes (ribozymes
in compartments)
• Selection for optimal gene composition
between compartments
• Competition among genes within the same
compartment
• Stochasticity in replication and fission
generates variation on which natural
selection acts
• A stationary compartment population
emerges
The paradox of gene dosage
• Koch, A.L. (1980)
• High dosage: safeguard against stochastic
loss
• BUT dilution of beneficial mutations
• If genes are ribozymes, there is a
concentration effect on catalysis
Group selection of early
replicators: sitting in the same boat
• Many more compartments than templates
within any compartment
• No migration (fusion) between
compartments
• Each compartment has only one parent
• Group selection is very efficient
• Selection for replication synchrony
The mathematical model
• Inside compartments, there are numbers rather
than concentrations
• Stochastic kinetics was applied:
• Master equations instead of rate equations: P’(n, t)
= ……. Probabilities
• Coupling of two timescales: replicator dynamics
and compartment fission
• A quasipecies at the compartment level appears
• Characterized by gene composition rather than
sequence
Further considerations
• Selection for replication synchrony by
clonal selection on compartments
• Start with a small number of genes 
synchronise replication rates  increase
gene number
• Selection for chromosomes: only one child
• Genes are certain to find their partners in
the same compartment (Maynard Smith &
Szathmáry, 1993)
A surprising recent result: increase
of the error threshold by intragenic,
intracompartment recombination
• Santos, M., Szathmáry, E. & Zintzaras, E.
(2004) J. Mol. Evol. In press.
• Typically, the wild type copies are lost by
mutation pressure
• They can be restored by recombination
• A within-compartment analogue to Muller’s
ratchet
A forthcoming publication
• E. Szathmáry & M. Santos (2005) Models
of compartments. In Walde, P. (ed.) Topics
in Current Chemistry, in prep.