Thermodynamics of evolution

Ilya Prigogine, Gregoire Nicolis, and Agnes Babloyantz

Citation: Physics Today 25, 11, 23 (1972); doi: 10.1063/1.3071090

View online: https://doi.org/10.1063/1.3071090
View Table of Contents: https://physicstoday.scitation.org/toc/pto/25/11
Published by the American Institute of Physics

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Thermodynamics of evolution
The functional order maintained within living systems
seems to defy the Second Law; nonequilibrium thermodynamics
describes how such systems come to terms with entropy.
lya Prigogine, Gregoire Nicolis and Agnes Babloyantz
The physicochemical basis of biological
order is a puzzling problem that has oc-
cupied whole generations of biologists
and physicists and has given rise, in the
it, to passionate discussions. Bio-
logical systems are highly complex and
ordered objects. It is generally accepted
that the present order reflects structures
acquired during a long evolution. More-
over, the maintenance of order in actual
living systems requires a great number
of metabolic and synthetic reactions as
well as the existence of complex mech-
anisms controlling the rate and the
timing of the various processes. All
these features bring the scientist a
wealth of new problems. In the first
place one has systems that have evolved
spontaneously to extremely organized
and complex forms. On the other hand
metabolism, synthesis and regulation
'mply a highly heterogeneous distribu-
tion of matter inside the cell through
Aemical reactions and active transport.
"ya Prigogine is professor of physical chem-
'% and theoretical physics at the Uni-
site Libre de Bruxelles and is director of
Center for Statistical Mechanics and
Thermodynamics at the University of Texas,
Austin. Gregoire Nicolis and Agnes Bab-
'"yantz are both at the Universite Libre de
'Welles: Nicolis is charge de cours and
yantz is chef de travaux.
Coherent behavior is really the char- the free energy become comparable.
acteristic feature of biological systems Thus the populations of the different
(see the box on page 24). energy levels tend to become equal.
In contrast to this is the familiar idea
The point is that in a nonisolated system
that the evolution of a physicochemical there exists a possibility for formation
system leads to an equilibrium state of of ordered, low-entropy structures at
maximum disorder. In an isolated sys- sufficiently low temperatures. This
tem, which cannot exchange energy and ordering principle is responsible for the
matter with the surroundings, this ten- appearance of ordered structures such
dency is expressed in terms of a functionas crystals as well as for the phenomena
of the macroscopic state of the system: of phase transitions.
the entropy. It amounts to saying that Unfortunately this principle cannot
entropy S increases monotonically until explain the formation of biological struc-
it becomes a maximum. This cele- tures. The probability that at ordinary
brated second law of thermodynamics temperatures a macroscopic number of
implies that in an isolated system the molecules is assembled to give rise to
formation of ordered structures is ruled the highly ordered structures and to the
out. coordinated functions characterizing liv-
Consider now a system in contact ing organisms is vanishingly small. The
with an energy reservoir at temperature idea of spontaneous genesis of life in its
T. Its state is now described by a new present form is therefore highly improb-
function, the free energy F defined by able, even on the scale of the billions of
years during which prebiotic evolution
F=E-TS (1) occurred.
where E is the internal energy. At The conclusion to be drawn from this
equilibrium, F is at a minimum. The analysis is that the apparent contradic-
probability P that the system is at a tion between biological order and the
state of energy En is then given by laws of physics—in particular the
second law of thermodynamics—cannot
exp(-En/kT) (2)
be resolved as long as we try to under-
At low temperatures, equations 1 and 2 stand living systems by the methods of
imply that only the low states (at small
En) will be populated. As T increases, This is the first part of a two-part article;
the energy and entropy contributions to the second half is scheduled for next month.
PHYSICS TODAY/NOVEMBER 1972 23
the familiar equilibrium statistical me-
chanics and equally familar thermody-
Nonequilibrium open systems
perature gradient. Assume that ini- til
tially the system has uniform composi- Coherent behavior,
tion. The separation of matter that is dissipation and life
achieved then corresponds to a decrease
of entropy from the initial value. •0

From the simplest bacterial cell to The existence of nonequilibrium con-

man, living organisms are maintained
and reproduced thanks to a continuous
exchange of energy and matter with the
surroundings. (Viruses present an ex-
ception to this rule. On the other hand
it is well known that they cannot multi-
ply unless they infect a cell; that is, until
they become open systems.) This trivial
statement has several less obvious and
even far-reaching consequences. The
straints is far from exceptional in bio-
logical systems. The biosphere as a
whole is subject to a solar energy gra-
dient. At the cellular level, products
of metabolism are either rejected to the
environment or diffuse within the cell
to fulfill other functions. As a rule,
then, a cell or a biochemical reaction
chain is subject to the gradients in
chemical potentials of the various react-
Although it is customary to associate
biological order with the formation of
low-entropy ordered structures such as
macromolecules, membranes and cells
as a whole, this is only part of the prob- •A
lem. Equally important is functional m
order, which in actual living cells is iflW
ensured by a great number of coupled
biochemical pathways. Biologists of •iff
development have always been puzzled itri
that these metabolic processes are r-'Jll

thermodynamic theory of open systems, ing constituents. associated with a great amount of en- mil'
systems exchanging both energy and ergy dissipation. As an example [A. I. •itt
The arguments we have advanced Zotin, R. S. Zotina, J. Theor. Biol. 17,
matter with the environment, has long here cannot, of course, suffice for solving -ssys
57, (1967)] the rate of heat production
been developed by Theophile DeDonder the problem of biological order. One in chicken eggs, which, roughly speak-
and the Brussels school (for a historical would like not only to show that the sec- ing, should furnish a measure of the en-
account, see reference 1). Ludwig von ond law is satisfied as a whole (diS 5; 0) tropy production, is about 6 kcal/day/gm
Bertalanffy
3
(1940)2 and Erwin Schrod- but also to indicate how the state of low at the fourth day of development. At
inger have insisted on the importance entropy and high coherence is main- the 16th day, it drops to about 1 kcal/
of this feature for biological systems. tained. The remaining part of our dis- day/gm. These rather high figures raise
One of us has formulated1 an extended cussion will be devoted to this question, the question of how living systems have
version of the second law that applies and we shall discuss in some detail the acquired the ability to dissipate in- : mil
both to isolated and to open systems. tensely. One of our main points here item
The main point is that the Clausius- approach we have developed during the shall be that an increase in dissipation swiff
Carnot inequality governing the varia- last few years. is possible for nonlinear systems driven
tion of entropy during a time interval dt far from equilibrium. Such systems
Dissipative structures may be subject to a succession of un-
takes the form stable transitions that lead to spatial
^fraction
Our qualitative arguments lead us to
inquire about the feasibility of extend- order and to increasing entropy produc-
dS = deS + diS tion.
ing the concept of order to nonequilib-
djS>0 (3) rium situations, to systems in which the
it*
where deS is the flow of entropy due to appearance of ordered structures, in
exchanges with the surroundings and thermodynamic equilibrium, would be
djS the entropy production due to irre- very unlikely. One of the main conclu-
versible processes inside the system such sions of our theory will be that there
as diffusion, chemical reactions, heat exists a class of systems showing two In a quite different domain, a spectac- ability,
conduction, and so on. For an isolated kinds of behavior: a tendency to the ular example of emergence of order far
system deS is zero, and equation 3 re- state of maximum disorder for one type from equilibrium has been worked out
duces to of situation and coherent behavior for a recently by Hermann Haken.5 He a spo
second type. The destruction of order shows that the generation of coherent
dS = diS > 0 (4)
always prevails in the neighborhood of light by a laser may be interpreted as a k dei
Thus open systems differ from isolated thermodynamic equilibrium. In con- nonequilibrium phase transition. Be- itdi
systems in the presence offlowterms in trast, creation of order may occur far low instability is the incoherent regime;
the entropy variation, terms related to from equilibrium and with specific non- beyond the transition threshold, cor-
exchanges of energy and of matter with linear kinetic laws, beyond the domain responding to a critical value of the ra-
the outside world. Although diS is of stability of the states that have the diation field, the system switches spon- w mi
never negative, the flux term deS has no usual thermodynamic behavior. Tradi- taneously to the coherent state.
definite sign. As a result, during evolu- tionally, thermodynamics has dealt with We have investigated systematically
tion a system may reach a state where the first type of behavior, but an exten- the behavior of nonlinear chemical net-
entropy is smaller than at the start sion of irreversible thermodynamics works of biological interest.4-6 At first
(see the box on page 25). Moreover, that permits treating the other aspects one would expect that those systems
this state, which from the standpoint of as well as this one has been developed that, contrary to the two previous ex- J print
equation 2 would be highly improbable, recently.* amples, are purely dissipative would ''teas
can be maintained indefinitely provided The best known examples of this du- always show a tendency to a disordered
the system can reach a steady state such ality in behavior are instabilities in regime. The surprising result was that
that dS = 0 or fluid dynamics, such as the onset of in fact they share most of the properties
deS = -dj.S < 0 (5) thermal convection in a fluid layer of hydrodynamic instabilities with the
heated from below. For a critical value additional important feature that the '•'main
Thus, in principle at least, if we supply of the external constraint (temperature variety of the regimes beyond insta- «lroi :

a system with a sufficient amount of gradient), that is, beyond a critical bility is much greater in chemical ki- -level
negative entropy flow, we can maintain distance from equilibrium, an insta- netics.
the system in an ordered state. Equa- bility arises that causes the spontaneous
tion 5 also implies that this supply must emergence of convection patterns. Be- This is not really surprising when we
occur under nonequilibrium conditions, low the instability threshold, the energy realize that in chemical kinetics non-
otherwise d[S (and, by equation 5, also of the system is distributed in the ran- linearity may arise in a practically un-
deS) would vanish identically. A sim- dom thermal motion of the molecules. limited number of ways through auto-
ple illustration1 of this nonequilibrium But beyond instability it appears partly catalysis, cross-catalysis, activation,
order is seen in a thermal diffusion ex- as the energy of macroscopic convec- inhibition, and so on. In contrast, the
periment in a system subject to a tem- tion patterns. stokes-Navier equations of fluid dy-
namics assume a universal form. Be-
24 PHYSICS TODAY/NOVEMBER 1972
 tems, so we shall illustrate the points we
wish to make with particular models.
The evolutionary feedback The development of irreversible ther-
modynamics of open systems by the
What is the thermodynamic meaning of prebiological evolution? Darwin's princi- Brussels school had, by the 1950's, led
ple of "survival of the fittest" through natural selection can only apply once pre- to the investigation of nonlinear pro-
biological evolution has led to the formation of some primitive living beings. A cesses (see reference 4 for a survey of the
new evolutionary principle, proposed recently by Manfred Eigen, would replace
Darwin's idea in the context of prebiotic evolution. It amounts to optimizing a
subject). Thus, we had already come
quantity measuring the faithfulness, or quality, of the macromolecules in reproduc- to recognize the important role of auto-
ing themselves via template action. We here propose an alternative description catalytic processes in the understanding
of prebiological evolution. The main idea is the possibility that a prebiological of biological order.4-7 It was only then
system may evolve through a whole succession of transitions leading to a hier- that we noticed a remarkable paper by
archy of more and more complex and organized states. Such transitions can only A. M. Turing (1952)8 who had actually
arise in nonlinear systems that are maintained far from equilibrium; that is, beyond constructed a chemical model showing
a certain critical threshold the steady-state regime becomes unstable and the instabilities. His work had previously
system evolves to a new configuration. As a result, if the system is to be able to escaped our attention because it dealt
evolve through successive instabilities, a mechanism must be developed whereby with the more specific subject of forma-
each new transition favors further evolution by increasing the noniinearity and the
distance from equilibrium. One obvious mechanism is that each transition en-
tion of morphogenetic patterns. The
ables the system to increase the entropy production. We may visualize this evolu- work we have undertaken since then
tionary feedback: has demonstrated the relation of this
type of behavior to thermodynamics as
Threshold instability through fluctuations well as its wide applicability to biology.
We shall briefly summarize here the
results obtained from the model chemi-
increased dissipation
cal reaction chain (see references 4 and
It is important to insist on the complementarity between this increasing dissipation 6 for details)
behavior, which we believe is essential for prebiological evolution, and the com-
monly observed tendency of physicochemicai systems near equilibrium toward a
state of minimum dissipation or entropy production, which we shall discuss later. B+X^Y+D (7)
Existing thermal data appear to indicate that this second type of behavior holds for
living systems after some initial period, which in higher organisms extends only
over a fraction of the embryonic life. One is tempted to argue that only after syn-
thesis of the key substances necessary fpr its survival (which implies an increase
in dissipation) does an organism tend to adjust its entropy production to a low Note the autocatalytic third reaction;
value compatible with the external constraints. At this point, contact can probably this reaction step introduces the non-
be made with Darwin's idea of the "survival of the fittest," because a low rate of linearity that will be largely responsible
entropy production is likely to give to an organism a selective advantage. for the unusual behavior of the system:
(a) At or near thermodynamic equi-
librium, the system of equation 7 has a
unique steady-state solution that is al-
ond instability, which again arises the flow of chemicals from the outside ways stable with respect to arbitrary
when a critical distance from equilib- world, and exchange can occur between perturbations.
num is reached, the reaction systems these chemicals and the reacting species (b) Suppose that the system is driven
may become spontaneously inhomoge- inside the reaction volume. For simpli- far from equilibrium. In the extreme
neous and present an ordered distribu- city we assume an isothermal system in case that the concentrations of D and E
ion of the chemical constituents in mechanical equilibrium. Moreover, are maintained vanishingly small in the
3. Under different conditions the if the concentration gradients are not system, the distance from equilibrium
oncentrations of the chemicals may very high, diffusion can be approxi- becomes very large. Still, for time-inde-
stow sustained oscillations. Finally, mated by Fick's law, which states that pendent boundary conditions, we can
other systems may exhibit a multipli- the flow of matter due to diffusion can define a steady state corresponding to
tity of steady states combined with be approximated by DVC where C is the continuation of the equilibrium-like
hysteresis. (We will discuss examples concentration and D is a diffusion coef- behavior. The branch of states defined
ater.) ficient. Finally, we take a diagonal dif- in this fashion will be referred to as the
In all these phenomena, a new order- fusion-coefficient matrix. Under these "thermodynamic branch." This time
mechanism, not reducible to the conditions the instantaneous state of the however, the study of the conservation
tquilibrium principle (equation 2), ap- system is described by the composition equations (equation 6) reveals that,
>Mra. For reasons to be explained variables \xt\ where i ranges from 1 to n, owing to the noniinearity and to the
to, we shall refer to this principle as which are, say, the average mole func- nonequilibrium constraints, states on
tions or the average partial densities of this branch are not necessarily stable.
tier through fluctuations. The struc- Depending on the type of perturbations
the chemicals. The time evolution of
ues are created by the continuous flow these variables is given by the well to which the system is subject and on
°f energy and matter from the outside known conservation-of-mass equations the values of the parameters—such as
lo
rid; their maintenance requires a cri- A (concentration of A) and B, the
iral distance from equilibrium, that is, dXi/dt=DtV2Xi+ VA\xj\) (6) diffusion coefficients DA, DB, D\ and
'minimum level of dissipation. For all DY—different situations will be real-
tae reasons we have called them dis- Here the source terms Vi describe the ef- lized. This is illustrated by the non-
Wive structures.* fect of chemical reactions. We assume equilibrium phase diagram of figure 1.
that the rates of the various chemical For simplicity, the parameters A,
ipative systems transformations are given by the law of DA, D\ are held constant and DB is
a first discussion of model systems mass action, so that V; (\XJ\) will be a taken so large that the distribution of
confirm the existence of dissipative nonlinear (usually algebraic) function B remains uniform.
'tortures in chemical kinetics, it will
convenient to adopt a macroscopic Equations 6 form a nonlinear system (c) In domain II of the diagram, the
Wiption. Consider a reacting mix- of partial differential equations. No thermodynamic branch becomes unsta-
"e of n species. The system is open to general theory is available for these sys- ble with respect to perturbations in the

PHYSICS TODAY/NOVEMBER 1972 25


chemical composition. Beyond the
transition threshold initial deviations
from the steady state are amplified and
finally drive the system to a new steady
state corresponding to a regular spatial
distribution of X and Y. This state is
represented in figure 2.
The result is a low-entropy spatial
dissipative structure arising beyond a
nonequilibrium transition that spon-
taneously breaks the initial symmetry of
the system. Its behavior is quite dif-
ferent from that of systems on the ther-
modynamic branch. In addition to the
coherent character exhibited by such
states, one can show that the final con-
figuration depends to some extent on
the type of initial perturbation. This
primitive memory effect makes these
structures capable of storing informa-
tion accumulated in a remote past.
(d) For DB » DA » DY ^ D x , the ther-
modynamic branch may again become
unstable. But this time the system is
driven beyond instability to a new state
that not only depends on space but also
is periodic in time. In the course of one
period, wavefronts of composition ap-
pear and propagate in the reaction vol-
ume, first outwards and then, after re-
flecting on the boundaries, to the in-
terior. Moreover, at each point in space
the system performs quasidiscontinuous
concentration oscillations in time. This
space-time dissipative structure there-
fore provides a primitive mechanism for
propagating information over macro-
scopic distance, in the form of chemical
signals.
(e) For DA finite, both structures dis-
cussed in c and d are localized inside the
reaction volume. Their boundaries, as
well as the periods and other character-
istics, are determined from the values
of the parameters A, B, D x and so
on, independently of the initial condi-
tions. For DA, DB ~~* °° the structures
100
O
o dxP/dt < 0
D / ^ X I O (ARBITRARY DIFFUSION UNITS)
Stability properties of the autocataiytic system described on page 25 (system 7) The non-
equilibrium steady-state solutions are shown as a function of the amount of substance B
present and of the diffusion constant for substance Y. In domain I the steady-state is stable
with respect to fluctuations in mixture composition. Fluctuations increase monotonically
in domain II (see figure 2) and, in domain
The steady-state, then, is unstable in both these regions.
26 PHYSICS TODAY/NOVEMBER 1972
tend to occupy the whole reaction vol-
ume. Finally, when D x , -DY are very
large (with respect to the chemical
rates) the space dependencies disappear
in case d, and the result is a system that,
beyond instability, oscillates with the
same phase everywhere. The ampli-
tude and period of the oscillations are
determined by the system itself. More-
over, the periodic motion is stable in the
sense that all perturbations introducing
an initial deviation from this state are
damped. This type of solution is well
known in mathematics and in analytical
mechanics as a "limit cycle." Note
that the existence of localized states and
of wavelike solutions shown in c and d
raises a number of fascinating mathe-
matical problems related to the exis-
tence and stability of periodic solutions
for nonlinear parabolic partial differ-
ential systems.
Obviously, the occurrence of insta-
bilities far from equilibrium is not a uni-
versal phenomenon in chemical kinetics.
Coherent behavior requires some very
particular conditions on the reaction
mechanism, whereas the equilibrium
order principle is always valid (for short-
range forces). But this variety of be-
havior in chemistry is welcome, if we
want to account for the variety of situa-
tions observed in systems driven far
from equilibrium.
The mechanism of instabilities
We have insisted on the diversity of
situations that may arise in nonlinear
systems far from equilibrium. Now we
shall see that despite this diversity,
there is a general thermodynamic theory
underlying the mechanism by which a
system is driven to the new regime be-
yond the instability of the thermody-
namic branch.
Within the framework of our macro-
scopic description, we would like to re-
they are present as amplified oscillations.
Figure 1
late instabilities to the thermodynamic^
properties of the systems, such as en-:*1
tropy, entropy production, and so on;*
Consider again the decomposition of d&
given by equation 3. Explicit calcula-
tion of djS/dt is possible for systems
that can be described macroscopicalljs^
in terms of a limited number of locals*
variables. (From the microscopic pointfe1
of view, this condition implies that, lo-.*1
cally, the momentum distribution func-jpB-
tion of the system should not deviate:;!
appreciably from the Maxwellian form.)*
Note that this restriction is compatible! 12
with large deviations from chemicaljts
equilibrium. The result is
p=diS/dt = ZpJt>x»-° <8>JLI
w
where the JP are the rates of irreversible^
processes (chemical reaction velocities,,;^;
diffusion, heat flow, and so on), X,f are:;ia
the corresponding forces (such as differ-jjjl
ences in chemical potentials and tem-i fa
perature gradients). Remarkably, in.s[t]
this bilinear form the entropy produc-6(a
tion is expressed entirely in terms oi.sgjt,
macroscopic quantities of direct physi-j^,
cal interest such as the flows and the
forces.
Near equilibrium, equation 8 becomes^
quadratic in the Xp's. One of us1-4 ^
has shown that in this limit, and pro-.'j^
vided the system is subject to time-inde-
pendent boundary conditions,
dP/dt < 0 (9)*ili
This implies a minimum entropy pro-"'
duction at the steady state and the sta-iii?
bility of this state; the proof is based on
a classical analytic result known as
Lyapounov's theorem, which demon-;'™
strates stability once one can construct"*!11
a definite function (the Lyapounov func-
tion) whose time variation is also defi:"in
nite with opposite sign. This result is^,
in agreement with the analysis of model
systems discussed in the previous sec-1"'1'''
tion.
Inequality 9 breaks down for states';"1*
far from thermodynamic equilibrium.**
but we can still obtain a general inequal- ^
ity in this domain if we decompose rifJtB>t
into two terms, according to equation 8: Pn
= djP/dt + dxP/dt (10;
We have introduced explicitly the varia- „
tion in P due to a variation of the flows
and a variation of the forces, and cartesk
now show that in the whole domair line
where equation 8 is valid, and providec-liled
the system is subject to time-indepen:~ttib
dent boundary conditions, ftnilil
(llf*
This in the extension of the minimum-ijfj
entropy-production property to the nonHs^
linear domain of irreversible processes^,
However, in contrast to inequality 9%st
inequality 11 does not imply the stabilt, ^
ity of the steady state, primarily be fek
cause dxP is not the differential of ^
state function in the general case. In \\\
Hie
tead, we use inequality 11 to derive a
tability condition for such states, and
we find that stability will be ensured
whenever
>0 (12)
Here iJc and 8XP are the excess flows
forces due to the deviation of the
state of the system from the reference
regime (the steady state). In deriving
this inequality it has been assumed that
the system remains in mechanical
equilibrium.
Relation 12 provides a universal ther-
modynamic stability criterion for non-
equilibrium states. One can show that
the inequality is always satisfied in the
neighborhood of equilibrium as well as
in the absence of a feedback process of
the autocatalytic type. An alternative
interpretation of the stability criterion
in terms of a Lyapounov function is also
possible.4 Consider the entropy S as a
function of the nonequilibrium state,
with So its value in the reference state
whose stability is studied. We expand
Saround So:
S = SQ + 5S + 52S/2 + ...
Now in the domain where relation 8 is
valid, one shows* that <52S, which is a
quadratic form, obeys the inequality
2 would be damped below the transition
(l/2)<5 S<0 (13a)
On the other hand, in mechanical equi-
librium, we show that
d(l/2)&2S/dt =£,U5Xp (13b)
Thus, according to Lyapounov's the-
orem, the reference state will be stable
provided inequality 12 is satisfied; that
is, provided the excess entropy (5 2 S)/2
increases in time.
Order through fluctuations
So far stability has been related to de-
viations (arising, for example, from ex-
ternal perturbations) from the reference
state. A much deeper insight is pro-
vided by the result of recent investiga-
tions9 that in the whole domain of valid-
ity of relation 8, the excess entropy 52S
also determines the probability of a
small fluctuation around the reference
state:
P<* exp(5 2 S/2fe) (14)
This expression provides a generaliza-
tion to nonequilibrium situations of
'he celebrated Einstein formula describ-
ing the distribution of small fluctuations
around equilibrium. Now fluctuations
-the spontaneous deviations from some
average regime—are a universal phe-
nomenon of molecular origin and are al-
^ys present in a system with many
degrees of freedom. Thus, a system in
an average state close to but below the
''ansition threshold will always have
a nonvanishing probability of reaching
"le unstable region through fluctua-
tions. When this happens, certain
'ypes of fluctuations will be amplified
SPACE (ARBITRARY UNITS)
Localized steady-state dissipative structure emerges in domain II of the stability diagram.
This new steady state (see figure 1) is found numerically and cannot be obtained in a con-
tinuous extrapolation of the equilibrium behavior. In domain III, concentration waves may
propagate. Numerical values of the pparameters here and in figure 1 are Dx = 1.05 X
3 3
1 0 " 3 , D Y = 5.25 X 1 0 " 3 , D A = 197 X 10~ 3 , D B and all forward kinetic constants
are equal to unity. In this domain B = 26.0, (A) = (X) = 14.0, (Y) = 18.6. Figure 2
and they will subsequently drive the sys- This state will then be the starting point
tem to the new regime. In the thermal for further evolution.
instability problem mentioned pre-
viously, these fluctuations would gener- Some biological examples
ate small convection currents that Dissipative structures have been pro-
duced in the laboratory in an organic
point but give rise to a macroscopic cur- oxidation reaction.10 More recently,
rent beyond the instability. D. Thomas11 demonstrated that an
In all these situations a new order inhomogeneous pH distribution may
principle appears that corresponds es- arise spontaneously inside an artificial
sentially to an amplification of fluc- membrane wherein two different types
tuations and to their ultimate stabiliza- of enzymes have been reticulated in a
tion by the flow of matter and energy spatially homogeneous fashion. How-
from the surroundings. We may call ever, the problem that concerns us here
this principle "order through fluctua- is primarily the usefulness of the theory
tions." outlined in the previous sections in the
An additional important element understanding of biological phenomena.
should be pointed out: The formation It will be convenient to discuss separ-
of a fluctuation of a given type is funda- ately two types of problems:
mentally a stochastic process. The re- • Is it possible to understand the func-
sponse of the system to this fluctuation tional order observed in actual living
is a deterministic process obeying the systems? This question refers to the
macroscopic laws as long as the system physicochemical basis of maintenance
can damp the fluctuation. Now in the of life.
domain of formation of a new structure, • How did the structures observed in
fluctuations are amplified and drive the living beings (nucleic acids, proteins,
average values to the new regime. cells as a whole) arise from an inert pre-
Thus, in this region the macroscopic de- biotic mixture of simple molecules?
scription in terms of averages breaks This is the problem of prebiotic evolu-
down and the evolution acquires an es- tion or of the origin of life.
sentially statistical character. We shall discuss the first point
We have then a picture of a system briefly, postponing for a while the prob-
evolving through instabilities: In the lem of evolution. A number of typical
neighborhood of a stable regime, evolu- phenomena can be analyzed in terms of
tion is essentially deterministic in the the theory outlined in the previous sec-
sense that the small fluctuations arising tion: regulatory processes, excitable
continuously are damped. But near the systems and cell aggregation.
transition threshold the evolution be- The existence of elaborate control
comes a stochastic process in the sense mechanisms to ensure that the various
that the final state will depend on the chemical reactions in living cells happen
probability of creating a fluctuation of a at the proper rate and at the right time
given type. Of course, once this prob- is well known. The first type of control
ability is appreciable, the system will mechanism ensures that there is no ex-
eventually reach a unique (apart from cessive synthesis, or lack of small me-
small fluctuations) stable state, once tabolites, for instance, of energy-rich
the boundary conditions are specified. molecules such as ATP (adenosine tri-
PHYSICS TODAY/NOVEMBER 1972 27
 phosphate). The usual way this mech-
anism operates is to affect the rate at
which a particular protein (enzyme)
catalyzing one reaction step acts. One
of the best studied biochemical chains
from this point of view is glycolysis, a
process of great importance for the ener-
getics of living cells. Experiments show
taint's that the concentrations of the chemicals
participating in the reaction present
undamped oscillations in time, with per-
Remarkable fectly reproducible periods and ampli-
tudes. On the other hand, starting from
Timing known data on the elementary reaction
steps, one can construct mathematical
models for glycolysis.12'13 A detailed
Discriminator study of the rate equations shows that
the experimental results may be inter-
preted quantitatively as oscillations of
the limit-cycle type arising beyond the
instability of a time-independent solu-
• VIRTUALLY INDEPENDENT tion that belongs to the thermodynamic
OF RISE TIME branch. In other words, glycolysis is a
temporal dissipative structure. This
• ±1.4 NANOSECOND WALK
IN 100:1 DYNAMIC RANGE, result is expected to extend to a whole
Ge(Li) series of regulatory processes at the
metabolic level.
af
A second type of control mechanism
TIMWE DISC in living cells affects the rate of synthe-
M0B61 SIOAt'
sis of the various protein molecules that
exist in a cell. Usually this mechanism
Now, walk-free works on a group of more than one en-
signals using any zyme molecule. Francois Jacob and
fit kind of detector —
without amplifiers
Jacques Monod have proposed several
ingenious models: Either the products
of the metabolic action of the enzymes
or timing filters!
And if you need act on the genetic material to inhibit
even less walk, call the synthesis, or the initial metabolites
ELSCINT . . . we
added to the medium have the effect of
have the technique.
switching on the action of a part of the
genetic material. Again, one can con-
That's typical of struct mathematical models for this
ELSCINT's process.1415 The study of rate equa-
unrivaled line of tions reveals that the activated and in-
nuclear instruments. activated regimes belong to two differ-
ent branches of solutions which, under
certain conditions, are separated by an
instability.
A number of vital biological processes,
in particular the functioning of the ner-
vous system, rest on the ability of cer-
tain cell membranes to switch abruptly
from a rest state of low ionic permeabil-
ity to an excited state of high permeabil-
ity. The former is a polarized state aris-
ing from the maintenance of different
ionic-charge densities on the two sides.
In the excited state the ionic-charge-
density difference tends to diminish in
an almost discontinuous fashion (all-or-
none transition). This depolarization
can be interpreted quantitatively16 as a
transition arising beyond the instability
FREE 16-PAGE of the polarized state and belonging to
"METHODS the "nonthermodynamic" branch.
OF NUCLEAR Here the constraint driving the system
INSTRUMENTATION"
far from equilibrium is the difference
in charge density on the two sides.
ELSCINT LTD. Certain unicellular organisms develop
Exclusive USA Sales & Service:
a kind of organization composed of indi-
PRINCETON APPLIED RESEARCH CORP.
NUCLEAR INSTRUMENT DEPT. vidual cells aggregated in colonies; a
P.O. Box 2565
Princeton. New Jersey 08540
primitive form of differentiation be-
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28 PHYSICS TODAY/NOVEMBER 1972
tween cells is also observed in these
colonies. Among the best studied fami-
lies showing this behavior are the slime
molds. Their aggregation is mediated
by a cyclic AMP (adenosine monophos-
phate) that can be secreted by the cells.
The initiation of this aggregation can be
interpreted17 as an instability of the uni-
form distribution (corresponding to the
absence of aggregation) of the individual
cells, which again belongs to the ther-
modynamic branch. One is tempted to
hope that these aggregation phenomena
will provide valuable indications of how
higher organisms develop. In this case
the interpretation in terms of dissipative
structures would provide a much needed
unifying principle for all these extremely
diverse and complex processes.
* * *
This is the first part of a two-part article.
In the second part, to appear next month, we
contrast prebiological with biological evolu-
tion, as described in terms of the "survival of
the fittest" principle. Of special interest to
us will be instabilities that may lead to in-
creased entropy production. We shall de-
scribe Eigen's recent theory of competition
among biopolymers and, with simple mathe-
matical models, shall illustrate the relation
between stability and evolution.
References
1. I. Prigogine, Etude thermodynamique
des Phenomenes Irreversibles, Desoer,
Liege (1947).
2. L. von Bertalannfy, General System The-
ory, Braziller, New York (1968).
3. E. Schrodinger, What Is Life''., Cam-
bridge University Press, London (1945).
4. P. Glansdorff, I. Prigogine, Thermody-
namic Theory of Structure, Stability
and Fluctuations, Wiley, New York
(1971).
5. R. Graham, H. Haken, Z. Phys. 237, 31
(1970).
6. I. Prigogine, G. Nicolis, Quart. Rev.
Biophys. 4, 107 (1971).
7. I. Prigogine, Physica 31, 719 (1965).
8. A. M. Turing, Phil. Trans. Roy. Soc.
(London) B237, 37 (1952).
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Sci. (US) 68, 2102(1971).
10. A. Zhabotinski, Biphysics 9, 306 (1969);
M. Herschkowitz-Kaufman, Comptes
Rendus 270C, 1049 (1970); A. T. Winfree,
Science 175, 634(1972).
11. D. Thomas, A. Goldbeter, private com-
munication (to be published).
12. E. E. Sel'kov, Eur. J. Biochem. 4, 79
(1968).
13. A. Goldbeter. R. Lefever, Biophys. J.
October 1972.
14. D. Cherniavskii, L. Grigorov, M. Polya-
kova in Oscillatory Processes in Biologi-
cal and Chemical Systems Nauka Mos-
cow (1967).
15. A. Babloyantz, G. Nicolis. J. Theor Biol
34,185(1972).
16. R. Blumenthal, J. P. Changeux, R. Lefe-
ver, J. Membrane Biol. 2, 351 (1970).