Thermodynamic nature of the biological evolution. The model and the reality
This paper is dedicated to the memory of professor
Institute of Ecological
Biophysical Chemistry, Academy of Creative
Endeavors, 36 Novy Arbat, Moscow 121205, Russia
Macrothermodynamic model describing the evolution of supramolecular
structures and chemical composition of living objects in the course of
ontogenesis, and also at long periods of biological evolution in general,
is presented. The study of quasi-closed (thermodynamically and kinetically)
systems, namely, the phases of supramolecular structures of biomass enables
one to make the conclusion about the thermodynamic nature of biological
evolution. According to the Second Principle of thermodynamics, this nature
leads to the variation of chemical composition and structure of living
systems in the process of their development. By means of direct and indirect
proofs, it is shown that the specific Gibbs function of supramolecular
structure formation for the tissue of animals in the course of ontogenesis
tends to a minimum. The conclusion that thermodynamics is the “motive force”
of the biological evolution, is verified.
Key words: Biological evolution, macrothermodynamics,
hierarchical system, quasi-closed system, ontogenesis, phylogenesis, chemical
composition of living bodies.
“The origin and evolution of life is the origin and
evolution of the thermodynamic self-organized (self-assembled), self-reproduced
The understanding of the evolution and behaviour of natural
systems is mostly based on classical natural science. Two approaches play
prevailing role here: the thermodynamic one and the kinetic one. Thermodynamic
description of systems and phenomena is based on the concept of the equilibrium
state. Thermodynamics answers the question about the direction of a process
before the equilibrium is achieved. It does not use time as a parameter
and does not consider the mechanisms of phenomena. In contrast, kinetics
deals directly with the rates of processes and studies their mechanisms.
During the recent decades, foundations of non-equilibrium
thermodynamics for near-equilibrium systems ( irreversible processes) have
been developed. This allowed the combination of both approaches mentioned
above. However, the results obtained so far can be applied only to a few
simple phenomena. A similar situation takes place for the thermodynamics
of systems that are far from equilibrium and for synergetics. Both of them
are based on purely kinetic methods.
Restricted scopes of the approaches mentioned above lead
a number of researchers to the opinion that the evolution of living systems
hardly agrees with the Second Principle of thermodynamics.
Recently a new scientific area appeared - hierarchic thermodynamics
(structural thermodynamics), or macrothermodynamics [1-6] - which points
out the way to study living objects on the basis of equilibrium thermodynamics
[7,8] and some branches of the physical chemistry of natural systems [1,9-11].
Besides, macrothermodynamics is also based on the principles of macrokinetics.
In a certain sense, it is an alternative to the thermodynamics of near-equilibrium
systems. Macrothermodynamic models are advantageous when used for the study
of slightly non-equilibrium processes of structure formation, which are
analogues of slightly non-equilibrium phase transitions.
In a few recent works approaches to the development of
the macrothermodynamic theory of biological evolution have been pointed
out [1,2]. A model has been created whose main elements have been verified
in various studies. At the same time, the model has never been presented
in relation to physical and chemical phenomena in a clear compact form,
understandable for biologists. Certainly, this complicates the understanding
of the approach suggested by the author, and - which is more significant
- does not allow one to estimate the scope of the theory’s predictions.
One of the reasons for such a situation was the author’s desire to find
the motive force of the evolution (for all biological hierarchies) based
on the general deductive principles (first of all, on the principle of
reductionism). Besides, the absence of strict experimental proofs of the
model apparently did not promote its wide use.
After the first works of the author have been published
 an essential advance has been achieved. With the help of quantitative
data, it became possible to apply the model to the evolution of the chemical
composition of living objects and to prove that the model agreed with reality
In the present paper, the physico-chemical model of biological
evolution is briefly described for the case of the evolution of biotissue`s
supramolecular structures (their chemical composition and structure). Besides,
a few experimental results confirming the model, are presented.
2. The model of a living system evolution
Consider a certain volume of biotissue (biomass) as a
heterogeneous thermodynamic system consisting of a liquid phase
(water solution of physiological substances), and a phase of supramolecular
structures (a supramolecular “frame” of biological structures), which
appeared due to the aggregation (self-assembly) of molecules and supramolecular
structures of different hierarchies [5,6]. Besides, the phase of supramolecular
structures results from slightly non-equilibrium phase transitions.
We suppose that there is local supramolecular equilibrium
in all points (microvolumes) of the phase of supramolecular structures
(which also includes small molecules). According to this, let us call the
self-assembly phenomenon, which leads to the supramolecular phase formation,
the thermodynamic self-organization. This notion must be distinguished
from Prigogine’s dynamic (kinetic) self-organization, or simply self-organization,
in Prigogine’s terms, which can be observed in systems far from equilibrium.
The existence of local equilibrium means that at times comparable with
the characteristic periods of relaxation to equilibrium we deal with a
set of microvolumes constituting the phase under consideration, - which
are thermodynamically quasi-closed. It is obvious hence that the integral
value of the specific (averaged over the volume) Gibbs (or Helmholz) function
of supramolecular structure “averaged local conformation” approaches
min; min ,
For the phase of supramolecular structures of constant
(at times of relaxation to local equilibrium)
where V is the volume of the system, m is
the mass of the selected microvolumes, x, y and z
are the coordinates; the sign "-"means
that the specific value is considered; the sign "~" points out the heterogeneous
nature of the system. We should mention that nobody seems to doubt the
validity of Eqn (1) at present.
At times much longer than those needed for relaxation
to the local intermolecular equilibria, the biosystem is naturally open
- there is a flow of matter passing through it. It seems as the biosystem
is blown up, its volume and mass increasing. The model assumes that the
average chemical composition of the flow of matter is constant (although
it fluctuates near the average value).
Thus the nature of the substance coming into the
system (into the phase of supramolecular structures) practically does not
vary. In other words, the supramolecular phase (structure) of an organism
undergoes an evolution “against the background” of the flow of chemical
substances of almost constant composition, which come into the system.
If the flow is slow enough then we can assume that the liquid phase of
the biosystem is always in equilibrium with the flux. This provides constant
average concentrations of substances coming into the liquid phase. This
phase together with the environment can therefore be considered as a thermostat
(in the broad sense of this term - T, p, concentrations of the chemical
components and other parameters are constant) for the phase of supramolecular
Chemical composition of a biosystem’s phase of supramolecular
structures varies slowly at times comparable with the duration of adaptive
processes and ontogenesis (it also varies in the course of phylogenesis
and at long periods of biological evolution in general). As the biotissue
gets older, the supramolecular structures become more stable thermodynamically
(here we mean the stability of supramolecular structures but not of the
chemical substance they contain).
Selection of supramolecular structures with higher thermodynamic
stability (structural stabilization of phase [1,2]) is determined by the
thermodynamic factor. Indeed, it is admitted that the retention (holding)
time (this term is taken from chromatography) of molecules (macromolecules)
in supramolecular phase, ,
is related to the value of the Gibbs function of supramolecular structure
where R is the gas constant.
The most long-holded molecules of the supramolecular phase
(coming into the biosystem from the environment or produced in the course
of the biosynthesis) initiate the selection of similar molecules. This
also changes the composition and chemical nature of the phase of supramolecular
structures. As we have already pointed out, these changes result from the
thermodynamic factor, though in its kinetic form (Eqn 2). Thus, above all,
those molecules are accumulated in the microvolumes of the phase of supramolecular
structures whose absorption (self-assembly) is most beneficial thermodynamically
(these molecules have higher affinity for the phase of supramolecular structures).
If there are mechanisms of matrix synthesis, such molecules have advantages
for reduplication (reproduction). Due to all this, the absolute value of
the specific Gibbs function of supramolecular structure formation, ,
(or the absolute value of the specific Helmholtz function, which, for the
condensed phase, practicaly, coincides with it) grows as the biotissue
gets older, becoming more negative. It follows that
For the phase of supramolecular structures of varying
(for the times of ontogenesis, phylogenesis, etc.)
Eqn (3) means that the value of (Eqn
1), whose minimum corresponds to a local equilibrium (),
in the course of ontogenesis (and also phylogenesis and long stages of
evolution) varies slowly, tending to a still lower value ().
Let us note for clarity that Eqn (3) follows from the
fact that the phase of supramolecular structures (or biotissue as a whole)
is partly quasi-closed in relation to the outcoming flows of matter.
This kinetical (dynamical) quasi-closeness leads to the accumulation of
aggregates of molecules with higher thermodynamic stability in the unit
volume of the phase of supramolecular structures [1, p.90-92]. Eqs (2)
and (3) actually determine the time axis (kinetic parameter) for the variations
of and ,
and, consequently, also for their sum, whose value is negative:
The last conclusion, however, as we have already stressed,
relates to the case where the flow of the matter coming into the
biosystem has constant composition. If the composition of the incoming
matter varies in time (for instance, at some physiological anomalies or
variable parameters of the thermostat), then the system can become not
quasi-closed kinetically, and the variation of can
The model described here has a simple analogue an adsorption
(absorption) system, which is open and which slowly receives a flow of
substance with constant composition. Inside the system, this substance
undergoes phase or chemical changes [1, p.90-92]. Indeed, suppose that
a homogeneous flow at the input contains a fatty acid and water as basic
components, and there is microemulsion formed inside a column (reactor),
so that the fatty acid concentration in the microemulsion is high. Then
the column will be soon “overfilled” with the fatty acid and will stop
operating. (Here the fact is demonstrated that the system is partly quasi-closed
kinetically.) Apparently, there is no doubt that the tendency presented
in Eqn (3) is valid in this case (, pp.71-75; 90-92; 163-165).
Eqn (3) means that as the biotissue gets older, it must
normally get enriched by chemical compounds with the most negative values
of the Gibbs function of supramolecular structure formation ().
Substances with high energetic capacity, having less negative values
of the Gibbs function of chemical compounds formation (from simple substances
or elements), ,
- are namely of this kind, and this follows from the theory and has been
found out experimentally [1, 13-15]. These are lipids, proteins, polysaccharides,
nucleic acids and so on, substances that force water out of the biotissue
volume as it ages. Such tendencies must also be observed in phylogenesis
and at long periods of the biological evolution when the average chemical
composition of the environment can be considered as constant (in this case,
one can assume that the biosystems are partially quasi-closed kinetically).
The model considers the processes of self-assembly independently
of the regime in which chemical reactions in the liquid phase take place.
The processes of supramolecular structure formation move the substance
synthesis and transport mechanisms to the background: they only “use” these
substances for the building of supramolecular structure of biotissue. The
model has also serious grounds to admit that the thermodynamic system under
consideration is a simple one - by definition, only expansion work is produced
in it (this kind of work is rather small in condensed phases). To be sure,
this approximation becomes unjustified while studying, for instance, the
evolution of a population (when it is considered by itself), which is a
structure of high hierarchy performing mechanical or any other work. (Here
the role of interacting particles is played by organisms, and the study
is focused on irreversible processes that are not accompanied by the entropy
Functioning of biological systems (for instance, of biotissue)
is possible if these systems are “penetrable” enough for the matter, which
is the building material for supramolecular structure. Besides, as it has
been first pointed out in paper , there should exist not only internal,
but also external forces leading to the “mixing” inside the substance -
to the metabolism. This role is played by periodic fluctuations of the
environment (thermostat) parameters around their mean values. Let us stress
that these necessary periodic variations of external parameters are the
essential “thermodynamic effect” of the environment on the evolution of
biosystems. We obtain that the joint action of internal thermodynamic factors
(observed inside the system) and of external thermodynamic effects (variations
and oscillations of the environmental physical parameters) determine the
direction and rate of the evolution.
In the model presented here special attention is paid
to the physical chemistry of supramolecular structures, which should be
considered as one of the “keys“ to the understanding of biological evolution.
It can be easily proved that this model does not contradict the kinetic
theory of Darwin and Wallace and pacifies the disputes around it.
3. On the experimental proofs of the model
According to the model presented above, a biosystem under
normal physiological conditions expands in the course of ontogenesis. According
to Eqs (3), (4), the system is enriched by energy-intensive substances,
which oust water from the biotissue. The experimental proofs of this have
been published in [1-6]. In Fig.1 the theoretical scheme is shown demonstrating
how the supramolecular (im) and chemical (ch) parts of the
specific Gibbs function of the biotissue vary in the course of ontogenesis
(ont) and phylogenesis (ph). (In the first papers by the
author the chemical part of the Gibbs function was denoted by index “m”
Indeed, there has been obtained various material concerning
the changes in the gross chemical composition of organisms (of their organs
and tissues) in the course of ontogenesis, phylogenesis and biological
evolution in general. A typical example of the variation of chemical compound
“water - organic substances” in the brains of different animals, depending
on relative levels of their evolutionary development, published in paper
Now our aim is to show that the discussed variation of chemical
composition results from the tendency of a biosystem to get (to aspire)
to supramolecular equilibrium in the course of the evolution. In other
words, the validity of Eqs (3), (4) is to be proved on the experimental
||Fig.1. Schematic variation of the specific
values that are parts of the Gibbs function of a biosystem j, in
the course of ontogenesis and phylogenesis. This scheme can be also applied
to the long periods of biological evolution. For instance, biosystem j
is a biotissue of an animal. and are
the specific values of chemical (ch) and supramolecular (im)
parts for j-th system; and denote
the time for ontogenesis and phylogenesis, respectively; and
are measured in relative units (
> ); are
arbitrary functions; values of with
indices characterize the specific values constituting the Gibbs function
of structure formation (the specific Gibbs free energy of the corresponding
structure formation) of the system at a certain time moment; values vary
in the course of evolution due to the variation in the chemical composition
of organisms or species.
Several results relating to the chemical composition variation
of proteins and nucleic acids in the course of the evolution of organisms
are discussed in papers [1,5,6,18]. However, there is still a lack of reliable
information unambiguously confirming the thermodynamic nature of changes
in the composition of these natural polymers. This is well illustrated
by the growth of the melting temperature of chromatin in the course of
ontogenesis. This growth is believed to indicate definitely that the evolutionary
aging of chromatin in the ontogenesis has thermodynamic nature [1, p. 161-163].
New results  make it possible to conclude that the evolutionary optimization
of the RNA structure is determined not only by the thermodynamic stability
of its secondary structure, but also by that of its tertiary structure.
This explains why not only the sequences containing GC pairs are selected
in the course of evolution (which is most beneficial thermodynamically
for the secondary structure formation). In the course of the evolution,
sequences including AU pairs are also selected. We obtain (according to
the theoretical predictions) that the thermodynamics of tertiary and higher
supramolecular structures influences the chemical composition and structure
of the RNA. Therefore, from our view point, selection of natural (AUGC)
sequences is most advantageous macrothermodynamically. P.Shuster considers
these sequences as the most stable ones with respect to mutations.
Recently new data appeared in literature that unambiguously
prove, after some calculations, the thermodynamic direction of the biotissue
development in the course of ontogenesis. For instance, by means of differential
scanning calorimetry the relation was studied between the age of the collagen
tissue of a rat's tail tendon and the temperature and heat of its denaturation
. Based on the study of about a hundred samples, it was found out that
as the age of the tissue varies from 2 weeks to 2 years, its denaturation
(melting) temperature increases
by 6°C - approximately from 58°C
to 64.5°C. According to our estimation, the
denaturation enthalpy variation, increases
in this process from 6.0Cal/g to 7.6Cal/g . The thermal capacity
variation corresponding to the transition of the biotissue from the native
state to the denaturated one is =
0.096Cal/deg× g ( ).
Using the data presented, one can easily, with the help
of the Gibbs-Helmholz equation, which takes into account the heat capacity
variation at a phase transition, calculate with a considerable accuracy
(not accounting for the heat capacity variation with the increase of temperature)
the Gibbs function variation corresponding to the supramolecular structure
formation at a standard (reference) temperature, ( :
Assuming, for example, T=298.2 K (25°C)
for the tissue of, say, a 2-year-old rat, we obtain:
For the tissue of a two-week-old animal .
Calculations carried out for different stages of the ontogenesis
show that indeed, in accordance with the theory, the value of for
the intact collagen of a rat's tail tendon tends to a minimum as the rat
gets older. In the case under consideration it varies by value Note
that a rough estimate, according to the approximate equation ,
yields the value (for
standard temperature, T0=40°C ).
Variations of (and
also of at
the aging of the collagen tissue correlate with the changes in the amount
of water, whose concentration in the tissue varies within the range of
78-58% weight units .
The absolute values of calculated
here for the collagen tissue are smaller than the analogous values for
the processes of some pure chemical substances condensation [5,21,22].
This contradicts neither the physical picture of the life phenomenon, nor
other well-known facts [8,10,20,23,24].
There are grounds to suppose that the presented experimental
results can be of greatest importance. They will stimulate new studies
aimed at further verification of the fact that the Second Principle can
be applied to the evolution of biological and other natural systems.
The existing experimental data allow to state that the
macrothermodynamic (hierarchic thermodynamic) model of the living systems
evolution can be applied to the real world: thermodynamics is the motive
force of the evolution.
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