On the way to the physical principles of biological evolution. Finish + full translation

    Abridged translation of an article by M. Katznelson, J. and E. Wolf Kunin
    Towards Physical Principles of Biological evolution
    Mikhail I. The Katsnelson, Yuri I. The by Wolf, Eugene V. The Koonin
    Original article
    (Two previous articles have already been published: the beginning and the continuation )

    Is convergence of physics and biology possible?

    An article suggestive of such reflections, I became interested in the presentation of the astrophysicist and popularizer of science Sergei Popov. In one of his reviews of preprints, an article with an intriguing title was mentioned, and among the authors was Yevgeny Kunin. I began to read the book of this author, "The Logic of Case" ... Of course, only separate sections. Engineering education, doing technical translations, reading popular science articles - all this brought me to a seditious thought - to perform a brief translation of an article written by Yevgeny Kunin in collaboration with Mikhail Katsnelson and Yury Wolf.


    Biological systems achieve complex organization, which significantly exceeds the complexity of any of the known inanimate objects. Biological entities, of course, are subject to the laws of quantum physics and statistical mechanics. However, is modern physics enough to adequately describe the model and explain the evolution of biological complexity?

    This article provides a detailed analysis of the analogies between statistical thermodynamics and the population-genetic theory of biological evolution. Based on the presented analogies, we outline new perspectives in relation to theoretical approaches in biology and major transitional periods of evolution, and also offer a biological equivalent of thermodynamic potential, which reflects the propensity for changes in the evolving population.

    It is assumed that there are deep analogies: between the properties of biological entities and the processes in them on the one hand, and non-equilibrium states in physics, for objects such as glass. Such systems are characterized by a violation whereby a local state with a minimum of free energy conflicts with a global minimum, resulting in “nascent qualities”. We disseminate such analogies through the study of manifestations of nascent qualities, such as, for example, between different levels of selection in biological evolution. Such frustration effects appear as drivers in the evolution of biological complexity.

    Next, we turn to evolution in multidimensional adaptive landscapes, considering them from the point of view of percolation theory (percolation), and assume that percolation at a level above the critical threshold causes a tree-like type of evolution of complex organisms. Taken together, these multiple connections between fundamental processes in physics and biology mean that the construction of a meaningful physical theory of biological evolution cannot be a futile attempt. However, it would not be realistic to expect such a theory to be created by “one scooping”; even if we move towards this, this can only happen through the integration of various physical models of evolutionary processes.


    What is the difference between living organisms and inanimate matter? There is an obvious answer to this question when defining in terms of chemical composition and structure. (At least, because the only suitable case, namely, life on Earth, refers to this). But when it comes to the basic processes of the evolution of life, the difference becomes less obvious. In the Darwinian tradition, it is tempting to argue that life is determined by evolution through the survival of the fittest [1-4].

    However, the uniqueness of this process can be questioned, since the entire history of the Universe consists of changes that withstand the most stable (adapted) structures. Moreover, the process of replication (reproduction) is not in itself unique and exists not only in biology: crystals also replicate. On a macroscopic scale of time and space, however, life is undoubtedly a clear phenomenon. For an objective determination of the characteristic features by which life differs from other phenomena existing in the Universe, it is important to investigate key processes of biological evolution within the framework of theoretical physics [5, 6].

    Perhaps the main feature that distinguishes modern physics from other areas of human exploratory activity is the obvious link between theory and experiment, in which research programs are formed by verifiable theoretical predictions. In a general sense, modern biology is not a science based on theory, in the sense in which physics is interpreted. But there is a significant exception, namely - population genetics (a formalized section of biology, which is effectively structured as a field of theoretical physics), similar mainly to statistical thermodynamics [7-10].

    At the same time, mathematical models of population genetics are highly effective in immunology [11, 12] and biological oncology [13–16], which, perhaps, suggests that further penetration of theory into biology could turn out to be real and productive. Modern theoretical physics is an area with many strong links in which the most diverse subdivisions of physics are intertwined. At present, population genetics or some other direction of theoretical biology is not part of such a network. It is possible to argue that this separation is not optimal, since many sections of theoretical physics would provide information and stimulate theoretical developments in biology.

    And yet there is still such a landmark question: is modern physics sufficiently filled to serve (provide support) for biology? A similar question, in various formulations (in particular, “whether biology is reducible to physics”), has a long and very dramatic history (for example, [17, 18]).

    Without going into details of a historical or philosophical plan, we reject any assumption that life may follow some special laws of “biological” physics instead of the general ones that exist. For example, quantum mechanics, in general, is quite effective and applicable to living organisms, just like any other form of matter. The problem is that this strong theory, to a certain extent, can be considered as a “theory of everything”, as it introduces little in explaining biological phenomena [19, 20]. Of course, quantum-mechanical calculations can be useful in analyzing biochemical reactions, but they can not help us in understanding evolution. Therefore, it is assumed that the physical concept, which could be the main one in the theoretical description of biological phenomena, is the appearance (or the appearance, emergency), that is, the collective behavior of large aggregates, which is qualitatively different from the behavior of their components. “More is different” is so anphoristically formulated by Anderson [19-24].

    In his book containing fruitful ideas “What is life? The physical aspect of the living cell "Schrodinger made several basic points that even after 70 years remain at the heart of many discussions about the significance of physics for biology [25]. Probably the most significant is the characterization (at that time hypothetical) of molecular carriers of heredity as “aperiodic crystals”. Schrödinger was inaccurate in such a definition of an aperiodic crystal, and so far this metaphor covers the basic properties that were later discovered (not without the influence of Schrödinger) of biological information carriers, DNA and RNA [26-28].

    Molecules of nucleic acids, in particular DNA, combine the uniformity (and periodicity) of the spatial structure with the effectiveness of multiple diversity (aperiodicity) of the main sequence. The combination of these distinctive features makes nucleic acids the only known molecules suitable for storing and transmitting digital information [29], in full accordance with Schrödinger's prediction. As for modern physics, biological “aperiodic crystals” are sometimes referred to as “glasses” [19, 20]. In fact, there are deep analogies, at various levels, between the state of glass and biological structures and the phenomena discussed below. At the same time, it will be shown that there are significant differences: in a certain sense, the glasses exhibit excessive confusion.

    Another well-known statement by Schrödinger that organisms use “negative entropy” (or negentropy, a term that Schrödinger obviously liked but was not picked up by researchers) is potentially deceptive. Strikingly, during the time of Schrödinger, it seemed widespread, albeit uncertain, the view that such complex systems as living beings sometimes violate the second law of thermodynamics, and that such an apparent “violation” requires a special explanation [30].

    Now we better understand the nature of entropy and the second law of thermodynamics, so that such a view of Schrödinger is possible and necessary to clarify. Obviously, the biosphere and the Earth as a whole are not closed systems, but rather open to a constant flow of energy, mostly from the Sun (other sources of relatively lesser environmental significance include the radioactive decay of heavy elements in the interior of the Earth).

    Earthly life uses this flow of energy through photosynthesis, carried out by photo autotrophs (organisms that use light energy to biosynthesis of cell components), which function, to a certain extent, like photochemical machines. Of course, when considering the Sun-Earth system, even the appearance of a violation of the second law of thermodynamics is absent. Each individual organism, population, or ecosystem is also thermodynamically open systems. And more appropriate would be the statement that organisms mainly consume energy along with chemical building blocks, rather than 'negentropy', according to Schrödinger's bizarre statement.

    However, with regard to Schrödinger's current motivation in the presentation of 'negentropy', one can say that this correlates with some of the most fundamental and complex problems of biology, namely, the emergence and preservation of a surprising order and gigantic complexity in living organisms. Complexity is undoubtedly one of the most problematic concepts in all of science; it confronts all-encompassing definitions [34]. In fact, the most used definitions of complexity are context dependent. In biology, complexity is significant, at least at the level of genomes, organisms, and ecosystems [35, 36].

    The complexity of the genome can be clearly interpreted through the number of nucleotide sites that are selected and thus carry biologically significant information [37-39], although the detailed definition does not take into account other important sources of complexity at the genome level, such as alternative transcription initiation and alternative splicing in eukaryotes (alternative splicing in eukaryotes). Complexity in relation to the organism and ecology is usually perceived as the number of individual constituent parts and / or hierarchy levels in the respective systems [40]. Regardless of the exact definitions, it seems clear that a consistently maintained, ever-increasing level of complexity is an exceptional characteristic feature of life and a major challenge for theoretical constructs.

    The most traditional means of interaction between physics and biology is biophysics, which studies the properties of the structure and dynamics of biological macromolecules, as well as the structure of cells and organisms, together with their functions, through the approaches adopted in physics. Various areas of biophysics have proven to be productive and successful for several decades [41]. However, this is, after all, a separate additional area of ​​interaction between physics and biology, whereby physical theory is used to describe, model and analyze biological processes, in particular, evolution at the population level.

    Already, Bohr attached particular importance (as part of the general discussion on the complementarity principle) of complementarity between the purely physical, structural approach to organisms and the “whole” nature as living beings [42]. The principle of drawing analogies between thermodynamics and statistical mechanics, on the one hand, and population genetics, on the other hand, was first proposed by the famous statistician and founder of the theory of population genetics, Ronald Fisher in the 1920s [43], and in subsequent years development of a theoretical approach to this process [7, 9, 10].

    In various forms, the theoretical formalism (mathematical models for describing a theory) from statistical mechanics was increasingly used to substantiate the model of biological evolution. Among other similar mathematical models, the use of percolation theory for analyzing evolution in adaptive landscapes [44-46] finds significant use. The main goal of such penetration of physics into evolutionary biology is rather ambitious: it is nothing more than the development of a physical theory of biological evolution, or even the transformation of biology into a part of physics [5, 6].

    Obviously, such a comprehensive program, even a feasible in principle, cannot be implemented in one fell swoop. Only progress is possible at one of the stages at a given time by simulating a diverse evolutionary process using the ideas and mathematical apparatus of theoretical physics in the hope that in the end it will be possible to combine such models into a harmonious theoretical justification.

    In this article, we discuss several aspects of biological evolution, where theoretical considerations, originating initially from condensed physical concepts, seem possible. We propose for consideration the statement that physical theory is capable of making a non-trivial contribution to the current understanding of evolution, and the latest theoretical developments in physics itself will probably be in demand with full consideration of the phenomenon of the emergence and evolution of the complexity level, which is characteristic of biological systems.

    * The following sections of the article are in a summary of the

    Analogy in thermodynamics and population genetics and the main evolutionary transitions

    Although the existence of analogies when comparing statistical mechanics and population genetics has already been noted by previous researchers, a detailed comparison was made in the paper by Sella and Hirsch, 2005 [7] with the subsequent development in the works of Barton and co-authors [9, 10] (Table 1).

    Thus, evolutionary transitions are represented as analogues of adiabatic transitions of the first kind, while the density of evolutionary information and the evolutionary temperature (effective population size) are thermodynamically related variables.

    Life, glass and patterns: frustrating systems and biological evolution

    According to the first presented “theory of spin glasses” in the work of Edwards and Anderson [58], in modern physics it is believed that glass represents a certain state of matter, intermediate between the equilibrium and nonequilibrium [59-62].

    A characteristic property of glass is aging, or structural relaxation. For example, suppose we define a specific characteristic in the equilibrium phase of a substance in a liquid or solid state, for example, the resistivity of a metal (or a liquid metal). The “equilibrium” state is characterized by the fact that during the subsequent measurement after the heating cycle (slow heating followed by cooling to the initial temperature) we obtain the same specific resistance value. For glass, it is possible to slowly change the measured value from measurement to measurement. The relief of potential energy (or landscape, when using the term in biological connotation) for glass is a function with many (asymptotic, infinite) local minima separated by barriers with an extremely wide distribution of energy. Each of the local minima is a metastable state. During the process of changing the thermal state, the system slowly moves from one minimum to another. It is important that the state of the glass is non-ergodic [59-62].

    The state of the glass is characterized by the “order parameter” always with a set of components, denoted by real numbers x ∈ (0,1) [63]. Such a number can be represented as an infinite, non-periodic binary fraction, such as 0.10001110 ..., where 0 (1) corresponds to the choice of bifurcation on the relief of the complex energy, when cooled from a liquid equilibrium state. This process of changing the thermal state is usually described by the term ultra-metricity: in other words, we are mainly interested in the topological description of the evolution of a system through bifurcations, rather than specific characteristics of barriers, transitions and other characteristics [60]. This feature is the main definition of the concept of an aperiodic Schrödinger crystal [25].

    The main difference is that glasses are not only aperiodic, but also non-ergodic - a sign that causes an evolutionary process. The suitability of the glassy concept for biology is noted in Laughlin et al. [19,20]. At the same time, the defining signs of life, namely, replication with selection, seem to go beyond the behavior of ordinary glass: the potential relief for glass seems to be too flexible and characteristic for a certain kind of substances, which does not quite correspond to the model of biological evolution. Glass shows essentially infinite variability, whereas life is based on discrete forms, such as genomes with specific sequences and certain, long intervals of stability (see further discussion regarding evolutionary transitions).

    * Translator's Note.

    The following two sections of the article are not translated. Best of all, of course, read the original article. The author of the abridged translation suggests that this text may be of interest to readers as a popular science material.

    Percolation + criticality: the basis and state of the tree-like evolutionary process
    Mapping and separation of the genotype-phenotype as a measurement

    Concluding remarks

    “The General Physical Theory of Biology” is probably an impossible dream, but it is indeed possible to describe key evolutionary processes in the language of statistical physics. It is already generally accepted that random (stochastic) processes play a significant role in evolution, and that fluctuations are the drivers of biological complexity, at least in part. Therefore, the use of statistical physics is natural. However, one should not go too far. Natural selection and adaptation are also essential factors of biological evolution, and for embedding these phenomena into the framework of physical theory, the existing apparatus of statistical physics probably requires clarification.

    Here we tried to suggest what kind of modifications might be required for this. The arising phenomena, which are peculiar for theoretical modeling, glass and other condensed matter states are also central for biology. However, it seems that special principles not yet developed in statistical physics need to be created for the physical theory of separation of the genotype-phenotype and mapping, which embodies the basis of evolution.

    Biological evolution in no way ignores the laws of physics, but the emerging biological phenomena initiate the further development of physics itself. Biological creatures and their evolution do not simply follow the principle of “more is different”, but in some respects, they seem to be qualitatively different from non-biological phenomena pointing to particular forms of the “phenomenon of appearance”, which requires a new physical theory.

    The difference between biology and physics (at least, known to us) is not that “nothing in biology makes sense except in the light of evolution” [3], whereas in physics “everything makes sense”. The last statement does not really seem to be true outside of quantum physics, since the whole universe can definitely be correctly perceived only in the light of its evolution over 13.8 billion years.

    Following the above analogy, in biology, as well as in physics, the execution of measurements initiates the arrow of time and creates the need to recognize evolution. However, biological evolution is characterized by significant distinctive features, an attempt to cover some of which we have undertaken here, in particular, by applying concepts of condensed matter physics, such as frustration and percolation (destruction and percolation), to the central processes of biological evolution. Obviously, the analysis and discussion of the material presented here will relate only to preliminary considerations for the continuous, concerted efforts that are required to unite biology and physics.

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