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      Principles of Molecular Evolution: Concepts from Non-equilibrium Thermodynamics for the Multilevel Theory of Learning

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          Abstract

          We present a non-equilibrium thermodynamics approach to the multilevel theory of learning for the study of molecular evolution. This approach allows us to study the explicit time dependence of molecular evolutionary processes and their impact on entropy production. Interpreting the mathematical expressions, we can show that two main contributions affect entropy production of molecular evolution processes which can be identified as mutation and gene transfer effects. Accordingly, our results show that the optimal adaptation of organisms to external conditions in the context of evolutionary processes is driven by principles of minimum entropy production. Such results can also be interpreted as the basis of some previous postulates of the theory of learning. Although our macroscopic approach requires certain simplifications, it allows us to interpret molecular evolutionary processes using thermodynamic descriptions with reference to well-known biological processes.

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          Most cited references75

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          A Mathematical Theory of Communication

          C. Shannon (1948)
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            Stochastic thermodynamics, fluctuation theorems and molecular machines.

            Stochastic thermodynamics as reviewed here systematically provides a framework for extending the notions of classical thermodynamics such as work, heat and entropy production to the level of individual trajectories of well-defined non-equilibrium ensembles. It applies whenever a non-equilibrium process is still coupled to one (or several) heat bath(s) of constant temperature. Paradigmatic systems are single colloidal particles in time-dependent laser traps, polymers in external flow, enzymes and molecular motors in single molecule assays, small biochemical networks and thermoelectric devices involving single electron transport. For such systems, a first-law like energy balance can be identified along fluctuating trajectories. For a basic Markovian dynamics implemented either on the continuum level with Langevin equations or on a discrete set of states as a master equation, thermodynamic consistency imposes a local-detailed balance constraint on noise and rates, respectively. Various integral and detailed fluctuation theorems, which are derived here in a unifying approach from one master theorem, constrain the probability distributions for work, heat and entropy production depending on the nature of the system and the choice of non-equilibrium conditions. For non-equilibrium steady states, particularly strong results hold like a generalized fluctuation-dissipation theorem involving entropy production. Ramifications and applications of these concepts include optimal driving between specified states in finite time, the role of measurement-based feedback processes and the relation between dissipation and irreversibility. Efficiency and, in particular, efficiency at maximum power can be discussed systematically beyond the linear response regime for two classes of molecular machines, isothermal ones such as molecular motors, and heat engines such as thermoelectric devices, using a common framework based on a cycle decomposition of entropy production.
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              Horizontal gene transfer in eukaryotic evolution.

              Horizontal gene transfer (HGT; also known as lateral gene transfer) has had an important role in eukaryotic genome evolution, but its importance is often overshadowed by the greater prevalence and our more advanced understanding of gene transfer in prokaryotes. Recurrent endosymbioses and the generally poor sampling of most nuclear genes from diverse lineages have also complicated the search for transferred genes. Nevertheless, the number of well-supported cases of transfer from both prokaryotes and eukaryotes, many with significant functional implications, is now expanding rapidly. Major recent trends include the important role of HGT in adaptation to certain specialized niches and the highly variable impact of HGT in different lineages.
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                Author and article information

                Contributors
                smiatek@icp.uni-stuttgart.de
                Journal
                J Mol Evol
                J Mol Evol
                Journal of Molecular Evolution
                Springer US (New York )
                0022-2844
                1432-1432
                29 August 2024
                29 August 2024
                2024
                : 92
                : 6
                : 703-719
                Affiliations
                Institute for Computational Physics, University of Stuttgart, ( https://ror.org/04vnq7t77) Allmandring 3, 70569 Stuttgart, Germany
                Author notes

                Handling editor: David Liberles.

                Author information
                http://orcid.org/0000-0002-3821-0690
                Article
                10195
                10.1007/s00239-024-10195-8
                11703993
                39207571
                28db50e2-6dfa-4219-b486-c15e169e0d2f
                © The Author(s) 2024, corrected publication 2024

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 6 July 2023
                : 11 August 2024
                Categories
                Original Article
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                © Springer Science+Business Media, LLC, part of Springer Nature 2024

                Evolutionary Biology
                non-equilibrium thermodynamics,minimum entropy production principle,evolutionary potential,horizontal gene transfer,mutations

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