Abstract

The current framework of evolutionary theory postulates that evolution relies on random mutations generating a diversity of phenotypes on which natural selection acts. This framework was established using a top-down approach as it originated from Darwinism, which is based on observations made of complex multicellular organisms and, then, modified to fit a DNA-centric view. In this article, it is argued that based on a bottom-up approach starting from the physicochemical properties of nucleic and amino acid polymers, we should reject the facts that (i) natural selection plays a dominant role in evolution and (ii) the probability of mutations is independent of the generated phenotype. It is shown that the adaptation of a phenotype to an environment does not correspond to organism fitness, but rather corresponds to maintaining the genome stability and integrity. In a stable environment, the phenotype maintains the stability of its originating genome and both (genome and phenotype) are reproduced identically. In an unstable environment (i.e., corresponding to variations in physicochemical parameters above a physiological range), the phenotype no longer maintains the stability of its originating genome, but instead influences its variations. Indeed, environment- and cellular-dependent physicochemical parameters define the probability of mutations in terms of frequency, nature, and location in a genome. Evolution is non-deterministic because it relies on probabilistic physicochemical rules, and evolution is driven by a bidirectional interplay between genome and phenotype in which the phenotype ensures the stability of its originating genome in a cellular and environmental physicochemical parameter-depending manner.

Highlights

  • The current framework of evolutionary theory that comes from the modern synthetic theory of evolution postulates that evolution relies on random mutations, generating a diversity of phenotypes on which natural selection acts

  • Supporting the notion that constraints on the physicochemical properties of one kind of polymer affects composition biases of the cognate polymers are the following observations: (i) Nucleosome positioning leaves a footprint in protein sequences, (ii) splicing sites and splicing factor binding motifs constrain the amino acid composition of peptides encoded by splicing-regulated exons, and (iii) mRNA secondary structures depending on base complementarity have consequences on the secondary structures of the encoded protein [40,49,50,51]

  • Part (i)acids defines physicochemical forces driving evolutiontofrom molecular origin of life and in nucleic andthe cognate proteins allows both polymers dealthe with the same fundamental (ii) describes the bidirectional interplay indefines terms ofthe stability between genomes and phenotypes

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Summary

Introduction

The current framework of evolutionary theory that comes from the modern synthetic theory of evolution postulates that evolution relies on random mutations, generating a diversity of phenotypes on which natural selection acts. The second objective of this article is to replace the notion of natural selection with the notion that the role of the phenotype in evolution is to maintain the physicochemical integrity and stability of its originating genome This establishes feedforward and feedback loops between the genome and the phenotype, i.e., the genome generates a phenotype that exerts a feedback loop by either maintaining genome stability or guiding genome variations depending on its efficiency to relax environment-dependent physicochemical constraints. Another issue raised by the current model of evolution relies on the fact that the combination of chance and natural selection does not provide a single conceptual framework that simultaneously explains both evolution and organism activities, since evolution, but not organism activities, would rely on chance and natural selection. A “bottom-up” approach redefines (i) the notion of chance in a precise context of physicochemical laws and (ii) the notion of adapted phenotype not in terms of organism fitness but rather in terms of the impact on genome stability

Overview
Environment-Dependent Physicochemical Constraints on Nucleic and Amino Acid
Physicochemical Constraints on Protein Composition
Physicochemical Constraints on Nucleic Acid Polymer Composition
Molecular Origin of Life and Evolution of the Genetic Code
Molecular Origin of Life
Evolution of the Genetic Code
Continuum between Physiological and Genetic Adaptation
Genetic Adaptation Directed by Transcription
Physiological Adaptation Facilitates Genetic Adaptation
Somatic Physiological Adaptation and Germline Genetic Adaptation
From Diversity to Complexity
Conclusions
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