Survival of Self-Replicating Molecules under Transient Compartmentalization with Natural Selection

The problem of the emergence and survival of self-replicating molecules in origin-of-life scenarios is plagued by the error catastrophe, which is usually escaped by considering effects of compartmentalization, as in the stochastic corrector model. By addressing the problem in a simple system composed of a self-replicating molecule (a replicase) and a parasite molecule that needs the replicase for copying itself, we show that transient (rather than permanent) compartmentalization is sufficient to the task. We also exhibit a regime in which the concentrations of the two kinds of molecules undergo sustained oscillations. Our model should be relevant not only for origin-of-life scenarios but also for describing directed evolution experiments, which increasingly rely on transient compartmentalization with pooling and natural selection.

Survival of self-replicating molecules under transient compartmentalization with natural selection

The problem of the emergence and survival of self-replicating molecules in origin-of-life scenarios is plagued by the error catastrophe, which is usually escaped by considering effects of compartmentalization, as in the stochastic corrector model. By addressing the problem in a simple system composed of a self-replicating molecule (a replicase) and a parasite molecule that needs the replicase for copying itself, we show that transient (rather than permanent) compartmentalization is sufficient to the task. We also exhibit a regime in which the concentrations of the two kinds of molecules undergo sustained oscillations. Our model should be relevant not only for origin-of-life scenarios but also for describing directed evolution experiments, which increasingly rely on transient compartmentalization with pooling and natural selection.

The origin of replicators and reproducers

Replicators are fundamental to the origin of life and evolvability. Their survival depends on the accuracy of replication and the efficiency of growth relative to spontaneous decay. Infrabiological systems are built of two coupled autocatalytic systems, in contrast to minimal living systems that must comprise at least a metabolic subsystem, a hereditary subsystem and a boundary, serving respective functions. Some scenarios prefer to unite all these functions into one primordial system, as illustrated in the lipid world scenario, which is considered as a didactic example in detail. Experimentally produced chemical replicators grow parabolically owing to product inhibition. A selection consequence is survival of everybody. The chromatographized replicator model predicts that such replicators spreading on surfaces can be selected for higher replication rate because double strands are washed away slower than single strands from the surface. Analysis of real ribozymes suggests that the error threshold of replication is less severe by about one order of magnitude than thought previously. Surface-bound dynamics is predicted to play a crucial role also for exponential replicators: unlinked genes belonging to the same genome do not displace each other by competition, and efficient and accurate replicases can spread. The most efficient form of such useful population structure is encapsulation by reproducing vesicles. The stochastic corrector model shows how such a bag of genes can survive, and what the role of chromosome formation and intragenic recombination could be. Prebiotic and early evolution cannot be understood without the models of dynamics.

The evolution of templates

In this chapter, we discuss the origin and early evolution of genetic replication. The argument is complex, so we start with a brief outline. Section 4.2 discusses the nature of replication. We draw a distinction between simple replicators, limited hereditary replicators and indefinite hereditary replicators. Continued evolution requires indefinite hereditary replicators: it seems that such replicators depend on some form of template reproduction. In section 4.3, we point out that there is an error threshold for the accuracy of replication: for a given total quantity of genetic information—for example, for a fixed number of bases—there is an upper limit on the error rate of replication. If the error rate rises above this limit, natural selection cannot maintain the information. This leads to what we have called Eigen's paradox. In the absence of specific enzymes, replication accuracy is low. Hence the total genome size must be small—almost certainly, less than 100 nucleotides. The genome is therefore too small to code for accurate replication machinery. There is a catch-22 situation: no enzymes without a large genome, and no large genome without enzymes. The next three sections discuss possible solutions to the paradox. Section 4.4 considers populations of replicating RNA molecules. We point out that the dynamics of replication are such as to lead to the stable coexistence of a diverse population, but we do not think that this constitutes a solution to the paradox. Section 4.5 discusses the hypercycle, a particular relationship between replicators that makes it possible for a greater total quantity of information to be maintained with a given accuracy of replication. We argue that the further evolution of hypercycles requires that they be enclosed within compartments, because otherwise they are sensitive to parasitic replicators. We also discuss, rather inconclusively, the possibility that, even in the absence of compartments, cooperation might evolve, by a processes analogous to kin selection, if the components of the hypercycle were confined to a surface. Finally, we discuss an alternative model, the stochastic corrector model. This also depends on the existence of compartments, but emphasizes the importance of stochastic effects arising if there are small numbers of each kind of molecule in a compartment. Essentially, small numbers serve to generate variation upon which selection can act.