Coevolution of reproducers and replicators at the origin of life and the conditions for the origin of genomes

Abstract There are two fundamentally distinct but inextricably linked types of biological evolutionary units, reproducers and replicators. Reproducers are cells and organelles that reproduce via various forms of division and maintain the physical continuity of compartments and their content. Replicators are genetic elements (GE), including genomes of cellular organisms and various autonomous elements, that both cooperate with reproducers and rely on the latter for replication. All known cells and organisms comprise a union between replicators and reproducers. We explore a model in which cells emerged via symbiosis between primordial ‘metabolic’ reproducers (protocells) which evolved, on short time scales, via a primitive form of selection and random drift, and mutualist replicators. Mathematical modeling identifies the conditions, under which GE-carrying protocells can outcompete GE-less ones, taking into account that, from the earliest stages of evolution, replicators split into mutualists and parasites. Analysis of the model shows that, for the GE-containing protocells to win the competition and to be fixed in evolution, it is essential that the birth-death process of the GE is coordinated with the rate of protocell division. At the early stages of evolution, random, high-variance cell division is advantageous compared to symmetrical division because the former provides for the emergence of protocells containing only mutualists, preventing takeover by parasites. These findings illuminate the likely order of key events on the evolutionary route from protocells to cells that involved the origin of genomes, symmetrical cell division and anti-parasite defense systems. Significance The origin of life, which is equivalent to the origin of cells, is arguably the greatest enigma in biology. The remarkable complexity characteristic of even the simplest extant cells could only evolve from simpler, pre-biological entities. Reconstructing that pre-cellular stage of evolution is a hard challenge. We present an evolutionary scenario in which cells evolved via symbiosis between protocells that harbored protometabolic reaction networks, could divide and were subject to selection, but lacked genomes, and primordial genetic elements. Mathematical modeling reveals conditions for the survival of such symbionts and the origin of modern-type genomes, in particular, coordination of the rates of protocell division and replication of genetic elements as well as random division of protocells.