Population Biology of the First Replicators: On the Origin of the Genotype, Phenotype and Organism

Prebiotic synthesis of short length macromolecules from precursor molecules results in a dynamic of spontaneous creation, which allows for growth from zero density. At this prereplicator stage in the evolution of life there is no life history, since the birth and death processes are intimately coupled through the physical chemistry of a single reaction. With the emergence of nonenzymatic, template-directed replication, the birth and death processes could diverge for the first time, since selection could act differently on the birth and death rates of the replicating molecule. Thus, with replication, natural selection and life-history evolution began. The genotype, or nucleotide sequence, of the replicating molecule gave rise to several phenotypic properties, the most important of which was its three-dimensional structure which in turn affected the birth and death processes. However, at this stage of nonenzymatic template replication, the phenotype was the physical structure of the genotype, nothing more: For the divergence of the phenotype from the genotype it was necessary for the replicator to produce a protein. It is shown here that the evolution of enzyme production is facilitated by the existence of population structure in the distribution of the macromolecules associated with replication. Initially, this structure was created passively by the localization of the macromolecules in rock crevices, suspended water droplets, etc. Ultimately, the replicator along with its proteins were localized in a protocellular structure and this became the first organism. Thus, initially, the organism was one extreme of the population structure of the macromolecules associated with life. The organism was the culmination of the encapsulation phase of evolution which proceeded through initial phases of passive localization.