Horizontal gene transfer (HGT) is a major factor in the evolution of prokaryotes. An intriguing question is whether HGT is maintained during evolution of prokaryotes owing to its adaptive value or is a byproduct of selection driven by other factors such as consumption of extracellular DNA (eDNA) as a nutrient. One hypothesis posits that HGT can restore genes inactivated by mutations and thereby prevent stochastic, irreversible deterioration of genomes in finite populations known as Muller’s ratchet. To examine this hypothesis, we developed a population genetic model of prokaryotes undergoing HGT via homologous recombination. Analysis of this model indicates that HGT can prevent the operation of Muller’s ratchet even when the source of transferred genes is eDNA that comes from dead cells and on average carries more deleterious mutations than the DNA of recipient live cells. Moreover, if HGT is sufficiently frequent and eDNA diffusion sufficiently rapid, a subdivided population is shown to be more resistant to Muller’s ratchet than an undivided population of an equal overall size. Thus, to maintain genomic information in the face of Muller’s ratchet, it is more advantageous to partition individuals into multiple subpopulations and let them “cross-reference” each other’s genetic information through HGT than to collect all individuals in one population and thereby maximize the efficacy of natural selection. Taken together, the results suggest that HGT could be an important condition for the long-term maintenance of genomic information in prokaryotes through the prevention of Muller’s ratchet.

Multilevel selection has been indicated as an essential factor for the evolution of complexity in interacting RNA-like replicator systems. There are two types of multilevel selection mechanisms: implicit and explicit. For implicit multilevel selection, spatial self-organization of replicator populations has been suggested, which leads to higher level selection among emergent mesoscopic spatial patterns (traveling waves). For explicit multilevel selection, compartmentalization of replicators by vesicles has been suggested, which leads to higher level evolutionary dynamics among explicitly imposed mesoscopic entities (protocells). Historically, these mechanisms have been given separate consideration for the interests on its own. Here, we make a direct comparison between spatial self-organization and compartmentalization in simulated RNA-like replicator systems. Firstly, we show that both mechanisms achieve the macroscopic stability of a replicator system through the evolutionary dynamics on mesoscopic entities that counteract that of microscopic entities. Secondly, we show that a striking difference exists between the two mechanisms regarding their possible influence on the long-term evolutionary dynamics, which happens under an emergent trade-off situation arising from the multilevel selection. The difference is explained in terms of the difference in the stability between self-organized mesoscopic entities and externally imposed mesoscopic entities. Thirdly, we show that a sharp transition happens in the long-term evolutionary dynamics of the compartmentalized system as a function of replicator mutation rate. Fourthly, the results imply that spatial self-organization can allow the evolution of stable folding in parasitic replicators without any specific functionality in the folding itself. Finally, the results are discussed in relation to the experimental synthesis of chemical Darwinian systems and to the multilevel selection theory of evolutionary biology in general. To conclude, novel evolutionary directions can emerge through interactions between the evolutionary dynamics on multiple levels of organization. Different multilevel selection mechanisms can produce a difference in the long-term evolutionary trend of identical microscopic entities.