Parasites constrain within-population diversification while accelerating between-population divergence in an RNA replication system

Diversification of replicators from simple self-replicating RNA molecules is a major challenge in prebiotic evolution. In our previous evolution experiment using an RNA replication system derived from the Qβ phage, a single RNA species spontaneously diversified into multiple coexisting host and parasite RNA lineages through arms race dynamics, suggesting that host-parasite interactions may promote diversification in molecular replicator ecosystems. To test this idea more directly, we evolved six independent RNA populations under high-parasite and low-parasite conditions. High-parasite populations showed accelerated mutation fixation and greater sequence divergence between populations. However, contrary to expectation, host diversification within populations was limited under high-parasite conditions, whereas transient diversification into at most three host lineages occurred under low-parasite conditions. Sequence and biochemical analyses indicate that this diversification was consistent with relaxed selection among host RNAs that achieved similar replication yields under compartmentalized replication. In contrast, coexistence with parasites helped maintain high replication capacities by continuously imposing selection for improved replication. These results suggest that antagonistic host-parasite interactions help maintain functional activity and promote divergence between populations while constraining diversification within populations. Such opposing effects may have shaped the balance between functional optimization and diversification during early molecular evolution.