Evolutionary Conflict Leads to Innovation: Symmetry Breaking in a Spatial Model of RNA-Like Replicators

Abstract

Molecules that replicate in trans are vulnerable to evolutionary extinction because they decrease the catalysis of replication to become more available as a template for replication. This problem can be alleviated with higher-level selection that clusters molecules of the same phenotype, favouring those groups that contain more catalysis. Here, we study a simple replicator model with implicit higher-level selection through space. We ask whether the functionality of such system can be enhanced when molecules reproduce through complementary replication, representing RNA-like replicators. For high diffusion, symmetry breaking between complementary strands occurs: one strand becomes a specialised catalyst and the other a specialised template. In ensemble, such replicators can modulate their catalytic activity depending on their environment, thereby mitigating the conflict between levels of selection. In addition, these replicators are more evolvable, facilitating survival in extreme conditions (i.e., for higher diffusion rates). Our model highlights that evolution with implicit higher-level selection—i.e., as a result of local interactions and spatial patterning—is very flexible. For different diffusion rates, different solutions to the selective conflict arise. Our results support an RNA World by showing that complementary replicators may have various ways to evolve more complexity.

The origin of the central dogma through conflicting multilevel selection

“…Consequently, selection operated at both cellular and molecular levels, and selection at one level was potentially in conflict with selection at the other [8,9]. Previous studies have demonstrated that such conflicting multilevel selection can induce a partial and primitive distinction between genomes and enzymes in replicating molecules [10,11]. Specifically, the molecules undergo catalytic symmetry breaking between their complementary strands, whereby one strand becomes catalytic and the other becomes non-catalytic.…”

Kin Selection in the RNA World

“… In the extreme case in which cooperative RNAs receive no benefits ( ), the ESS value of cooperation is capped at 0.5, and only partial cooperation can evolve, because complete cooperation would mean that there were no individuals available to receive benefits. This applies, for example, in some RNA trans-replicases, in which becoming a replicase enzyme prevents individuals from being replicated by other replicases [ 16 , 44 ]. This result is analogous to the result obtained in Frank’s (1997) model of paired sibling suicide in animals [ 45 ].…”

“…This result is analogous to the result obtained in Frank’s (1997) model of paired sibling suicide in animals [ 45 ]. This suggests that the evolution of the cooperative enzyme that cannot receive benefits (as in [ 16 , 24 , 44 ]) is analogous to the evolution of sterility in higher organisms.…”