Evolution before genes

We cannot confirm previous claims that autocatalytic sets of organic polymer molecules could undergo evolution in any interesting sense by themselves. While we and others have previously imagined inhibition would result in selectability, we found that it produced multiple attractors in an autocatalytic set that cannot be selected for. Instead, we discovered that if general conditions are satisfied, the accumulation of adaptations in chemical reaction networks can occur. These conditions are the existence of rare reactions producing viable cores (analogous to a genotype), that sustains a molecular periphery (analogous to a phenotype).We conclude that only when a chemical reaction network consists of many such viable cores, can it be evolvable. When many cores are enclosed in a compartment there is competition between cores within the same compartment, and when there are many compartments, there is between-compartment competition due to the phenotypic effects of cores and their periphery at the compartment level. Acquisition of cores by rare chemical events, and loss of cores at division, allows macromutation, limited heredity and selectability, thus explaining how a poor man's natural selection could have operated prior to genetic templates. This is the only demonstration to date of a mechanism by which pre-template accumulation of adaptation could occur.This article was reviewed by William Martin and Eugene Koonin.There are two camps in the origin of life. The metabolism-first camp advocates consider improbable that RNA-like self-replicating polymers appeared before natural selection had operated on chemical networks [1-3], whereas genetics-first supporters find implausible the idea that molecular networks without genetic control could have undergone Darwinian evolution [4]. This Gordian knot was obviously cut on Earth around 3.5 billion years ago or even earlier [5]. A solution to the conundrum can be found in general evolutionary principles shared by some chemical