De-Darwinizing the proteome: the genome as the original germ line

Abstract

A hallmark of evolutionary transitions in individuality is the suppression of lower-level Darwinian dynamics through germ-soma specialization. The RNA world hypothesis posits that early life arose through ribozymes, RNA molecules that functioned as both catalysts and hereditary units, housed within protocells. This dual role is the chief appeal of the RNA world framework, because it makes ribozymes capable of open-ended Darwinian evolution. It is also its chief liability. Each ribozyme is a fully Darwinian entity: it replicates, accumulates mutations via Mullers ratchet, and can be displaced by selfish variants that replicate faster but contribute less to collective function. We show that between-protocell selection, even when strong, cannot overcome this within-cell evolutionary erosion, particularly as protocells evolve increased complexity by increasing the number of ribozyme types they contain. The origin of a low-copy-number informational RNA genome, translated by an ancient ribosome into protein enzymes, resolves this conflict by producing a functional workforce that is non-heritable. Protein-based enzymes are intrinsically stripped of evolutionary agency, confining heritable variation to the genome and entrenching the protocell as the primary level of Darwinian individuality. The genome, in this view, is not merely a storage device but the original germ line, and its origin marks the point at which cellular life became capable of open-ended growth in complexity.