Genomics in the light of evolutionary transitions.

Molecular biology has entrenched the gene as the basic hereditary unit and genomes are often considered little more than collections of genes. However, new concepts and genomic data have emerged, which suggest that the genome has a unique place in the hierarchy of life. Despite this, a framework for the genome as a major evolutionary transition has not been fully developed. Instead, genome origin and evolution are frequently considered as a series of neutral or nonadaptive events. In this article, we argue for a Darwinian multilevel selection interpretation for the origin of the genome. We base our arguments on the multilevel selection theory of hypercycles of cooperative interacting genes and predictions that gene-level trade-offs in viability and reproduction can help drive evolutionary transitions. We consider genomic data involving mobile genetic elements as a test case of our view. A new concept of the genome as a discrete evolutionary unit emerges and the gene-genome juncture is positioned as a major evolutionary transition in individuality. This framework offers a fresh perspective on the origin of macromolecular life and sets the scene for a new, emerging line of inquiry--the evolutionary ecology of the genome.