Genomic complexity places less restrictions on the evolution of young coexpression networks than protein-protein interactions

Abstract

The differences in evolutionary patterns of young protein-protein interactions (PPIs) among distinct species have long been a puzzle. However, based on our genome-wide analysis of available integrated experimental data, weconfirmthat young genes preferentially integrate into ancestral PPI networks, and that this manner is consistent in all of six model organisms with widely different levels of phenotypic complexity.We demonstrate that the level of restrictions placed on the evolution of biological networks declines with a decrease of phenotypic complexity. Compared with young PPI networks, new co-expression links have less evolutionary restrictions, soa younggenewitha high possibility tobe coexpressedotheryounggenes relatively frequentlyemergesinthefour simplergenomes among the six studied. However, it is not favorable for such young-young coexpression in terms of a young gene evolving into a coexpression hub, so the coexpression pattern could gradually decline. To explain this apparent contradiction,wesuggest that young genes that are initially peripheral to networks are temporarily coexpressed with other young genes, driving functional evolution because of lowselective pressure. However, as the expression levels of genes increase and they gradually develop a greater effect on fitness, younggenes start tobe coexpressedmore withmembers of ancestral networks andless withother younggenes.Ourfindings provide new insights into the evolution of biological networks.