On the specificity of gene regulatory networks: How does network co-option affect subsequent evolution?

Abstract

The process of multicellular organismal development hinges upon the specificity of developmental programs: for different parts of the organism to form unique features, processes must exist to specify each part. This specificity is thought to be hardwired into gene regulatory networks, which activate cohorts of genes in particular tissues at particular times during development. However, the evolution of gene regulatory networks sometimes occurs by mechanisms that sacrifice specificity. One such mechanism is network co-option, in which existing gene networks are redeployed in new developmental contexts. While network co-option may offer an efficient mechanism for generating novel phenotypes, losses of tissue specificity at redeployed network genes could restrict the ability of the affected traits to evolve independently. At present, there has not been a detailed discussion regarding how tissue specificity of network genes might be altered due to gene network co-option at its initiation, as well as how trait independence can be retained or restored after network co-option. A lack of clarity about network co-option makes it more difficult to speculate on the long-term evolutionary implications of this mechanism. In this review, we will discuss the possible initial outcomes of network co-option, outline the mechanisms by which networks may retain or subsequently regain specificity after network co-option, and comment on some of the possible evolutionary consequences of network co-option. We place special emphasis on the need to consider selectively-neutral outcomes of network co-option to improve our understanding of the role of this mechanism in trait evolution.