Organ-specific propensity drives patterns of gene expression evolution

Abstract

The origins of multicellular physiology are tied to evolution of gene expression. Genes can shift expression as organisms evolve, but how ancestral expression influences altered descendant expression is not well understood. To examine this, we amalgamated 1,903 RNA-seq datasets from 182 research projects, including 6 organs in 21 vertebrate species. Quality control eliminated project-specific biases, and expression shifts were reconstructed using gene-family-wise phylogenetic Ornstein-Uhlenbeck models. Expression shifts following gene duplication result in more drastic changes in expression properties than shifts without gene duplication. The expression properties were tightly coupled with protein evolutionary rate, depending on whether and how gene duplication occurred. Fluxes in expression patterns among organs were nonrandom, forming modular connections which were reshaped by gene duplication. Thus, if expression shifted, ancestral expression in some organs induces a strong propensity for expression in particular organs in descendants. This supports a major role for what might be termed "preadaptive" pathways of gene expression evolution.