Stochastic Modeling of Gene Expression Evolution Uncovers Tissue- and Sex-Specific Properties of Expression Evolution in the Drosophila Genus

Gene expression evolution is typically modeled with the stochastic Ornstein-Uhlenbeck (OU) process. It has been suggested that the estimation of within-species variations using replicated data can increase the predictive power of such models, but this hypothesis has not been fully tested. We developed EvoGeneX, a computationally efficient implementation of the OU-based method that models within-species variation. Using extensive simulations, we show that modeling within-species variations and appropriate selection of species improve the performance of the model. Further, to facilitate a comparative analysis of expression evolution, we introduce a formal measure of evolutionary expression divergence for a group of genes using the rate and the asymptotic level of divergence. With these tools in hand, we performed the first-ever analysis of the evolution of gene expression across different body-parts, species, and sexes of the Drosophila genus. We observed that genes with adaptive expression evolution tend to be body-part specific, whereas the genes with constrained evolution tend to be shared across body-parts. Among the neutrally evolving gene expression patterns, gonads in both sexes have higher expression divergence relative to other tissues and the male gonads have even higher divergence than the female gonads. Among the evolutionarily constrained genes, the gonads show different divergence patterns, where the male gonads, and not the female gonads, show less constrained divergence than other body-parts. Finally, we show interesting examples of adaptive expression evolution, including adaptation of odor binding proteins.