Drift and directional selection are the evolutionary forces driving gene expression divergence in eye and brain tissue ofHeliconiusbutterflies

Abstract

AbstractInvestigating gene expression evolution over micro- and macroevolutionary timescales will expand our understanding of the role of gene expression in adaptation and speciation. In this study, we characterized which evolutionary forces are acting on gene expression levels in eye and brain tissue of fiveHeliconiusbutterflies with divergence times of ~5-12 MYA. We developed and applied Brownian motion and Ornstein-Uhlenbeck models to identify genes whose expression levels are evolving through drift, stabilizing selection, or a lineage-specific shift. We find that 81% of the genes evolve under genetic drift. When testing for branch-specific shifts in gene expression, we detected 368 (16%) shift events. Genes showing a shift towards up-regulation have significantly lower gene expression variance than those genes showing a shift leading towards down-regulation. We hypothesize that directional selection is acting in shifts causing up-regulation, since transcription is costly. We further uncover through simulations that parameter estimation of Ornstein-Uhlenbeck models is biased when using small phylogenies and only becomes reliable with phylogenies having at least 50 taxa. Therefore, we developed a new statistical test based on Brownian motion to identify highly conserved genes (i.e., evolving under strong stabilizing selection), which comprised 3% of the orthoclusters. In conclusion, we found that drift is the dominant evolutionary force driving gene expression evolution in eye and brain tissue inHeliconius. Nevertheless, the higher proportion of genes evolving under directional than under stabilizing selection might reflect species-specific selective pressures on vision and brain necessary to fulfill species-specific requirements.