Fly wing evolution explained by a neutral model with mutational pleiotropy

Abstract

To what extent the speed of mutational production of phenotypic variation determines the rate of long-term phenotypic evolution is a central question in evolutionary biology. In a recent study, Houle et al. addressed this question by studying the mutational variation, microevolution, and macroevolution of locations of vein intersections on fly wings, reporting very slow phenotypic evolution relative to the rates of mutational input, high phylogenetic signals of these traits, and a strong, linear correlation between the mutational variance of a trait and its rate of evolution. Houle et al. examined multiple models of phenotypic evolution but found none consistent with all these observations. Here we demonstrate that the purported linear correlation between mutational variance and evolutionary divergence is an artifact. More importantly, patterns of fly wing evolution are explainable by a simple model in which the wing traits are neutral or neutral within a range of phenotypic values but their evolutionary rates are reduced because most mutations affecting these traits are purged owing to their pleiotropic effects on other traits that are under stabilizing selection. We conclude that the evolutionary patterns of fly wing morphologies are explainable under the existing theoretical framework of phenotypic evolution.