Convergence and molecular evolution of floral fragrance after independent transitions to self–fertilization

Abstract

AbstractThe study of the independent evolution of similar characters can highlight important ecological and genetic factors that drive phenotypic evolution. The transition from reproduction by outcrossing to self-fertilization has occurred frequently throughout plant evolution. A common trend in this transition is the reduction of flower features in the selfing lineages, including display size, flower signals and pollinators’ rewards. These changes are believed to evolve because resources invested in building attractive flowers are reallocated to other fitness functions as the pressures to attract pollinators decrease. We investigated the similarities in the evolution of flower fragrance after independent transitions to self-fertilization in Capsella. We identified a large number of compounds that are similarly changed in different selfer lineages, such that the composition of the flower scent can predict the mating system in this genus. We further demonstrate that the emission of some of these compounds convergently evolved based on mutations in different genes. In one of the Capsella selfing lineages, the loss of β-ocimene emission was caused by a mutation altering subcellular localization of the ortholog of TERPENE SYNTHASE 2 without apparent effects on its biosynthetic activity. This mutation appears to have been selected at the early stage of this selfing lineage establishment through the capture of a variant segregating in the ancestral outcrossing population. The large extent of convergence in the independent evolution of flower scent, together with the evolutionary history and molecular consequences of a causal mutation, suggest that the emission of specific volatiles has important fitness consequences in self-fertilizing plants without obvious energetic benefits.