Exceptional diversification of floral form in a specialized orchid pollination system

Abstract

Abstract Traits that facilitate specialized interactions, such as those in flowers that promote pollination, are often invoked as targets of stabilizing selection across macroevolutionary timescales. However, the diversity of pollination mechanisms across flowering plants begs further investigation into the generality of this pattern. We fit a model of multivariate character evolution on a dataset of 140 orchid species sampled across 65 genera from the diverse neotropical Cymbidieae clade to characterize the role of pollination mode on the pace of flower shape evolution. We find that, contrary to the expectation of pollinator-mediated stabilizing selection causing stasis, orchids pollinated by specialized scent-collecting male euglossine bees (“perfume flowers” sensu (1, 2)) exhibit elevated rates of floral evolution compared to plants utilizing other rewarding or deceptive mechanisms. This pattern is recapitulated across at least 5 independent origins of this pollination system amidst a complex backdrop of background rate evolution. The rapid rates of change we observed in perfume flowers may be facilitated by weak evolutionary coupling between functional regions in their flowers, allowing for independent trajectories of evolution. Our results provide novel insights into the capacity for pollinators to generate selective pressures on flowers at macroevolutionary scales, providing an engine for trait diversification in some of the world’s most floristically rich regions.