Repeated loss of floral scent in independent transitions from bee to hummingbird pollination in spiral gingers

Abstract

The repeated evolution of the same trait in different lineages provides powerful natural experiments to study the phenotypic and genotypic predictability of how traits are gained and lost. A fascinating example of this is the repeated evolution of hummingbird pollination in plant lineages in the Americas, a widespread and seemingly unidirectional phenomenon. The spiral gingers in the genus Costus are ancestrally bee-pollinated and hummingbird pollination has evolved multiple times independently in the tropical Americas. These pollinator transitions are accompanied by predictable morphological and color changes but the changes in floral scent have not been described. In this study, we describe the floral scent composition of 29 species of Costus sampled across the phylogeny to understand how floral scent has evolved across the genus with respect to pollinator transitions. We then combine transcriptomics and genomics in one clade of Costus to identify genetic expression differences and gene family evolution associated with pollinator transitions. We show that hummingbird-pollinated species have mostly lost their floral scent, whereas bee-pollinated species exhibit either floral scent maintenance or in some cases, gains of more diverse scent profiles. The remarkable consistency of scent loss in hummingbird-pollinated species highlights the shared strong selection pressures experienced by these lineages. Even species with more recent transitions from bee to hummingbird pollination exhibit scent loss, highlighting the rapid breakdown of scent production following pollinator transitions. We also find the floral scent loss appears to be due to gene downregulation rather than pseudogenization. This research highlights the capacity for rapid changes when selection pressures are strong through downregulation of floral scent genes.