Well-resolved phylogeny supports repeated evolution of keel flowers as a synergistic contributor to papilionoid...

The butterfly-shaped keel flower is a highly successful floral form in angiosperms. These flowers steer the mechanical interaction with bees and thus are hypothesized to accelerate pollinator-driven diversification. The exceptionally labile evolution of keel flowers in Papilionoideae (Fabaceae) provides a suitable system to test this hypothesis. Using 1456 low-copy nuclear loci, we confidently resolve the early divergence history of Papilionoideae. Constrained by this backbone phylogeny, we generated a time tree for 3326 Fabales to evaluate the tempo and mode of diversification within a state-dependent evolutionary framework. The first keel flowers emerged c. 59.0 million years ago in Papilionoideae, predating the earliest fossil by 3-4 million years. The Miocene diversification of Papilionoideae coincided with the rapid evolution of keel flowers. At least six independent origins and 32 losses of keel flowers were identified in Papilionoideae, Cercidoideae, and Polygalaceae. However, the state-dependent diversification model was not favored. Lack of radiation associated with keel flowers suggests that diversification within Papilionoideae was not solely driven by pollinator-mediated selection, but instead an outcome of the synergistic effects of multiple innovations, including nitrogen fixation and chemical defense, as well as dispersal into subtropical and temperate regions.