Well-resolved phylogeny reveals multiple origins of keel flowers during the diversification of papilionoid legumes

The butterfly-shaped keel flowers are among the most successful pollination syndromes in angiosperms. These flowers steer the mechanical interaction with bees and thus are hypothesized to accelerate pollinator-driven diversification. The highly labile evolution of keel flowers in Papilionoideae (Fabaceae) provides a suitable system to test this hypothesis but a robust phylogeny is lacking.

Using 1,456 low-copy nuclear loci, we confidently resolve the early divergence history of Papilionoideae. Constrained by this backbone phylogeny, we generated a time tree for 3,326 Fabales to evaluate the tempo and mode of diversification within a state-dependent evolutionary framework.

The first keel flowers emerged around 59.0 Ma in Papilionoideae, predating the earliest fossil by 3–4 million years. The Miocene diversification of Papilionoideae coincided with rapid evolution of keel flowers. At least seven independent origins and twenty-seven losses of keel flowers were identified in Papilionoideae, Polygalaceae, and Cercidoideae during this time. 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 fixing and chemical defense as well as dispersal to the subtropical and temperate regions.