Evolution of funnel-revolver flowers and ornithophily in Nasa (Loasaceae)

Floral morphology, distribution, and flower visitors for 60 taxa of Nasa are investigated and compared to molecular trees inferred both from a combined marker analysis (ITS1 and trnL(UAA)) and from a single marker (ITS1). Flowers conform to two different floral types: Firstly, "tilt-revolver flowers", with spreading to reflexed, white to yellow petals and small, brightly coloured floral scales contrasting with the petals and firmly enclosing the nectar (Saccatae and Carunculatae); secondly, "funnel-revolver flowers", with half-erect to erect, orange to red petals and floral scales not contrasting with the petals, or enclosed in the corolla, and nectar freely accessible by funnel-shaped floral scales (Alatae, Grandiflorae, and N. venezuelensis species group). Phylogenetic analysis shows that "tilt-revolver flowers" represent the plesiomorphic condition by outgroup comparison. The two groups with tilt-revolver flowers in Nasa are not monophyletic (Saccatae are paraphyletic, Carunculatae are polyphyletic). Most Saccatae fall into two monophyletic assemblages, the N. poissoniana species group and the N. triphylla species group. The remainder of Saccatae group either with Grandiflorae (N. insignis species group) or with Alatae (N. taxa species group). The clades retrieved in the molecular analysis contradict the traditional classification, but are congruent with vegetative morphology, details of the flower morphology, and biogeography. "Funnel-revolver flowers" represent the derived condition, but molecular data suggest a convergent development (at least twice independently), since the corresponding species do not constitute a monophyletic group. "Tilt-revolver flowers" are visited and pollinated by bees (especially Colletidae), whereas "funnel-revolver flowers" are mostly visited by hummingbirds. The transition from melittophily to ornithophily may have been the license for the colonization of, and the diversification in, both cloud forest and high Andean habitats.