Low bee visitation rates explain pollinator shifts to vertebrates in tropical mountains

Evolutionary shifts from bee to vertebrate pollination are common in tropical mountains. Reduction in bee pollination efficiency under adverse montane weather conditions was proposed to drive these shifts. Although pollinator shifts are central to the evolution and diversification of angiosperms, we lack experimental evidence of the ecological processes underlying such shifts. Here, we combine phylogenetic and distributional data for 138 species of the Neotropical plant tribe Merianieae (Melastomataceae) with pollinator observations of 11 and field pollination experiments of six species to test whether the mountain environment may indeed drive such shifts. We demonstrate that shifts from bee to vertebrate pollination coincided with occurrence at high elevations. We show that vertebrates were highly efficient pollinators even under the harsh environmental conditions of tropical mountains, whereas bee pollination efficiency was lowered significantly through reductions in flower visitation rates. Furthermore, we show that pollinator shifts in Merianieae coincided with the final phases of the Andean uplift and were contingent on adaptive floral trait changes to alternative rewards and mechanisms facilitating pollen dispersal. Our results provide evidence that abiotic environmental conditions (i.e. mountain climate) may indeed reduce the efficiency of a plant clade's ancestral pollinator group and correlate with shifts to more efficient new pollinators.