Pollinator Shifts and Floral Evolution in the Merianieae

The angiosperms (flowering plants) are by far the largest and most diverse major plant lineage and it seems clear that the tremendous diversity of their flowers has evolved primarily in connection with their manifold animal pollinators. A particularly interesting topic located at the interface of pollination ecology and floral evolution is the occurrence of so-called pollinator shifts, i.e., the shift from one functional group of pollinators to another (e.g., from bees to birds). Although the importance of such pollinator shifts for understanding angiosperm diversification and evolution has long been recognized, there are only few studies linking micro- and macroevolutionary patterns. One important hypothesis holds that pollinator shifts are triggered by differences in pollinator efficiency among different types of pollinators. A pollinator shift usually affects a series of floral traits and specific trait combinations are often linked with specific functional groups of pollinators. Such trait combinations are commonly referred to as pollination syndromes. Bird-pollinated flowers, for example, are usually red, scent- less, and produce a lot of nectar. Hawkmoth pollinated flowers, on the other hand, are mostly white, strongly scented, and produce relatively little nectar. Although the concept of pollination syndromes is very intuitive and has been shown to be applicable in some plant lineages, it is still controversially debated. It appears that shifts in functional pollinator group are not always correlated with expected changes in pollination syndrome. Our study focuses on a group of Central- and South American plants (the tribe Merianieae) belonging to the melastome family (Melastomataceae). The Merianieae include bee-, bat-, hummingbird- as well as passerine pollinated species. This diversity in pollination systems will allow us to assess in detail the changes in floral traits associated with different functional groups of pollinators. In addition, using a population genetic approach, we will assess gene flow and pollination efficiency in the different pollination systems. The main hypothesis that we will test is that birds are more efficient pollinators and promote higher levels of outcrossing than bees under certain environmental conditions. In addition, we will challenge the concept of pollination syndromes and will test whether the concept holds up in Merianieae. We will apply field experiments for the assessment of pollination ecology, molecular tools for the characterization of population genetic structure, micro tomography for the analysis of floral morphology, and a morphospace approach for testing the validity of pollination syndromes. The novel combination of these state-of-the-art methods will provide a strong basis for future experimental work to elucidate drivers of pollinator shifts in Merianieae and will lead to a better understanding of pollinator shifts in general. Such studies are particularly important in tropical ecosystems, which are notoriously understudied and at the same time under ever increasing threat through human impact.

In the project "Pollinator shifts and flower evolution in the Merianieae" a team around Prof. Dr. Jürg Schönenberger and Dr. Agnes Dellinger from the University of Vienna investigated the evolutionary adaptations of flowers to different groups of pollinators. The tribe Merianieae from the plant family Melastomataceae is distributed across the tropics of Central and South America and contains around 300 species. The species are mostly shrubs and treelets and occur from lowland rainforests in the Amazon Basin to the cloud forests of the Andes. Most lowland species have small, white flowers, while species in the Andes show larger, colorful flowers with conspicuous stamens (the floral organs that produce pollen). Through extensive fieldwork in Ecuador and Costa Rica, the researchers could show that lowland species are exclusively pollinated by bees, while Andean Merianieae show repeated evolutionary pollinator shifts from bee to vertebrate pollination (e.g., hummingbirds, bats, rodents, tanagers). These pollinator shifts go along with marked morphological changes in the flowers, such as changes in flower shape (from open to pseudo-campanulate), changes in pollinator reward (pollen for bees, nectar or food bodies for vertebrates) and mechanisms of pollen release. In bee-pollinated Merianieae, for example, pollen can only be released through the application of special vibrations applied to flowers by bees. Vertebrates cannot produce comparable vibrations and do not actively collect pollen. Since the plants need to disperse pollen for reproduction, however, modifications in the stamens have evolved to release pollen differently, i.e., through an explosive bellows mechanism. Importantly, the researchers could show that such floral modifications happen partially independently of each other, possibly rendering high evolutionary flexibility to these flowers. The researchers could further demonstrate a strong link between pollinator shifts and climatic factors. Pollinator shifts only happened in Merianieae genera that occur in tropical mountains, which are characterized by cooler, rainier conditions than lowland rainforests. Using field experiments, Schönenberger and Dellinger could show that bees are less efficient pollinators than vertebrates under the unhostile montane climate impeding their activity as ectothermic pollinators. Additional molecular investigations revealed that vertebrates are more mobile pollinators than bees, linking plant populations more effectively over larger geographic distances, thereby reducing genetic differentiation among populations. Through this project, funded by the Austrian Science Fund, Schönenberger and Dellinger could establish Merianieae as novel study system for tropical biology and the evolution of the extraordinary biodiversity of the Neotropics. Currently, Dellinger is working on a follow-up project to resolve the evolutionary mechanisms and historic events (i.e., Andean uplift 12 million years ago) driving the diversification of Merianieae.