Pollinator-driven ecological speciation in plants: new evidence and future perspectives

The hypothesis that pollinators have been important drivers of angiosperm diversity dates back to Darwin, and remains an important research topic today. Mounting evidence indicates that pollinators have the potential to drive diversification at several different stages of the evolutionary process. Microevolutionary studies have provided evidence for pollinator-mediated floral adaptation, while macroevolutionary evidence supports a general pattern of pollinator-driven diversification of angiosperms. However, the overarching issue of whether, and how, shifts in pollination system drive plant speciation represents a critical gap in knowledge. Bridging this gap is crucial to fully understand whether pollinator-driven microevolution accounts for the observed macroevolutionary patterns. Testable predictions about pollinator-driven speciation can be derived from the theory of ecological speciation, according to which adaptation (microevolution) and speciation (macroevolution) are directly linked. This theory is a particularly suitable framework for evaluating evidence for the processes underlying shifts in pollination systems and their potential consequences for the evolution of reproductive isolation and speciation. This Viewpoint paper focuses on evidence for the four components of ecological speciation in the context of plant-pollinator interactions, namely (1) the role of pollinators as selective agents, (2) floral trait divergence, including the evolution of pollination ecotypes, (3) the geographical context of selection on floral traits, and (4) the role of pollinators in the evolution of reproductive isolation. This Viewpoint also serves as the introduction to a Special Issue on Pollinator-Driven Speciation in Plants. The 13 papers in this Special Issue range from microevolutionary studies of ecotypes to macroevolutionary studies of historical ecological shifts, and span a wide range of geographical areas and plant families. These studies further illustrate innovative experimental approaches, and they employ modern tools in genetics and floral trait quantification. Future advances to the field require better quantification of selection through male fitness and pollinator isolation, for instance by exploiting next-generation sequencing technologies. By combining these new tools with strategically chosen study systems, and smart experimental design, we predict that examples of pollinator-driven speciation will be among the most widespread and compelling of all cases of ecological speciation.