Hidden conflict in pollination and its implications for diversification

Abstract

Pollinator-driven selection plays an important role in flowering plant diversification. Different pollinator guilds (e.g., butterfly, hummingbird, bat) have different preferences for and performance on flowers, which in turn generates selective forces on plant evolution. In response to these selective forces, plants often evolve a suite of floral traits called a “pollination syndrome” to adapt to their most efficient pollinator guild. Therefore, floral traits which affect both the plant’s and the pollinator’s fitness are the key to understanding how plant-pollinator interaction influences diversification. I first examined the genetic basis of floral scent evolution in Mimulus, discovering that parallel loss-of-function in the OCIMENE SYNTHASE gene, whose protein product synthesizes a floral scent important for bumblebee attraction, can be explained by divergent selection by different pollinator guilds in different Mimulus taxa. This result adds support to the notion that pollinator-driven selection has a large impact on floral trait evolution and promotes plant speciation. Next, I employed a morphospace analysis approach to examine the fitness consequences of corolla shape variation on both plant and pollinator, through a combination of 3D-printing, electronic sensing, and machine vision. I found that corolla curvature variation can generate a conflict of evolutionary interest between plants and their hawkmoth pollinators as a consequence of the disparate requirements from pollination: efficient pollen transfer for the plant vs. efficient resource exploitation by the pollinator. Finally, I compared the fitness landscape of two different pollinator guilds – hummingbirds and hawkmoths – on a common set of flower shapes with variation in petal curvature and reflexing. I found that a conflict of interest also exists in hummingbird pollination. Taken together, pollinator specificity is an important ecological factor that influences flowering plant diversification, and the finding of a conflict of interest between plant and pollinator suggests that the framework used to understand diversification driven by antagonistic species interactions can be extended to understanding diversification promoted by seemingly cooperative plant-pollinator interactions.