Beyond the Grant-Stebbins model: floral adaptive landscapes and plant speciation.

Background: Floral diversity, a striking feature of angiosperm evolution, provides the impetus and rationale for linking pollinator-driven selection to speciation processes. Perhaps the most widely adopted model for pollinator-driven speciation is the Grant-Stebbins model, in which plant populations locally adapt to the most effective pollinator, leading to floral ecotype formation and, eventually, reproductive isolation and speciation. However, modelling and empirical studies suggest that populations need not adapt to the most effective pollinator, and major floral transitions remain poorly explained.

Scope: We evaluate the Grant-Stebbins model, focusing especially on the most effective pollinator principle. We use floral adaptive landscapes to articulate a more complete and accurate framework for understanding floral adaptation, starting with the premise that plants evolve to maximize fitness. We highlight ways to improve the assessment of pollinator fitness functions, both singly and in combination. We show how floral adaptive landscapes can be used to describe processes of floral adaptation within populations, evolutionary transitions between floral phenotypes, and a variety of real-world situations that do not fit neatly under the Grant-Stebbins model. Finally, we evaluate how floral adaptive landscapes can clarify the role of pollination in speciation under a variety of species concepts.

Conclusions: The Grant-Stebbins model, while inspiring decades of empirical studies, is a caricature of pollinator-driven speciation and explains only a limited range of adaptive outcomes. By using adaptive landscapes, we acknowledge that flowers are not adaptations to the most effective pollinator, but adaptations to maximize fitness, making evolutionary shifts between distinct floral phenotypes easier to understand in multi-pollinator environments. Finally, we argue that while pollinators often drive floral divergence, speciation most likely results from simultaneous divergence in multiple niche axes across a geographic range, which has been underemphasized in plant speciation research.