Pollinator foraging tactics have divergent consequences for the mating system of a tropical plant.

Resolving the consequences of pollinator foraging behaviour for plant mating systems is a fundamental challenge in evolutionary ecology. Pollinators may adopt particular foraging tactics: complete trapline foraging (repeated movements along a fixed route), sample-and-shift trapline foraging (a variable route that incorporates information from previous experiences) and territorial foraging (stochastic movements within a restricted area). Studies that integrate these pollinator foraging tactics with plant mating systems are generally lacking. We investigate the consequences of particular pollinator foraging tactics for Heliconia tortuosa. We combine parentage and sibship inference analysis with simulation modelling to: estimate mating system parameters; infer the foraging tactic adopted by the pollinators; and quantify the impact of pollinator foraging tactics on mating system parameters. We found high outcrossing rates, ubiquitous multiple paternity and a pronounced departure from near-neighbour mating. We also found that plants repeatedly receive pollen from a series of particular donors. We infer that the pollinators primarily adopt complete trapline foraging and occasionally engage in sample-and-shift trapline foraging. This enhances multiple paternity without a substantial increase in near-neighbour mating. The particular pollinator foraging tactics have divergent consequences for multiple paternity and near-neighbour mating. Thus, pollinator foraging behaviour is an important driver of the ecology and evolution of plant mating systems.

The Landscape Genetic Signature of Pollination by Trapliners: Evidence From the Tropical Herb, Heliconia tortuosa.

Animal-mediated pollination is essential for the maintenance of plant reproduction, especially in tropical ecosystems, where pollination networks have been thought to have highly generalized structures. However, accumulating evidence suggests that not all floral visitors provide equally effective pollination services, potentially reducing the number of realized pollinators and increasing the cryptic specialization of pollination networks. Thus, there is a need to understand how different functional groups of pollinators influence pollination success. Here, we examined whether patterns of contemporary pollen-mediated gene flow in Heliconia tortuosa are consistent with the foraging strategy of its territorial or traplining hummingbird pollinators. Territorial hummingbirds defend clumps of flowers and are expected to transfer pollen locally. In contrast, traplining hummingbirds forage across longer distances, thereby increasing pollen flow among forest fragments, and are thought to repeatedly visit particular plants. If trapliners indeed visit the same plants repeatedly along their regular routes, this could lead to a situation where neighboring plants sample genetically distinct pollen pools. To test this hypothesis, we genotyped 720 seeds and 71 mother plants from 18 forest fragments at 11 microsatellite loci. We performed TwoGener analysis to test pollen pool differentiation within sites (among neighboring plants within the same forest fragment: Φ SC ) and between sites (among forest fragments: Φ CT ). We found strong, statistically significant pollen pool differentiation among neighboring mother plants (Φ SC = 0.0506), and weaker, statistically significant differentiation among sites (Φ CT = 0.0285). We interpret this pattern of hierarchical pollen pool differentiation as the landscape genetic signature of the foraging strategy of traplining hummingbirds, where repeatable, long-distance, and high-fidelity routes transfer pollen among particular plants. Although H. tortuosa is also visited by territorial hummingbirds, our results suggest that these pollinators do not contribute substantially to successful pollination, highlighting differences in realized pollination efficiency. This cryptic reduction in the number of realized pollinators potentially increases the vulnerability of pollination success to the decline of populations of traplining hummingbirds, which have been shown to be sensitive to forest fragmentation. We conclude that maintaining habitat connectivity to sustain the foraging routes of trapliners may be essential for the maintenance of pollen-mediated gene flow in human-modified landscapes.