Pollinator identity and spatial isolation influence multiple paternity in an annual plant

Abstract

The occurrence and extent of multiple paternity is an important component of variation in plant mating dynamics. However, links between pollinator activity and multiple paternity are generally lacking, especially for plant species that attract functionally diverse floral visitors. In this study, we separated the influence of two functionally distinct floral visitors (hawkmoths and solitary bees) and characterized their impacts on multiple paternity in a self-incompatible, annual forb, Oenothera harringtonii (Onagraceae). We also situated pollinator-mediated effects in a spatial context by linking variation in multiple paternity to variation in plant spatial isolation. We documented pronounced differences in the number of paternal sires as function of pollinator identity: on average, the primary pollinator (hawkmoths) facilitated mating with nearly twice as many pollen donors relative to the secondary pollinator (solitary bees). This effect was consistent for both isolated and nonisolated individuals, but spatial isolation imposed pronounced reductions on multiple paternity regardless of pollinator identity. Considering that pollinator abundance and pollen dispersal distance did not vary significantly with pollinator identity, we attribute variation in realized mating dynamics primarily to differences in pollinator morphology and behaviour as opposed to pollinator abundance or mating incompatibility arising from underlying spatial genetic structure. Our findings demonstrate that functionally distinct pollinators can have strongly divergent effects on polyandry in plants and further suggest that both pollinator identity and spatial heterogeneity have important roles in plant mating dynamics.

The messenger matters: Pollinator functional group influences mating system dynamics

“…In comparison, solitary bees are much smaller, groom between floral visits, and when foraging pollen of O. harringtonii , do not necessary make contact with stigmas. Further, pollinator observations confirmed that visitation frequency and pollen dispersal distance did not differ between pollinator types, meaning that differences in paternity were likely due to pollinator behaviour and morphology (Rhodes et al., ). Using pollinator exclusion treatments and genetic analyses, the authors were able to isolate the effects of widely different pollinators, hawkmoths and bees, on multiple paternity.…”

“…Interestingly, Rhodes et al. () did not find significant biparental inbreeding in open‐pollinated treatments, but seed families from both hawkmoth‐ and bee‐pollinated seed families did have some biparental inbreeding. Understanding why exclusive pollinator types increase biparental inbreeding compared to open‐pollinated plants requires further investigation.…”

“…Rhodes et al. () demonstrate the importance of understanding the roles that functionally diverse pollinators play in mating system dynamics.…”

“…Rhodes, Fant, and Skogen () address this question in the Arkansas Valley evening primrose, Oenothera harringtonii , an endemic to the grasslands of Colorado. Oenothera harringtonii is visited by both hawkmoths and diurnal solitary bees, which exhibit different morphologies and foraging patterns (Figure ).…”

“…Oenothera harringtonii is visited by both hawkmoths and diurnal solitary bees, which exhibit different morphologies and foraging patterns (Figure ). Hawkmoths forage shortly after flowers open in the evening whereas bees visit flowers in the morning before senescence (Rhodes et al., ; Skogen et al., ). Hawkmoths are not only larger‐bodied, but forage deep into the corolla in search of nectar and do not groom pollen between foraging bouts.…”