Evolution of different adaptations for pollen uptake from flowers of Heliotropium (Boraginaceae) with narrow corolla tube in pollen wasps of the genus Celonites (Hymenoptera: Vespidae: Masarinae)

Abstract

The evolution of flower-visiting behaviour in pollen wasps remains poorly investigated. The females of oligolectic Celonites species show two fundamentally different behavioural patterns for pollen uptake from Heliotropium flowers with a narrow corolla tube. They remove pollen from the concealed anthers either with their forelegs or with their proboscis. Single-frame video analysis revealed that pollen collection with the proboscis consists of a hitherto unknown, unique, and stereotypic behavioural pattern. The first phylogenetic reconstruction of Celonites based on ultra-conserved elements demonstrates that this highly complex behaviour is presumably homologous and evolved only once. It probably derived from accidental consumption of pollen adhering to the proboscis during nectar uptake and is associated with morphological adaptations of the foretarsi and mouthparts. Pollen uptake with the forelegs evolved independently. Morphological adaptations to this type of pollen uptake are the elongation of the forelegs and a tarsal pollen brush formed by hooked setae. These results confirm for pollen wasps a view that has been developed in studies of bee–flower relationships, namely that pollen collection, contrary to nectar collection, is a specific and stereotypic behaviour that often requires morphological and behavioural adaptations, possibly underlying the high rate of specialization observed in pollen-collecting Hymenoptera.