To buzz or to sip: Asymmetric pollination effectiveness hints at the evolutionary transition of floral rewards

Evolutionary transitions between floral reward types, such as the repeated loss of nectar, are common across angiosperms, yet the ecological mechanisms driving these shifts remain poorly understood. In Pedicularis, the evolutionary loss of nectar is hypothesized to be associated with shifts to buzz pollination. However, empirical comparisons of pollination effectiveness between nectar- and pollen-foraging behaviours within a single transitional system are largely lacking.

We investigated Pedicularis alaschanica and its principal pollinator, Bombus friseanus, in the Hengduan Mountains. This plant represents a transitional evolutionary state, as it possesses a beak for specialized pollen delivery but still secretes copious nectar. This novel and unique system allows for a direct comparison of two distinct intraspecific foraging behaviours performed by the same bee species: upright nectar feeding (dorsal contact) versus vibratile pollen collection (ventral contact/buzz pollination). We quantified floral traits, nectar dynamics, single-visit pollen removal and deposition, and assessed the plant's breeding system and natural pollen limitation.

We confirmed and quantified the nectar properties of this transitional species, revealing distinct nectar secretion dynamics. While single-visit pollen removal did not differ significantly between the two foraging behaviours, buzz-pollinating visits were significantly more time-efficient and deposited on average more than twice as many pollen grains on stigmas compared to nectar-foraging visits. Breeding system experiments revealed that P. alaschanica is a partially self-incompatible outcrosser, and its natural seed set is not pollen-limited.

Our study revealed a marked functional asymmetry in pollen transfer driven by intraspecific behavioral variation among pollinators. In a non-pollen-limited system, the superior per-visit pollen deposition achieved by buzz-pollinating bees likely enhances male siring success. This high effectiveness likely relaxes the selective pressure to maintain metabolically costly nectar. Our findings provide a compelling mechanistic explanation for the repeated evolutionary loss of floral nectar.