High ratio of illegitimate visitation by small bees severely weakens the potential function of heteranthery

Aims In heterantherous plants, 'division of labor' among structurally different stamens, i.e. pollinating and feeding functions, has been thought to reduce the evolutionary conflict of relying on pollen both as the carrier of male gametes and as the food for pollinators. The key to successful division of labor among different sets of stamens is the size match between stamens and legitimate pollinators, which results in the precise deposition of pollen onto specific locations on pollinator's body and facilitates cross pollination. However, the potential impact of small illegitimate insects that are ubiquitous during the pollination process on the plant reproduction in heterantherous species has been largely neglected in previous studies and never been demonstrated experimentally. Methods Here, we investigated the functions of three different types of stamens in Commelina communis. The pollinator visitation, pollen removal and deposition were compared among flowers with different types of anthers emasculated at two natural populations. Moreover, the mating systems of C. communis in wild populations were estimated using microsatellite markers. Important Findings Our data showed that the main floral visitors for C. communis at the two studied populations were small illegitimate bees rather than legitimate pollinators, accounting for 77.5 and 92.2% of total flower visits, respectively. Flower manipulations in C. communis demonstrated that the two types of brightly yellow stamens separately functioned as 'deceptive attraction' and 'feeding' functions. Although the brown inconspicuous stamens of C. communis with the largest amount of fertile pollen had the potential function in offering pollen for cross pollination, the high ratio of illegitimate visitation by small bees significantly affected the dispersal and deposition of pollen from the pollinating anthers, and subsequently decreased the levels of outcrossing (t(m) = 0.23-0.32) in wild populations. Our work further confirmed that the size match between pollinators and the floral morphology is the prerequisite to successfully fulfill the functional differentiation among different sets of stamens in heterantherous plants. Local high ratio of illegitimate visitation by size unmatched insects could significantly weaken the potential functions of heteranthery, affecting the dispersal and deposition of functional pollen in heterantherous plants and further the whole mating systems.