Pollination ecology and mating system of Solanum rostratum (Solanaceae) in North America

Abstract

Buzz-pollination or pollination by vibration occurs in several families of angiosperms including some important commercial crops such as potatoes and tomatoes. Buzz-pollinated flowers release pollen via small pores or slits on the anther’s tip that require the use of vibrations by specialized pollinators, usually bees, to remove the pollen. Some buzz-pollinated species have elaborate floral morphologies including dimorphic anthers within the same flower (heteranthery), and mirror-image flowers (enantiostyly) where the style is reciprocally deflected to either the left or right side of the floral axis. The complex floral morphology and buzz-pollination syndrome seen in these species require a close physical interaction between the sexual organs of the flowers and the bodies of insect visitors. Despite the broad taxonomic distribution of buzz-pollination in angiosperms (more than 60 families are buzz-pollinated) relatively few studies have described the pollination ecology of these species under natural conditions. The main goal of the present work was to characterize the pollination biology, mating patterns and antagonistic interactions (e.g. pollen theft) in natural populations of a buzz-pollinated species. For this purpose, I studied Solanum rostratum (Solanaceae), a buzz-pollinated, self-compatible, annual weed with complex floral morphology (both enantiostylous and heterantherous flowers). This species usually grows in disturbed areas in its native range (Mexico) and has become invasive around the world. My research was divided into three components. First, I characterized the pollination and reproductive biology of natural populations in Mexico. I performed floral manipulations in six natural populations of S. rostratum to estimate fruit and seed set. In three of these populations, I carried out 115 hours of pollinator observations and quantified the incidence of pollinators versus pollen thieves. I also measured the efficiency of a subset of floral visitors in triggering fruit set after single visits. Second, I investigated whether morphological correspondence between the size of the pollinator’s body and floral morphology influences pollen transfer. In experimental arrays, I exposed flowers of S. rostratum that varied in the distance between their sexual organs, to bumblebees (Bombus terrestris) of different sizes, and recorded pollen deposition and fruit and seed production. Finally, I determined the mating system (i.e. the proportion of self- and cross-fertilized offspring) of natural populations in Mexico and of introduced populations in the United States of America, using newly developed microsatellite markers. My results show that S. rostratum is visited by a wide range of bees of different sizes (0.9–9.8 mm in thorax diameter), but that only a small subset of these visitors act as pollinators. Most visitors act as pollen thieves, consuming pollen while effecting little or no pollination. I also found that correspondence between a pollinator’s size and the separation of the S. rostratum sexual organs determines pollen deposition and fruit production; pollen deposition decreased when bees were small relative to the distance between the sexual organs visited the flowers. My genetic analyses show that natural populations of S. rostratum maintain a relatively high outcrossing rate (tm = 0.75 ± 0.03) across the native and introduced range. Furthermore, genetic diversity is reduced in invasive populations, but this is not accompanied by changes in mating system. My work shows that the morphological fit between the pollinator and the flowers is important in determining the dynamics of pollen transfer and fruit production in this buzz-pollinated plant. Distinguishing between pollinators and pollen thieves in buzz-pollinated plants is essential for understanding the evolution of buzz-pollination, as pollen theft could be a major selective force for these species.