Heteranthery in Clarkia: pollen performance of dimorphic anthers contradicts expectations

Abstract

PREMISE OF THE STUDY:Wild plant species that require the services of pollen-feeding insects for reliable pollination may evolve features that attract and reward their mutualistic partners. Heterantherous species have been proposed to exhibit a "division of labor" whereby "feeding anthers" (which produce pollen that may be consumed by an insect) are distinguished from "reproductive anthers" (which produce pollen more likely to contribute to reproduction). In some heterantherous species, including Clarkia unguiculata (Onagraceae), these two anther types differ with respect to stamen length, anther size, pollen production, and pollen color. METHODS:The primary goal of this study was to test one component of the "division of labor" hypothesis by comparing the performance of the pollen produced by each type of anther in C. unguiculata. To achieve this goal, under greenhouse conditions, we hand pollinated and assessed pollen performance (using epifluorescence microscopy) within ~228 flowers.KEY RESULTS: The pollen produced by the two anther types differed significantly with respect to both stigma and style penetration. The inner series of anthers produce pollen with higher performance than the outer series of longer, dark red anthers. CONCLUSIONS: These findings contradict previous descriptions of the genus, reporting that the inner diminutive series of anthers in Clarkia produce "abortive and nonfunctional" pollen. We outline the future research required to demonstrate the ecological function of heteranthery in this iconic wildflower group.

Climate Predicts UV Floral Pattern Size, Anthocyanin Concentration, and Pollen Performance in Clarkia unguiculata

“…Future studies should examine anthocyanin concentration of the anthers and pollen grains themselves to determine if these pigments offer a direct protective function in high UV environments (Koski and Galloway, 2018). The results presented here also corroborate previous reports of significant differences in pollen performance between the dimorphic anthers of C. unguiculata (Peach and Mazer, 2019).…”

“…The flowers of C. unguiculata are hermaphroditic and protandrous (i.e., anther maturity precedes stigma receptivity), and each flower bears two whorls of dimorphic stamens. The inner whorl is smaller, shorter and often white; the outer whorl is several millimeters longer, matures later, and bears anthers that range from dark red to purple (Lewis and Lewis, 1955;Peach and Mazer, 2019). We classified the developmental stages of the flowers of C. unguiculata into three distinct phases: male stage 1 (when the short anthers release their pollen), male stage 2 (when the long anthers release their pollen), and female (stage 3, when the stigma becomes receptive).…”

“…We quantified pollen performance by determining the proportion of these pollen grains that penetrated the stigma surface (PSP, proportion stigma penetrance) and the proportion whose tubes successfully grew to a distance of 4.5mm down the style (P4.5, the proportion of tubes to reach 4.5mm from the stigma surface) within the 4-hour post-pollination period. We selected 4.5mm because it represents ∼25% of the mean style length of this species (Peach and Mazer, 2019). We were able to quantify these metrics by examining the aniline blue stained stigma and style under a fluorescence microscope (with a DAPI filter) and counting the number of callose plugs deposited in the specified region of the pistil (cf.…”

Sex‐specific floral attraction traits in a sequentially hermaphroditic species

“…Five to seven days after stage 2, the stigma becomes receptive (stage 3). We divided the male phase into two distinct stages because in C. unguiculata the inner whorl of anthers (stage 1) produces pollen with significantly higher performance than the outer whorl (Peach & Mazer, ). Heterantherous species such as C. unguiculata have been proposed to exhibit a “division of labor” whereby “feeding anthers” (which produce pollen that may be consumed by an insect) are distinguished from “reproductive anthers” (which produce pollen more likely to contribute to reproduction).…”

Darwin's vexing contrivance: a new hypothesis for why some flowers have two kinds of anther

“…Yet we noticed that heterantherous species tend to release pollen from inner and outer anther whorls at different times and rates, making division of labour between feeding and pollinating functions unlikely, since the putative pollinating anthers are not yet mature when the feeding anthers would be attracting and rewarding bees. Moreover, in the only investigation of heteranthery in Clarkia, pollen from the inconspicuously coloured outer anthers, which putatively specialize on pollinating, was found to pollinate more poorly, in terms of stigma penetration and pollen tube growth [17]. Instead of dividing labour between pollinating and feeding functions during a bee visit, we propose that the inconspicuous colour and deflection of the outer anther whorl make it cryptic until the conspicuous inner whorl has dehisced, at which point the outer anthers move to the center of the flower and gradually release pollen.…”