Floral evolution and male reproductive success: Optimal dispensing schedules for pollen dispersal by animal-pollinated plants

Summary Selection favouring an outcrossing plant's ability to sire seeds generally promotes floral characters that increase (1) the frequency of pollinator visits, (2) the number of pollen grains dispersed to other plants by each pollinator and (3) the probability of a pollen grain successfully fertilizing an ovule after reaching a stigma. Flowers influence pollen dispersal and fertilization probabilities by determining the pattern of pollen removal during a series of visits (dispensing schedule). We model male reproductive success to identify optimal dispensing schedules, which characteristically involve monotonic increases in the proportion of remaining pollen removed during successive visits. These schedules balance the benefits of restricted removal, which counteracts the diminishing returns associated with animal pollination (e.g. pollinator grooming, local mate competition), with the advantages of increased removal to avoid time-dependent losses in fertilization ability (e.g. pollen precedence, declining viability). Because pollinator availability mediates this balance, the most effective dispensing schedule allows dynamic adjustment of removal to the prevailing frequency of visits experienced by individual plants. As an example of such dynamic removal we demonstrate that the dispensing mechanism ofLupinus sericeus flowers allows facultative adjustment of removal to the interval between visits. Because optimal control of pollen removal can increase a plant's mating opportunities by an order of magnitude, dispensing mechanisms should be a common component of floral design.     

Stability of floral specialization in Trollius europaeus in contrasting ecological environments

Specialization of some plants on seed‐eating pollinators is intriguing, especially when co‐pollinators exclusively feeding on nectar are also present. We examined the stability of the morphological specialization of Trollius europaeus (L.) globeflowers with respect to Chiastocheta (Pokorny) flies by artificially opening the flowers. In the montane and subalpine environments studied, other visitors contributed 2% and 28% of all the visits, respectively, and visited open flowers nearly eight times more often than closed flowers, but in both environments their contribution to pollination did not compensate for Chiastocheta aversion against open phenotypes. Net seed set (female success) was slightly higher (+4%) and pollen export (male success) was much higher (+85%) for closed than open flowers. Selection in favour of the closed phenotype was even more intense in patches where open phenotypes were most common, precluding the evolution of open flowers in the study populations.     

Highly efficient pollination by bumblebees ensures seed production in Pedicularis lachnoglossa (Orobanchaceae), an early-flowering Himalayan plant

Pedicularis (Orobranchaceae) is a common high altitude genus of the Himalayas that may be affected by pollination limitation.Using Pedicularis lachnoglossa from Yulong (Jade Dragon) Snow Mountain in Li...     

Pollinator‐mediated phenotypic selection does not always modulate flower size and number in the large‐flowered Mediterranean shrub Cistus ladanifer (Cistaceae)

Flower size and number usually evolve under pollinator‐mediated selection. However, hot, dry environments can also modulate display, counteracting pollinator attraction. Increased pollen deposition on larger flower displays may not involve higher female fitness. Consequently, stressful conditions may constrain flower size, favouring smaller‐sized flowers. The large‐flowered, self‐incompatible Mediterranean shrub Cistus ladanifer was used to test that: (1) this species suffers pollen limitation; (2) pollinators are spatially–temporally variable and differentially visit plants with more/larger flowers; (3) increased visits enhance reproduction under pollen limitation; (4) stressful conditions reduce female fitness of larger displays; and (5) phenotypic selection on floral display is not just pollinator‐mediated. We evaluated pollen limitation, related floral display to pollinator visits and fruit and seed production and estimated phenotypic selection. Flower size was 7.2–10.5 cm and varied spatially–temporally. Visitation rates (total visits/50 min) ranged from 0.26 to 0.43 and increased with flower size. Fruit set averaged 80% and seed number averaged 855, but only fruit set varied between populations and years. Selection towards larger flowers was detected under conditions of pollen limitation. Otherwise, we detected stabilizing selection on flower size and negative selection on flower number. Our results suggest that selection on floral display is not only pollinator‐dependent through female fitness in C. ladanifer. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 176 , 540–555.     

A two-pollinator model for the evolution of floral complexity

For a new, more complex floral form to become established in a population it must overcome the problem of frequency-dependent constancy to successfully attract pollinators. This may be achieved by complex floral forms offering absolute greater rewards than the simpler forms, or by complex flowers offering a higher probability of being rewarding because fewer pollinators are able to visit them. In this paper we examine the effect of three pollinator foraging strategies on the ratio of flights within and between floral morphs and hence on the probability of a new morph establishing in a population without offering a greater reward. We incorporate pollinator behaviour based around observations of two pollinator species systems into three models of competition for pollinators. In the first model the constancy of the pollinator of the new floral morph is a function only of the foraging strategy of the existing pollinator of the original floral morph. In the next model the constancy of the second pollinator is determined by the number of rewarding flowers of each floral morph left by the original pollinator and in the third model it is determined by the ratio of rewarding flowers of each morph left by the original pollinator. The results demonstrate that under conditions of intense competition for pollinators, new, more complex floral forms are indeed able to attract high levels of constant pollinators without offering intrinsically higher rewards. However, for this to occur constancy in one of the pollinators must be a function of the ratio of rewarding to non-rewarding flowers of both floral forms. One prediction from our results is that sympatric speciation of floral complexity based on a higher probability of reward is more likely to occur in flowers offering rewards of pollen rather than nectar. This is because the cost of visiting non-rewarding flowers is usually higher where the reward is pollen rather than nectar. We also predict that complex flowers occurring at low frequency, which offer rewards of nectar, may need intrinsically greater rewards if they are to successfully attract pollinators.     

Effects of variation in flower number on pollinator visits in Cirsium purpuratum (Asteraceae)

We examined the functional relationships between floral display and two types of bumble bee response, the visitation rate per plant and the number of flowers visited on a plant, in an artificially arranged field population of Cirsium purpuratum. To reduce the variance in data, we collected data for each day separately and adopted a Latin square design in selecting the focal plants within a day. We then tested several types of regressions to each set of data to find the best-fitting line accounting for the observed relationship between pollinator response and display size. We found that the visitation rate of bumble bees per plant was a decelerating function of floral display, and that the number of flowering heads visited on a plant increased linearly with display size. Predicted from the above two functions, the visitation rate per head was independent of floral display and nearly constant within each day. Our results suggest that conventional methods in collecting and analyzing data on pollinator visitation may yield large variance in data derived from temporal and spatial heterogeneity and that improved methods employed here are effective in reducing the variance and estimating patterns of pollinator response to floral display more accurately.     

The phenology of gender in homogamous flowers: temporal change in the residual sex function of flowers of Oil-seed Rape (Brassica napus)

1. We investigated the phenology of the male and female sexual functions in flowers of Oil-seed Rape ( Brassica napus ) that were exposed to pollinators in an experimental garden. The female 'residual sex function' (RSF) of flowers was measured by hand-pollinating with genetically marked pollen in order to determine the proportion of ovules that remained available for fertilization by incoming pollen. Male RSF was measured by estimating the proportion of pollen grains that remained in dehiscing anthers.
2. Following flower opening, an average flower's male and female sexual functions each required for completion c. 13 h of exposure to pollinators. One hour after opening, c. 50% of a flower's ovules were unavailable to incoming pollen whereas only c. 10% of pollen was removed. Therefore, a flower's sexual function was predominantly female for the first hour and predominantly male thereafter.
3. We found a fairly close correspondence between the proportion of the stigma covered with pollen and the depletion of female RSF.
4. On average, floral senescence occurred after c. 14·5 h of exposure to pollinators. Our observations are fairly consistent with a simple, economic model of optimal senescence time because the flowers remained open for approximately the same length of time as was necessary for the completion of their sexual functions.
5. A flower's senescence was hastened when pollen was removed from the anthers, but not when pollen was deposited on the stigma.
6. When flowers were either left undisturbed or hand-pollinated, senescence occurred after c. 24 h. Pollen removal caused senescence after c. 13 h, which also approximated the longevity of flowers in the experimental garden. Apparently, pollen removal governed floral longevity under field conditions.     

'Anti-bee' and 'pro-bird' changes during the evolution of hummingbird pollination in Penstemon flowers

Floral phenotypes may be as much the result of selection for avoidance of some animal visitors as selection for improving the interaction with better pollinators. When specializing on hummingbird-pollination, Penstemon flowers may have evolved to improve the morphological fit between bird and flower, or to exclude less-efficient bees, or both. We hypothesized how such selection might work on four floral characters that affect the mechanics of pollen transfer: anther/stigma exsertion, presence of a lower corolla lip, width of the corolla tube, and angle of flower inclination. We surgically modified bee-pollinated P. strictus flowers changing one trait at a time to make them resemble hummingbird-pollinated P. barbatus flowers, and measured pollen transfer by bumblebees and hummingbirds. Results suggest that, apart from 'pro-bird' adaptations, specific 'anti-bee' adaptations have been important in shaping hummingbird-flowers. Moreover, some trait changes may have been selected for only if changing in concert with other traits.