Pollen Competition Research Articles

Natural levels of pollination intensity and effects of pollen loads on offspring quality in females of Thalictrum pubescens (Ranunculaceae)

Females of Thalictrum pubescens produce stamens containing sterile pollen. Earlier studies have shown the presence of stamens does not increase seed set through increased visitation by insects. Insects may, however, increase pollen deposition on stigmas and increase pollen competition. This paper examines: 1) pollen deposition levels in natural populations and 2) whether larger pollen loads lead to higher quality offspring. The majority of stigmas in two populations received less than 15 grains, but a small proportion had large loads. The latter may represent the occasional insect visit. These visits may provide the opportunity for pollen tube competition. In the greenhouse, flowers receiving heavy-pollen loads had higher seed set than flowers receiving light-pollen loads. Seeds from the two treatments were the same mass, had similar germination times, and seedlings had the same mass. In conclusion, it does not appear that pollen tube competition can account for the maintenance of stamens in females of T. pubescens.

Character displacement in style length between pollinator-sharing Clerodendrum trichotomum and C. izuinsulare (Verbenaceae)

Competition for pollination may occur between pollinator-sharing sympatric plants and this may cause character displacement of their floral traits. We examined this possibility by comparing flower morphology of the sympatric population of Clerodendrum trichotomum and its co-flowering congener, C. izuinsulare, with that of the allopatric populations. The two species were visited in common by such insects as diurnal hawkmoths, bees, swallowtails and nocturnal hawkmoths, and were pollinated nocturnally as well as diurnally. Interspecific pollen transfer can occur by sharing pollinators; however, they did not hybridize when artificially pollinated. Flower size, including stamen and style lengths, is larger in C. trichotomum with an overlap in range. The style of C. izuinsulare in the sympatric population was significantly shorter than that in the allopatric population, while there was no significant difference in style length between the allopatric and the sympatric C. trichotomum. This seems to facilitate avoidance of interspecific pollen transfer in the sympatric population.

Factors affecting phenological patterns of bombacaceous trees in seasonal forests in Costa Rica and Mexico

We compared phenological patterns of tree species of the family Bombacaceae in three seasonal forests in Mexico and Costa Rica whose dry seasons vary in duration and intensity. The objectives were to (1) determine intraspecific variation in phenology between sites in different geographic locations with different precipitation regimes, (2) compare interspecific phenological patterns within sites during one year, and (3) document seasonal pollinator use of floral resources at one site in relation to the flowering phenology of these species. To determine the sequence of phenological events in trees of the family Bombacaceae across three study sites, phenology of marked individuals was recorded every 2 wk from September 2000 through August 2001 for six species. To estimate the importance of bombacaceous species in the diet of nectarivorous bats, pollen samples were collected from the bodies or feces of bats once every 2 wk during flowering. Our study suggests that phenological patterns of the Bombacaceae family in Neotropical dry forests are mainly constrained by phylogenetic membership and adaptive selective pressures associated with competition for pollinators. Abiotic factors related to precipitation and soil water content appear to be regulating leaf flushing and abscission, but the principal causes of flowering are related to ultimate factors associated with competition for pollinators. This study is the first that evaluates the phenological pattern of species and genera of the same family at different latitudes in a similar life zone.

Pollen performance before and during the autotrophic-heterotrophic transition of pollen tube growth.

For species with bicellular pollen, the attrition of pollen tubes is often greatest where the style narrows at the transition between stigmatic tissue and the transmitting tissue of the style. In this region, the tubes switch from predominantly autotrophic to predominantly heterotrophic growth, the generative cell divides, the first callose plugs are produced, and, in species with RNase-type self-incompatibility (SI), incompatible tubes are arrested. We review the literature and present new findings concerning the genetic, environmental and stylar influences on the performance of pollen before and during the autotrophic-heterotrophic transition of pollen tube growth. We found that the ability of the paternal sporophyte to provision its pollen during development significantly influences pollen performance during the autotrophic growth phase. Consequently, under conditions of pollen competition, pollen selection during the autotrophic phase is acting on the phenotype of the paternal sporophyte. In a field experiment, using Cucurbita pepo, we found broad-sense heritable variation for herbivore-pathogen resistance, and that the most resistant families produced larger and better performing pollen when the paternal sporophytes were not protected by insecticides, indicating that selection during the autotrophic phase can act on traits that are not expressed by the microgametophyte. In a study of a weedy SI species, Solanum carolinense, we found that the ability of the styles to arrest self-pollen tubes at the autotrophic-heterotrophic transition changes with floral age and the presence of developing fruits. These findings have important implications for selection at the level of the microgametophyte and the evolution of mating systems of plants.

Males outcompete hermaphrodites for seed siring success in controlled crosses in the polygamous Fraxinus excelsior (Oleaceae)

Polygamy (including trioecy and subdioecy), the co-occurrence of males, hermaphrodites, and females in natural populations, is a rare and poorly studied breeding system expressed in Fraxinus excelsior L. (Oleaceae), a wind-pollinated tree. Here we investigate siring ability of pollen from male vs. hermaphrodite individuals to better understand this sex polymorphism. We conducted single-donor and two-donor pollination experiments and compared both fruit set and seed siring success, assessed with polymorphic microsatellite markers, of male and hermaphrodite individuals. Single pollen donor crosses allowed us to verify the male function of hermaphrodites. However, pollen from hermaphrodites was much less proficient than male pollen, with males siring 10 times as many fruits in single donor pollination treatments. This result was strengthened by the surprisingly low reproductive success of hermaphrodites in pollen competition conditions: of the 110 seedlings analyzed three were selfed and only one was sired by the hermaphrodite donor. The remaining 106 were sired by the male pollen donor. These results raise the question of the maintenance of male fertility in hermaphrodites in Fraxinus excelsior. Male function of hermaphrodites in this species now needs to be assessed under field conditions.

Pollen Deposition, Pollen Tube Growth, Seed Production, and Seedling Performance in Natural Populations ofClarkia unguiculata(Onagraceae)

In natural plant populations, pollen grain load sizes may vary greatly and have the potential to affect the intensity of pollen competition for ovules. Pollen competition can in turn, affect seed production, fruit set, and progeny vigor, with important ecological and evolutionary consequences. In this investigation, we determined the potential for pollen competition in four adjacent natural populations of Clarkia unguiculata during three growing seasons. We collected stigmas and styles after 6, 24, and 48 h of exposure to pollinators and determined pollen load sizes, the number of pollen tubes reaching the upper and lower portions of the style, and pollen tube attrition rates. We also collected mature seeds to determine the effect of pollen load size on seed set, seed germination, and seedling vigor. Pollen load sizes increased with increasing length of exposure to pollinators and varied from year to year and from population to population. In most plants, pollen loads were large enough to result in pollen competition on the stigma. The number of pollen tubes reaching the upper and lower portions of the style was affected by pollen load sizes. Pollen tube attrition rates in the style were moderate and were not affected by pollen load sizes. However, as pollen tubes completed growth in the style, the opportunity for pollen competition decreased as the number of pollen tubes became smaller than the number of ovules in the ovary. Seed production in this experiment was dependent on pollen load sizes, even though the number of seeds produced was well below the number typically recorded for this species. Our measures of seedling vigor (percentage seed germination, cotyledon length, and first foliar leaf length) were not affected by pollen load size.

Pollen competition does not affect the success of self-pollination in Eucalyptus globulus (Myrtaceae)

This study investigated whether pollen competition favours cross- over self-pollination in Eucalyptus globulus Labill. ssp. globulus. Controlled pollinations with self-pollen, cross-pollen and a mixture of self- and cross-pollen were conducted on three partially self-incompatible trees. The paternity of individual seeds resulting from mixed pollination was determined by isozyme analysis. No evidence for pollen competition was found. Instead, seed paternity reflected the level of self-incompatibility of each tree as determined by separate self- and cross-pollinations. Furthermore, the number of seeds set per capsule following mixed pollination was significantly less than that following cross-pollination in the two least self-compatible trees. These results suggest that both self- and cross-pollen tubes reach ovules following mixed pollination and that a late-acting self-incompatibility mechanism operates to abort a certain proportion of self-penetrated ovules.

CONTRASTING FLOWERING PHENOLOGY AND SPECIES RICHNESS IN ABIOTICALLY AND BIOTICALLY POLLINATED ANGIOSPERMS

Biotic pollination is thought to correlate with increased interspecific competition for pollination among plants and a higher speciation rate. In this study we compared patterns of flowering phenology and species richness between abiotically (wind) and biotically pollinated plants, using phylogenetically independent contrasts. We compiled phenological data from eight local seasonal floras, in which we found geographically overlapping sister clades. Of 65 documented origins of wind pollination, we were able to use up to 17 independent contrasts. In contrast to previous studies we found no difference in global species richness between wind- and biotically pollinated sister clades. Regarding phenology, we found wider phenological spread in biotically pollinated clades, earlier flowering onset in wind-pollinated trees, but no difference in duration of flowering between pollination modes. These results corroborate previous views that niche space is more constrained for wind-pollinated species, and that niche partitioning is less important between wind-pollinated plants compared to plants pollinated by animals.

Seed paternity in flowering plants: an evolutionary perspective

The ultimate importance of paternal contributions to fitness and of post-pollination selection in flowering plants have remained elusive, largely because of the technical difficulty of assigning paternity. I review empirical studies that use heritable markers to investigate per-fruit seed paternity in natural populations and after experimental multiple-donor pollination. Thirty-one studies covering 23 species from 16 plant families document that in natural populations seeds from a single fruit are often fathered by multiple pollen donors (5 species from 5 families), that donors can differ significantly in seed-siring success (8 species from 6 families), that variation in pollen tube growth rates can be heritable (n = 1 out of 4 studies), that donor and recipient genotypes can simultaneously affect paternity (n = 2), and that temporal order of pollen deposition (n = 1) and environmental effects(n = 2) affect the outcome of pollen competition. These studies also investigate the role of post-pollination selection in the avoidance of inbreeding and for species boundaries. Most studies of male reproductive success in plants to date base on isozyme electrophoresis. The availability in the last decade of highly polymorphic molecular markers such as microsatellite DNA has been expected to open new possibilities to investigate competition and selection during the gametophytic phase. Yet, to date, there is still need for greater data wealth on seed paternity to test theories of sex allocation and to gain deeper understanding of floral trait evolution and of the evolutionary consequences of post-pollination selection in flowering plants.

Pollen competition as a unilateral reproductive barrier between sympatric diploid and tetraploid Chamerion angustifolium.

Speciation requires the evolution of barriers to gene exchange between descendant and progenitor populations. Cryptic reproductive barriers in plants arise after pollination but before fertilization as a result of pollen competition and interactions between male gametophytes and female reproductive tissues. We tested for such gametic isolation between the polyploid Chamerion angustifolium and its diploid progenitor by conducting single (diploid or tetraploid) and mixed ploidy (1 : 1 diploid and tetraploid) pollinations on both cytotypes and inferring siring success from paternity analysis and pollen-tube counts. In mixed pollinations, polyploids sired most (79%) of their own seeds as well as those of diploids (61%) (correcting for triploid block, siring success was 70% and 83%, respectively). In single donor pollinations, pollen tubes from tetraploids were more numerous than those from diploids at four different positions in each style and for both diploid and tetraploid pollen recipients. The lack of a pollen donor x recipient interaction indicates that the tetraploid siring advantage is a result of pollen competition rather than pollen-pistil interactions. Such unilateral pollen precedence results in an asymmetrical pattern of isolation, with tetraploids experiencing less gene flow than diploids. It also enhances tetraploid establishment in sympatric populations, by maximizing tetraploid success and simultaneously diminishing that of diploids through the production of inviable triploid offspring.

Studies on the possible competition for pollen between the honey bee, Apis mellifera sudanensis, and the imported dwarf honey bee Apis florea (Hym., Apidae) in North‐Khartoum (Sudan)

Abstract: Based on identification of collected pollen, in the area of North Khartoum, 21 plant genera (ca. 21 spp.) proved to be the main pollen sources for the honey bee Apis mellifera sudanensis. The imported dwarf honey bee Apis florea exploited 11 of these. The main pollen flow in the study area occurred between early December and late March. This is reflected by the amount of pollen collected by colonies of A. mellifera sudanensis. In spite of observations conducted soon after the introduction of A. florea, which gave hints of competition between the two bee species, further studies showed that A. mellifera sudanensis and A. florea do seem to coexist. This coexistence is based on different daily rhythms of pollen collection. A. mellifera collected pollen of Acacia seyal, date palm, and onions early in the morning (and partly in the late afternoon), while A. florea started pollen collection mostly later in the morning and ended it earlier in the afternoon. But in contrast to A. mellifera, A. florea was collecting pollen all day without interruption, even at very high air temperatures. Niche overlap (concerning the times of visits to flowers) between the two bee species was very low in date palms, and of medium importance in Acacia seyal. But it is remarkable that in total, A. florea is always present in higher numbers than A. mellifera sudanensis, on flowers. The significance of the introduction of A. florea to Sudan for pollination is discussed.

Characterization of the pollen growth transition in self-incompatible Petunia inflata

In Petunia inflata, as in other species that shed bicellular pollen, early pollen tube growth in the pistil is slow, then increases 2- to 5-fold depending on the genotype of the female parent. We refer to the time point at which pollen tubes enter the accelerated phase of growth as the pollen growth transition (PGT). Here, we present evidence that pre-PGT and post-PGT growth are quantitatively and qualitatively different, and that the PGT is triggered when pollen tubes reach the transition zone (TZ) below the stigma. The capacity of various pistil zones to precipitate the PGT was tested through 'stump' pollinations: varying lengths of the pistil apex were excised, the cut surface of the remaining pistil (the stump) coated with stigmatic exudates then dusted with compatible pollen. Pollen applied to TZ tissues entered the PGT earlier than pollen growing in intact control pistils; the PGT was delayed in stylar stumps, largely because of delayed germination and reduced pre-PGT growth. In immature pistils, the PGT was delayed by several hours relative to its onset in mature pistils. The PGT fails to occur in pollen cultured in vitro. Collectively, the data suggest that pollen tubes become competent to enter the PGT when they reach a critical size, but the physicochemical environment of the transmitting tissue is necessary for triggering the cellular changes that result in accelerated growth. An analysis of the distribution of pollen tube tips before and after the PGT suggests that pollen competition is most intense during the pre-PGT phase.

Competition for Pollination between an Invasive Species (Purple Loosestrife) and a Native Congener

Invasive species are frequently regarded as superlative competitors that can vegetatively crowd out natives, but little is known about whether invasives can compete for pollination services with native plants. We hypothesized that, when the showy invasive species Lythrum salicaria (purple loosestrife) was present, pollinator visitation and seed set would be reduced in a native congener, L. alatum (winged loosestrife). To test this hypothesis, we constructed mixed and monospecific plots of the two species. Over two years of study, we found that L. salicaria significantly reduced both pollinator visitation and seed set in L. alatum. Furthermore, pollinators moved frequently between the two plant species, which may cause heterospecific pollen transfer. Thus, reductions in both pollen quantity and pollen quality may reduce L. alatum seed set. If similar patterns occur in the field, invasive plants may be an even greater threat to natives than previously thought.

Effects of population size and pollen diversity on reproductive success and offspring size in the narrow endemic Cochlearia bavarica (Brassicaceae)

In small, fragmented populations of self-incompatible plant species, genetic drift and increasingly close relationships between plants may restrict the number of genetically different pollen donors, the availability of compatible mates, and the opportunity for pollen competition and selection. These restrictions may reduce the siring success or increase the probability of inbreeding depression in the offspring. To test if this was the case, we hand-pollinated maternal plants in small and large populations of the rare, endemic plant Cochlearia bavarica (Brassicaceae) with pollen from one, three, or nine donors from the same population or with nine donors from a different population. In one additional population of intermediate size, maternal plants were hand-pollinated with ten donors located at a distance of 1, 10, 100, or 1000 m. We then recorded seed and offspring characters. On average, offspring from small populations were smaller than normal and fewer survived to maturity. Increasing the number of pollen donors had a positive effect on reproductive success in small and large populations, but at the highest pollen diversity this occurred at the expense of slightly reduced offspring fitness. Because the total amount of transferred pollen was held constant, these effects could not be attributed to increasing pollen load. Rather, the increasing pollen diversity may have increased the chances of selecting a particularly "good" donor for fertilization-an example of a sampling effect of diversity. Pollen from outside a population or from 10-100 m away resulted in higher reproductive success and greater offspring size. Effects of population size and pollination treatments on reproductive success and offspring fitness were additive. Apparently, there is no obvious size threshold above which the potential of inbreeding depression can be ignored in C. bavarica.

Evolution of syncarpy in angiosperms: theoretical and phylogenetic analyses of the effects of carpel fusion on offspring quantity and quality

Abstract The repeated evolution of fused carpels (syncarpy) is one of the dominant features of angiosperm macroevolution. We present results of new phylogenetic and theoretical analyses to assess the frequency and nature of transitions to syncarpy, and the possible advantages of syncarpy over apocarpy under a variety of ecological conditions. Using a recent molecular estimate of angiosperm phylogeny, we ascertained that a minimum of 17 independent evolutionary transitions from apocarpy to syncarpy have occurred; about three-quarters of these transitions allowed pollen tubes to cross between carpels and fertilize ovules that would otherwise be left unfertilized. Most of these transitions also intensified competition between pollen, potentially enhancing offspring fitness. The high proportion of evolutionary transitions promoting pollen competition and pollen-tube access to all carpels supports the hypothesis that the main advantage of syncarpy is in increasing offspring quality and quantity. The potential advantages of syncarpy were more thoroughly evaluated by analytical and simulation studies. These showed that the advantage of syncarpy over apocarpy involving increased offspring-quantity held under conditions of marginal pollination and declined with increasing pollination. The offspring-quality advantage persisted over a wider range of conditions, including under quite high pollination rates.

Genotype-environment interactions in pollen competitive ability in an anemophilous tree, Betula pendula Roth.

This study describes genotype-environment interactions in pollen competitive ability expressed as pollen-tube growth rate and seed-siring success in Betula pendula Roth. A factorial crossing design was applied using the same maternal and paternal clones in two different environmental conditions, in a B. pendula seed orchard established in a greenhouse and at an outdoor clone collection. Both single donor and two-donor pollinations were employed. Female inflorescences were collected after a fixed time of germination, pollen-tube lengths were measured for each cross, and paternity of the seeds sired by two-donor pollen mixtures was analyzed using isozyme markers. The pollination site had a significant influence on pollen-tube growth rate and seed-siring success. Significant interactions between pollination site and pollen donor indicated genotype-environment interactions in pollen-tube growth rate and seed-siring success. A highly significant positive correlation between pollen-tube growth rate and seed-siring success was found in the greenhouse but not at the outdoor clone collection. These results suggest that the pollen-tube growth rate can be a predictor of seed-siring success in controlled greenhouse conditions, where differences among maternal plants are mainly of genetic origin, but not in more heterogeneous outdoor conditions. In natural birch stands, environmental maternal effects probably diminish the significance of pollen competition for sexual selection in Betula pendula. At seed orchards, the effects of environmental conditions on pollen competitive ability can have important consequences for the genetic composition of the seed crop.

Pollen competition and seed-siring success in Picea abies.

The aim of the present work was to study pollen-tube competition in Picea abies. Controlled crossings were performed with pollen mixtures including pairs of pollen lots with fast and slowly elongating pollen-tubes. Paternity analysis using isozyme markers was performed on the progenies in order to study whether the in vitro pollen-germination vigour corresponds to the proportion of seeds sired by the pollen donor. Paternal success was found to be unequal, 15 out of 23 crossings producing progeny that differed significantly from the hypothetical ratio of 1:1. The paternal contribution in the majority of the crossings was as expected: the pollen parent with more-vigorous in vitro germination sired more seeds than the less-vigorous pollen. In the case of two pollen mixtures, however, the seed-siring success summed over the maternal trees was the opposite to the expected value. Despite these aberrations, the results support the hypothesis that pollen-tube competition is one of the factors contributing to male fitness in P. abies.However, when all the other factors affecting pollination and seed set under natural conditions are taken into account, it is clear that the seed-siring success of a particular paternal genotype cannot be predicted reliably by measuring only the in vitro pollen vigour.

The Effects of Pollen Competition on Progeny Vigor in Fragaria virginiana (Rosaceae) Depend on Progeny Growth Environment

Competition among pollen grains to fertilize ovules is expected to lead to increased vigor of the resulting progeny. Tests of this “pollen‐competition hypothesis,” however, have been equivocal, and this may, in part, result from the levels of pollen competition (pollen load sizes) and/or progeny growth environment chosen. Our study of Fragaria virginiana controlled for these variables by identifying seeds produced under low and high pollen loads from an empirically derived pollen load–seed set response curve. We assessed fitness of seeds at germination under uniform conditions but fitness of progeny at juvenile and adult life stages under two different resource levels in the greenhouse. We hypothesized that the effect of pollen load size on progeny vigor would be stronger when progeny were grown under low resources than when grown under high resources. We found that the effect of pollen load size was negligible at germination but was significant in later life when assessed under two resource levels. The direction of the pollen load effect, however, depended on the progeny growth environment. Under low resources, progeny from high pollen loads grew faster, attained greater biomass, and had a higher probability of flowering than progeny from low pollen loads, while the reverse was true under high resource availability. These results indicate that the effects of pollen competition on juvenile and adult characters depend on progeny growth environment.

Pollen competition between cultivated and wild rice species (Oryza sativaandO. rufipogon)

Summary Post‐pollination competition is reported here in cultivated rice (Oryza sativa) and a perennial wild rice (O. rufipogon) to investigate the occurrence of crop‐to‐wild gene flow. Wild and cultivated rice (variety Minghui‐63) were grown in a common garden in Hunan province, China, and crop‐specific genetic markers were used to detect hybridization following hand‐pollinations. Using 11 sequential pollination treatments, the effects of the relative timing of pollination on the success of foreign pollen was investigated. Foreign pollen from the crop resulted in lower pollen germination, fewer pollen tubes per style, and a significant reduction of seed set, demonstrating a disadvantage of foreign pollen even in the absence of pollen competition. When 1 : 1 pollen mixtures were applied, only 2% of the resulting seeds were hybrids, revealing a much stronger disadvantage of foreign pollen when competing with conspecific pollen. Testing the effects of the relative timing of pollination on the success of foreign pollen suggested that conspecific pollen is often more successful than foreign pollen. Nonetheless, hybridization is possible following the deposition of pollen mixtures, especially when foreign pollen arrives earlier than conspecific pollen. Pollen competition between wild and cultivated rice could slow the rate of crop‐to‐wild gene flow, but even if pollen competition was ubiquitous it would not prevent gene flow from the crop.

INFLUENCE OF PLANT ABUNDANCE ON POLLINATION AND SELECTION ON FLORAL TRAITS OFIPOMOPSIS AGGREGATA

Competition for pollination has been hypothesized to select for the diver- gence of floral traits between species and populations. A primary prediction of this hy- pothesis is that the strength of competition for pollination, mediated by variation in plant abundance, should directly influence the strength of selection on floral traits. To test this prediction, I examined the relationships between multiple components of plant abundance and pollination, reproductive success, and phenotypic selection via female fitness on four floral traits in artificial and natural populations of the hummingbird-pollinated Iponlopsis aggregate. In the artificial arrays, I manipulated the absolute density and interspersion of neighboring I. aggregate and a competitor for pollination (Castilleja linariaefolia). I also measured natural variation in the absolute and relative density of these two species within a 2.5-m radius of focal I. aggregate plants in three natural populations. The strength of competition for pollination in the I. aggregata-C. linariaefolia system was only weakly influenced by local plant abundance. Both the absolute density and in- terspersion of plants in the arrays significantly influenced at least one component of I. aggregate's pollination and reproductive success, but the effects were not consistent across these components. For example, the treatment groups that received more nonspecific pollen were not the same ones that set more seeds/fruit. Within the natural populations, variation in relative and absolute plant density influenced two components of I. aggregata's polli- nation and reproductive success, but only in one to two populations per component. As would be expected from these inconsistent effects of plant abundance on pollination and reproduction, the strength of selection on floral traits of I. aggregata in both the arrays and natural populations was also only weakly dependent on abundance. Previous studies have indicated (1) that self-incompatible species such as I. aggregate should experience strong, abundance-dependent effects on pollination, and (2) that variation in plant abundance at a local scale should have a stronger effect on pollination than variation at a larger spatial scale. In contrast, my results suggest that the effect of plant abundance on pollination cannot be easily predicted from simple diagnostic traits such as breeding system or spatial scale.