Size-number trade-offs and pollen production by Papilionaceous legumes

The intra- and interspecific relations between the size and number of pollen grains were examined for 21 species of papilionaceous legumes to test for the trade-off expected from the subdivision of limited resources. We observed a tradeoff between pollen grain diameter and the number of grains produced per flower within 17 of the 21 species examined. For 12 of these species, the observed partial regression coefficient for In (pollen grain diameter) equaled -3, as expected. The remaining five species exhibited more negative partial regression coefficients than expected. Relations between pollen grain size and number that are more negative than expected may result from a decelerating relation between pollen grain size and the resource investment per grain. Flower production significantly influenced pollen production for only eight species so that pollen production seems to be determined primarily on a per flower basis. Interspecifically, pollen size also varied inversely with pollen number for the 21 species even after the effect of phylogenetic relatedness was removed. Pollen size varies relatively little compared to the number of pollen grains produced per flower and therefore may be the primary target of natural selection. The presence of a trade-off in pollen production probably constrains the evolutionary options by which flowering plants can maximize male success.     

COMPONENTS OF SEED AND POLLEN YIELD OF LOBELIA CARDINALIS: VARIATION AND CORRELATIONS

Plants from three Lobelia cardinalis populations were grown under common garden conditions to assess intra- and interplant variation in seed and pollen production. Seed number per flower and mean seed weight varied systematically with floral position on the inflorescence (lowest values were from terminal flowers) but pollen grain number per flower did not vary systematically with floral position. Most of the remaining variance in seed and pollen grain number per flower and mean seed weight was distributed among plants; clones produced very similar amounts of pollen and seed. Seed yield was positively correlated with seed production per flower and with total flower production, but not with mean seed weight; pollen yield was also positively correlated with pollen grain production per flower and total flower production. Seed and pollen yield were simple linear functions of plant size but only pollen yield was a simple linear function of flower production; seed yield was a quadratic function in which the second order term was negative. This quadratic relationship resulted from a negative correlation between seed number per flower and total flower production. This correlation, in addition to the wide variation among plants in pollen number per flower, accounts for the weak correlation of seed and pollen yield. I conclude from these data that it is unlikely that plants in natural L. cardinalis populations transmit genes to the population's seed crop equally through pollen and ovules—emphasizing the importance of measuring both male and female components of reproductive success.     

Pollen-pistil size correlation and pollen size-number trade-off in species of Argentinian Nyctaginaceae with different pollen reserves

Data on pollen and pistil traits from 14 Argentinean Nyctaginaceae species with starch or lipids as pollen reserves are presented. We expect differences in the traits between these two groups of species, but the same pattern within each group for (a) the relationship between pollen size and pistil length assuming that pollen tube length is predetermined by provisions in the pollen independently of the pollen reserve type, and for (b) a trade-off between size and number because available resources for male function are not unlimited. In particular we expect that (a) species with longer pistils will have larger pollen grains, (b) pollen grain size and the number of pollen grains per flower will be negatively correlated. Significant differences in the mean pollen number per flower and mean pollen size were observed between species with different pollen reserve type but not for pistil length. Then, correlation analyses were performed for species with starchy pollen or with pollen with lipids separately. Pollen size - pistil length correlation was positive and significant for species with starchy pollen but not for species with pollen with lipids. On the other hand, pollen size - number correlation was not significant for both starchy and oil-rich species. Results suggest that pollen reserve type would be a relevant factor that constraint pollen size in species of Nyctaginaceae, and that this pollen trait should be considered when studying pollen-pistil relationships, mainly between species of those families with mixed pollen reserves.     

Effects of soil fertility and mycorrhizal infection on pollen production and pollen grain size of Cucurbita pepo (Cucurbitaceae)

The effects of soil fertility (two levels of soil nitrogen and two levels of soil phosphorus) and mycorrhizal infection on pollen production and pollen grain size were studied in two cultivars of the common zucchini (Cucurbita pepo). Overall, soil fertility and mycorrhizal infection had significant effects on traits affecting the male function of plants (staminate flower production, pollen production per flower and pollen grain size). There were also differences between the cultivars for these male traits in all three experiments. In addition, pollen grain size decreased toward the end of the growing season. In the mycorrhiza experiment, both phosphate concentration per pollen grain and total phosphate content per anther were greater but not significantly greater in the mycorrhizal plants than in the non-mycorrhizal plants. A significant negative relationship between pollen production and pollen grain size was found in the mycorrhiza and soil phosphorus experiments, indicating that there was a trade-off between pollen production and pollen size. This study is the first to show that mycorrhizal infection has an effect on male function (pollen production and size) in addition to the well-documented effects on female function (fruit/seed production and size).     

A model for seed size variation among plants

Summary I developed a model for seed size variation among plants assuming that the pollen captured per flower depends on both the allocation to pollen capture mechanisms per flower and the number of flowers on each plant. I showed that the optimal seed size increases with (1) the total resource allocation to reproduction, (2) decreasing outcross pollen availability, (3) decreasing probability of seedling establishment and (4) decreasing selfing rate. However, optimal seed size does not depend on the total resource allocation if the total number of pollen grains captured by a plant increases linearly with its flower number. In addition, the optimal seed size is not always positively correlated with the optimal resource allocation to pollen capture mechanisms per flower. I discussed implications of the results for seasonal decline in seed size and seed size variations among populations, such as alutitudinal variation.     

Floral display, pollinator visitation and reproductive success in the dioecious perennial herb Wurmbea dioica (Liliaceae)

Floral traits that increase attractiveness to pollinators are predicted to evolve through selection on male function rather than on female function. To determine the importance of male-biased selection in dioecious Wurmbea dioica, we examined sexual dimorphism in flower size and number and the effects of these traits on pollinator visitation and reproductive success of male and female plants. Males produced more and larger flowers than did females. Bees and butterflies responded to this dimorphism and visited males more frequently than females, although flies did not differentiate between the sexes. Within sexes, insect pollinators made more visits to and visited more flowers on plants with many flowers. However, visits per flower did not vary with flower number, indicating that visitation was proportional to the number of flowers per plant. When flower number was experimentally held constant, visitation increased with flower size under sunny but not overcast conditions. Flower size but not number affected pollen removal per flower in males and deposition in females. In males, pollen removal increased with flower size 3 days after flowers opened, but not after 6 days when 98% of pollen was removed. Males with larger flowers therefore, may have higher fitness not because pollen removal is more complete, but because pollen is removed more rapidly providing opportunities to pre-empt ovules. In females, pollen deposition increased with flower size 3 days but not 6 days after flowers opened. At both times, deposition exceeded ovule production by four-fold or more, and for 2 years seed production was not limited by pollen. Flower size had no effect on seed production per plant and was negatively related to percent seed set, implying a tradeoff between allocation to attraction and reproductive success. This indicates that larger flower size in females is unlikely to increase fitness. In both sexes, gamete production was positively correlated with flower size. In males, greater pollen production would increase the advantage of large flowers, but in females more ovules may represent a resource cost. Selection to increase flower size and number in W. dioica has probably occurred through male rather than female function. Received: 15 June 1997 / Accepted: 12 February 1998     

ECOLOGICAL CONSEQUENCES AND PHENOTYPIC CORRELATES OF PETAL SIZE VARIATION IN WILD RADISH,RAPHANUS SATIVUS (BRASSICACEAE)

In this paper we examine some ecological consequences and phenotypic correlates of flower size variation in wild radish, Raphanus sativus. Mean corolla diameter varied significantly among individuals within natural populations of R. sativus in California. On the average, almost 40% of flower biomass was allocated to corolla tissue. In field experiments, pollinator visitation increased significantly with corolla size. Large flowers also accumulated more nectar when pollinators were excluded from plants. In three populations, corolla size was positively correlated with allocation to pollen per flower (either anther weight or pollen grain number), but there was usually no phenotypic relationship between corolla size and several measures of female allocation (ovule number per flower, proportion fruit set, and total seed mass per fruit). Plants growing in the field produced fewer large flowers per unit of stem, and stem biomass was negatively related to corolla size for plants grown under controlled greenhouse conditions. Male and female fitness may covary differently with allocation to attractive floral features in species such as R. sativus, where seed production is often limited by resources rather than by pollen.     

Factors affecting pollinator movement and plant fitness in a specialized pollination system

The rate of pollen exchange within and among flowers may depend on pollinator attraction traits such as floral display size and flowering plant density. Variations in these traits may influence pollinator movements, pollen receipt, and seed number. To assess how floral display size and flowering plant density affect parameters of pollinator visitation rate, pollen receipt per flower, seed number per fruit and the between-plant pollinator movements, we studied the self-incompatible plant, Nierembergia linariifolia. Per-flower pollinator visitation rate and bout length increased linearly with increasing floral display size. Pollen receipt per flower increased linearly with increasing flowering plant density. For seed number per fruit, a polynomial model describing an increased seed number per fruit at low density and a decreased seed number per fruit at high density provided a significant fit. Per-flower pollinator visitation rate was not associated with pollen receipt per flower and seed number per fruit. Bees visited plants located near to the center of the population more frequently than plants located at the periphery. Increases in both floral display size and flowering plant density led to an increased chance of a plant being chosen as the center of the pollinator foraging area. These results suggest that even though large floral displays and high flowering plant density are traits that attract more pollinators, they may also reduce potential mate diversity by restricting pollen movement to conspecific mates that are closely located.     

Limiting factors for seed production in Cynoglossum officinale

Summary Over three years of study, small plants of Cynoglossum officinale consistently produced more flowers per unit of dry weight than large plants. In contrast to earlier results, weight of all seeds tended to increase more than proportional to size. As a result a positive correlation existed between seed set per flower and plant size. The correlation between the mean number of pollinator visits per flower and size was positive but not significant. In a field experiment we found that resources rather than pollen were limiting seed set. Thus, it is unlikely that enhanced pollination of the largest plants causes the size-dependency of seed set per flower. Alternative hypotheses are discussed briefly.Publication of the Meijendel Comité, New Series No. 96     

Plant size,geitonogamy and seed set in Ipomopsis aggregata

Summary We used powdered fluorescent dyes to estimate receipt of self vs. outcross pollen in the self-incompatible species Ipomopsis aggregata (Polemoniaceae). Flowers on small and large plants received equal amounts of outcross pollen, whereas flowers on large plants received more self pollen, so the proportion of self pollen delivered through geitonogamy increased with plant size. In natural populations emasculation of all flowers on a plant raised average seed set per flower from 5.19 to 6.99 and also raised fruit set, though not significantly. From these results one expects a negative correlation between plant size and seeds per flower. The opposite trend was observed in a sample of plants in the field, suggesting that deleterious effects of geitonogamy on female fecundity in large plants can be overruled by other factors such as size-related fruit or seed abortion. Results are discussed in relation to the evolution of gynodioecy.     

VARIATION AND COVARIATION AMONG FLORAL TRAITS WITHIN AND AMONG FOUR SPECIES OF NORTHERN EUROPEAN PRIMULA (PRIMULACEAE)

Phenotypic and genetic variation and correlations among floral traits within and among four Primula species were measured to seek evidence for potential constraints on the independent evolution of floral characters, to examine the relationship between mating system, ploidy level, and sex allocation, and to determine whether some traits are more conservative than others within and across these congeners. We measured mean flower diameter, corolla depth, pollen production, modal pollen grain volume, ovule number per flower, and pollen: ovule ratios for 64 field-collected genotypes from northern Europe. These represented one heterostylous (P. farinosa: 2n = 18) and three homostylous (P. scotica: 2n = 54, P. scahdinavica: 2n = 74, and P. stricta: 2n ~ 126) species. All traits differed significantly among species and among the six taxon/morph categories identified (including three morphs of P. farinosa: pin, thrum, and homostylous). Pollen production per flower was significantly higher (and individual pollen grain volume lower) in the outcrossing P. farinosa than in any of the homostylous species; also, pin morphs produced significantly more pollen per flower than thrums in P. farinosa. Among the homostylous species, there were significant differences in all traits except modal pollen grain volume. Ovule number per flower and flower size were less variable among taxa than pollen production and pollen volume. Within species, there were several strong negative correlations among genets between pairs of traits, but each species exhibited a unique set of inverse relationships. We detected only one significant positive genetic correlation; in P. stricta, ovule number and pollen production per flower were positively correlated among genets. Among species means, two pairs of traits were negatively correlated: mean ovule number per flower vs. flower diameter (but P = 0.0587), and mean pollen production per flower vs. modal pollen grain volume. These negative correlations within and among taxa suggest that there may be intrinsic genetic constraints on the independent evolution of these floral characters, but that these constraints differ among species.     

The relationship of the female reproductive success of Eucalyptus globulus to the endogenous properties of the flower

Low capsule and seed set is a major factor limiting seed production in Eucalyptus globulus seed orchards. Controlled pollination studies showed that the reproductive success (number of seeds produced per flower pollinated) was primarily determined by the female. We aimed to identify the factors contributing to the differences in reproductive success between female genotypes in terms of the physical and anatomical properties of the flower. We studied pairs of genotypes of high and low reproductive success from each of three races (Furneaux Group, Strzelecki Ranges and Western Otways) growing in a seed orchard. Controlled pollinations were performed on six females and along with flower physical measurements, pollen tube growth and seed set were assessed. Overall tree reproductive success was positively correlated with flower size, ovule numbers, style size, cross-sectional area of conductive tissue within the style (all of which were inter-correlated) and the proportion of pollen tubes reaching the bottom of the style. Significant positive correlations of reproductive success and flower physical properties between different ramets of the same genotypes across seasons suggests a genetic basis to the variation observed. The majority of pollen tube attrition occurred within the first millimetre of the cut style and appeared to be associated with differences in style physiology. When examined as pairs within races the difference in reproductive success for the Western Otways pair was simply explained by differences in flower size and the number of ovules per flower. Physical features did not differ significantly for the Strzelecki Ranges pair, but the proportion of pollen tubes reaching the bottom of the style was lower in the less reproductively successful genotype, suggesting an endogenous physiological constraint to pollen tube growth. The difference in reproductive success between the females from the Furneaux Group was associated with a combination of these factors.     

Phylogenetic evidence for a flower size and number trade-off

The size and number of flowers displayed together on an inflorescence (floral display) influences pollinator attraction and pollen transfer and receipt, and is integral to plant reproductive success and fitness. Life history theory predicts that the evolution of floral display is constrained by trade-offs between the size and number of flowers and inflorescences. Indeed, a trade-off between flower size and flower number is a key assumption of models of inflorescence architecture and the evolution of floral display. Surprisingly, however, empirical evidence for the trade-off is limited. In particular, there is a lack of phylogenetic evidence for a trade-off between flower size and number. Analyses of phylogenetic independent contrasts (PICs) of 251 angiosperm species spanning 63 families yielded a significant negative correlation between flower size and flower number. At smaller phylogenetic scales, analyses of individual genera did not always find evidence of a trade-off, a result consistent with previous studies that have examined the trade-off for a single species or genus. Ours is the first study to support an angiosperm-wide trade-off between flower size and number and supports the theory that life history constraints have influenced the evolution of floral display.     

Sexual reproduction and variation in floral morphology in an ephemeral vernal lily,Eyythronium americanum

Summary In a riparian population of Erythronium americanum (Liliaceae) in central New Jersey, experimentally self-pollinated plant produced markedly fewer fruit and fewer seeds per fruit than hand-outcrossed and open pollinated plants, even though differences were not evident between pollen tubes that penetrated stigmas from self or foreign pollen. This weak self-compatibility and a positive relation between the percentage of seeds set by outcrossed plants and the distance between pollen donor and recipient plants indicate that this population could be susceptible to inbreeding depression.Limited resources for seed development apparently constrained maximal seed production, based on low seed set (40.6%) by hand-pollinated plants and positive correlations for these plants between plant size and the number and size of seeds set. In contrast, naturally-pollinated plants set a smaller proportion of their ovules, suggesting that limited pollinator service reduced the quantity of seeds produced in this population. Free-foraging bees usually removed more than half of the available pollen in a single visit, so that individual plants probably have few opportunities to disseminate their pollen.Even though sexually reproductive ramets produce only a single flower per year, less than a third of variation in floral morphology is associated with variation in plant size. Within the flower, the sizes of some closely associated structures, such as the style and ovary, and the anthers and filaments, vary essentially independently of one another. Production of nectar and pollen, the ultimate attractors of pollinating insects, was positively correlated with flower size.     

Genetics of sex allocation in Mimulus (Scrophulariaceae)

Theoretical models of the evolution of resource allocation patterns to male and female function make the assumption that there are inherent trade-offs between the two. Here we use a quantitative genetic approach to quantify trade-offs between male and female function and to determine whether plant populations could readily respond to natural selection by quantifying the amount of genetic variation for pollen and ovule production. Both intra- and interspecific crossing designs were applied to two populations of the predominantly outcrossing Mimulus guttatus and two populations of the highly selfing congener, M. micranthus. The only significant correlations observed among pollen number, pollen size and ovule number were positive. Positive genetic correlations among the traits were sometimes reduced after removing the effect of flower size but still no significant negative correlations were detected. These results suggest that positive correlations between pollen and ovule production may be due to the joint positive correlation of these characters with the resource pool available for pollen and ovule production, as reflected by flower size. Heritabilities were moderate to high for ovule production but low for pollen number and pollen size and suggest that responses to selection would differ between the two traits. Crosses between the species revealed that there are additional genetic factors contributing to differences between the two species for corolla width, vs. pollen:ovule ratio. This is consistent with the hypothesis that genetic variation for resource acquisition may in part be responsible for the overall lack of a negative correlation between pollen and ovule production and provides a genetic explanation for little evidence of trade-offs between sexual functions in Mimulus.     

VARIATION IN POLLEN SIZE,FERTILIZATION ABILITY,AND POSTFERTILIZATION SIRING ABILITY IN ERYTHRONIUM GRANDIFLORUM

The mean volume of pollen grains and total pollen production varied both within and among plants of Erythronium grandiflorum. The second flowers of two-flowered plants tended to produce smaller and fewer grains than first flowers, but there was no overall relationship between mean pollen grain size and production per flower. I evaluated the effects of pollen size differences within and among plants on two components of male reproductive success: pollen tube growth and postfertilization siring ability. Pollen tubes grown in media were longer for second flowers, but were not correlated with the mean size of pollen grains, suggesting that (1) internal resource content of pollen (i.e., carbohydrates plus lipids) was not associated with the hydrated size of pollen, and that (2) pollen from second flowers contained more resources. I analyzed the growth rate and the fertilization ability of pollen growing in styles. Growth rate differed among donors and recipients, but no effects of pollen or donor characters (i.e., pollen production, grain size, and flower position) were detected. In single donor pollinations, pollen size was negatively correlated with fertilization ability across donors, and positively correlated with postfertilization siring ability of donors. A second experiment used pairs of donors; within-plant differences in pollen size and flower position had effects similar to the single donor experiment on fertilization ability, but among-plant differences were not significant. The results corroborate earlier experiments that suggest that the growth of pollen tubes in the style is probably controlled by the recipient, since donor characters had minimal effects on pollen fertilization ability. Postfertilization siring ability was not affected by within-plant differences in mean grain size and production. For among-donor differences, the number of seeds set for each donor was positively correlated with the mean grain volume, and when a donor producing large pollen fertilized ovules in an ovary, there was increased seed abortion for seeds in the same ovary sired by a second donor. In addition, the total number of seeds produced by a fruit was decreased when both donors had large pollen, apparently due to increased postfertilization abortion. Postfertilization processes appear to be influenced by paternal differences that are expressed through competition among developing seeds for maternal resources.     

Selecting for floral character associations in wild radish,Raphanus sativus L.

ESS models of reproductive allocation have been used extensively to explain patterns of floral diversity in angiosperms. These theoretical explorations assume that proportional allocation to pollen, ovules, and seeds, as well as to secondary features such as showy petals and nectar rewards, can evolve independently within the limits set by total resource availability. In populations of California wild radish, we have shown previously that petal size, a strong determinant of visitation by honey bee pollinators, is positively correlated with both pollen and nectar production, but not with ovule or seed number per flower. These phenotypic associations may reflect selection, environmental correlation, and/or genetic constraint. By exerting selection on the petal size : pollen number ratio over two generations, we eliminated the positive correlation between petal size and pollen production, with both characters showing significant change after a single selection episode. Once these two floral traits became uncoupled, nectar sugar production was significantly correlated only with petal size. Our results suggest that natural selection could readily alter reproductive allocation in these flowers, and that the phenotypic correlations observed in nature may be maintained by selection for effective reproductive phenotypes.     

RE-EVALUATING THE SIGNIFICANCE OF CORRELATIONS BETWEEN SEED NUMBER AND SIZE: EVIDENCE FROM A NATURAL POPULATION OF THE LILY,CLINTONIA BOREALIS

The basis for the negative correlation between seed number and seed size was experimentally investigated in a natural population of Clintonia borealis. Clones of this species vary significantly in estimated self-compatibility (ratio of seed set with selfing to that with outcrossing) and this appears to affect the number and size of seeds set in individual flowers of each. Clones estimated to be largely self-compatible set more seeds per flower than incompatible ones under natural pollination. However, naturally pollinated flowers of self-compatible clones set smaller seeds than those of incompatible clones, and the significance of the negative relationship between seed number and size in individual flowers was removed by holding variation due to compatibility constant. Supplementing resources per flower (by reducing the number of fruits competing for resources per stem) significantly increased total seed mass but had no effect on the negative relationship between seed number per flower and seed size. In contrast, supplementing cross pollination did not significantly influence total seed mass per flower but changed the relationship between seed number and size to positive, regardless of resource level. In other words, with plentiful cross pollination maternal genets capable of setting more seeds per flower also produced heavier ones. Thus, evidence is provided that the balance between seed number and seed size in this population is regulated by the interaction of maternal self-compatibility with natural pollination.     

Post-pollination reproductive isolation between diurnally and nocturnally flowering daylilies, Hemerocallis fulva and Hemerocallis citrina

To examine whether floral and post-pollination isolation develops independently or not, we conducted a crossing experiment between Hemerocallis fulva and Hemerocallis citrina that shows large floral divergence adapted for diurnal and nocturnal pollinators that have been believed to be fully cross-fertile. Flowers of the two species from sympatric populations were hand-pollinated with conspecific pollen from the same population (control), interspecific pollen from the same area (sympatric cross), and interspecific pollen from the different area (allopatric cross). After capsule dehiscence, the fruit set, seed set per fruit and seed set per flower were determined among three cross categories. The seed sets per flower were 32 and 77% lower in sympatric and allopatric crosses than in the control when H. fulva was the pollen recipient. There was no difference in three reproductive measures among the cross categories when H. citrina was the pollen recipient. This finding indicates that post-pollination isolation does exist between H. fulva and H. citrina, although it is partial, asymmetric, and weakened in sympatry. Our result suggests that floral and post-pollination isolation may develop independently, and reinforcement may not be a general phenomenon in plants.     

The influence of plant and corolla size on pollen deposition and seed set in Geranium sanguineum (Geraniaceae)

In a coastal grassland area the influence of plant and corolla size on insect visitation rate, pollen deposition on stigmas and seed set was measured in a natural population of Geranium sanguineum. Visits by bumble bees, the primal pollinators, were significantly affected by plant size measured as the number of flowers, and differences in visit rates among plants were explained by size differences among these. On average, larger plants had bigger corollas. The mean corolla area affected pollen deposition positively whereas deposition did neither affect seed set (number per flower) nor seed weight. Insects reaction to corolla size was dependent on plant size, and thus we found the effect of corolla size on pollen deposition to decline with plant size. Instead pollen deposition per plant seemed to be correlated to overall floral display. We argued that resource status of the individual plants could explain corolla size and seed set variation. The finding of some plant setting seeds while other plant with comparable size did not set any seeds could not be explained satisfactory by resource limitation.