INCOMPATIBILITY AND THE POLLEN ECONOMY OF JEPSONIA PARRYI

Jepsonia parryi (Saxifragaceae) has heterostylous flowers and is strongly self-incompatible. Pin flowers have long styles, large stigmas, short stamens, and numerous, small pollen grains with finely sculptured walls. Thrum flowers have short styles, small stigmas, long stamens, and fewer, larger pollen grains with coarsely sculptured walls. Pin plants and thrum plants occur in a 1:1 ratio in field populations. Although the insect pollinators of J. parryi transfer ample compatible pollen to pin and thrum stigmas to account for full seed production, much of the pollen deposited on stigmas is incompatible. Analysis of the pollen deposits on stigmas collected from field populations indicates that compatible “legitimate” pollination of pin and thrum flowers is essentially random and is not obviously aided by floral dimorphism. It is suggested that although heterostyly had a positive adaptive value in the past evolutionary history of Jepsonia it is no longer adaptive under the present pollination regime, although it is maintained because of its strong genetic fixity.     

HETEROSTYLY,POPULATION COMPOSITION,AND POLLEN FLOW IN HEDYOTIS CAERULEA

Hedyotis caerulea is a perennial, spring-flowering herb native to eastern North America with distylous flowers that differ in a number of morphological and physiological traits. However, the pin and thrum morphs produce the same numbers of buds, flowers, and fruits per plant, although it is possible that differences in these may occur in some populations at certain times of the flowering period. The two morphs are self-incompatible and cross-compatible. Most populations contained an excess of pins over thrums (anisoplethy); less commonly pins and thrums were equally represented (isoplethy). Populations change from anisoplethy to isoplethy and in the reverse direction. The spatial distribution of pin and thrum flowers in populations was random in some populations but non-random in others. There is some indication that the two morphs in some populations have somewhat different flowering periods. Pollinators seem to be chiefly bombyliid flies and perhaps thrips, but insects were rarely observed visiting flowers. In some populations, the two morphs produced equal numbers of pollen grains per flower; in others they did not. The average pollen viability varied, but on the average there was a moderate level of pollen sterility. High numbers of pollen grains remained in dehisced anthers, probably as a result of low pollinator activity. However, between 5% and 9% of the pollen produced participated in pollination. Stigmas of most pin flowers received more pin pollen grains than thrum pollen grains; on stigmas of thrum flowers pin pollen grains outnumbered thrum pollen grains. Thus, compatible pollen flow from pins to thrums was greater than in the reverse direction. Anisoplethic and isoplethic populations had the same pollen flow patterns. A plant-by-plant examination of stigmas indicated that many stigmas bore few or no pollen grains. Seed production of the two morphs was equal. Despite the inequities in pollen flow patterns, the widespread and occasionally weedy nature of H. caerulea suggests that its breeding system must be viewed as a successful one.     

Pollen flow inPrimula veris (Primulaceae)

Observations on two natural and one artificial distylous populations ofPrimula veris in Britain revealed very high proportions of intramorph pollen on pin stigmas and moderate proportions of intermorph pollen on thrum stigmas. The average ratio of pin: thrum pollen production per flower was 2.4:1. Large amounts of pollen remained in dehisced anthers, perhaps reflecting low levels of pollinator activity. Population size and density had no clear effect on pollen flow patterns, which are asymmetrical for the two morphs.     

Cryptic self‐incompatibility and distyly in Hedyotis acutangula Champ. (Rubiaceae)

Distyly, floral polymorphism frequently associated with reciprocal herkogamy, self‐ and intramorph incompatibility and secondary dimorphism, constitutes an important sexual system in the Rubiaceae. Here we report an unusual kind of distyly associated with self‐ and/or intramorph compatibility in a perennial herb, Hedyotis acutangula. Floral morphology, ancillary dimorphisms and compatibility of the two morphs were studied. H. acutangula did not exhibit precise reciprocal herkogamy, but this did not affect the equality of floral morphs in the population, as usually found in distylous plants. Both pin and thrum pollen retained relatively high viability for 8 h. The pollen to ovule ratio was 72.5 in pin flowers and 54.4 in thrum flowers. Pistils of pin flowers remained receptive for longer than those of thrum flowers. No apparent difference in the germination rate of pin and thrum pollen grains was observed when cultured in vitro, although growth of thrum pollen tubes was much faster than that of pin pollen tubes. Artificial pollination revealed that pollen tube growth in legitimate intermorph crosses was faster than in either intramorph crosses or self‐pollination, suggesting the occurrence of cryptic self‐incompatibility in this species. Cryptic self‐incompatibility functioned differently in the two morphs, with pollen tube growth rates after legitimate and illegitimate pollination much more highly differentiated in pin flowers than in thrum flowers. No fruit was produced in emasculated netted flowers, suggesting the absence of apomixis. Our results indicate that H. acutangula is distylous, with a cryptic self‐incompatibility breeding system.     

Asymmetry in pollen flow promotes gender specialization in morphs of the distylous neotropical herb <Emphasis Type="Italic">Arcytophyllum lavarum</Emphasis> (Rubiaceae)

Distyly is a floral polymorphism, characterized by a reciprocal positioning between stigmas and anthers in different flowers, where two floral morphs, long-styled (pin) and short-styled (thrum) occur within the population. Distyly is suggested as one of the routes leading to the evolution of separate sexes in plants. In this evolutionary pathway, pollinators may disrupt the complementarity of pollen transfer between morphs. Consequently, the floral morphs gradually specialize as either male or female. A key process required for gender specialization in distylous plants is a deviation of the realized functional gender (i.e. the proportion of genes transmitted to the next generation via pollen donation and seed production) from the potential functional gender (i.e. the expected contribution of male and female function to reproductive success from the number of ovules or pollen grains produced by each morph). I selected the distylous herb Arcytophyllum lavarum (Rubiaceae) to determine if asymmetry in pollen flow promotes differences in seed production, pollen donation and a discrepancy between the potential and the realized functional genders in pin and thrum floral morphs. Pollen flow in A. lavarum is asymmetric and the pin morph is more efficient at performing cross-pollination than the thrum morph. Conversely, the thrum morph produced two times more seeds than the pin morph. Male and female contributions to the potential functional gender were equivalent in both morphs. However, the pin morph transmitted more genes through pollen donation and the thrum morph more through seed production than expected from their potential functional genders. These results support the hypothesis that if pollinators consistently promote asymmetric pollen flow between morphs over generations, it is possible that gender specialization may evolve to the extreme of dioecism from an original distylous condition.     

The effectiveness of heterostyly in preventing illegitimate pollination in dish-shaped flowers

Heterostyly is thought to have evolved because it confers efficiency of cross-pollination. While it can be an alternative to an incompatibility mechanism in tube-shaped flowers, its effectiveness in dish-shaped flowers, such as those of Fagopyrum esculentum, has not been demonstrated. Stigmatic pollen loads were examined over the daily course of pollination in a planted field of this crop species. Natural pollination by bees resulted in 23% of the pollen on pin flowers and 69% on thrum flowers being legitimate. Both flower morphs therefore received the two pollen types in about the same proportions. Pin pollen constituted 74% of the pollen delivered to stigmata, even though the two morphs are present in equal numbers. Pin flowers collected about 75 pollen, and thrum flowers about 25 pollen by the end of the day of anthesis. The net result was about 15 compatible pollen per flower on both floral morphs. These results indicate that heterostyly is associated with excess pin-pollen delivery rather than excess legitimate-pollen delivery in F. esculentum.     

Studies on heteromorphic self-incompatibility systems: Physiological aspects of the incompatibility system of Primula obconica

Summary In Primula obconica, a species with a heteromorphic self-incompatibility system, the distinction between compatible and incompatible pollen tubes takes place on the stigma surface in thrum flowers, self tubes growing randomly over the papillar cells. No differences were seen between self and cross tube behaviour on the pin stigma surface, but self tubes were inhibited within the stigmatic tissue with differences in tube length evident after 24 h. The stigma surface bears a proteinaceous pellicle and binds the lectin Concanavalin A. Removal of the stigma removes the incompatibility barrier in mature gynoecia. Bud pollination shows that pollen tubes cannot grow in a normal manner on immature stigmas; the random growth of tubes over the stigma surface resembles that of mature thrum selfs. Fewer compatible tubes reach the style base of young gynoecia and smaller numbers of seeds are set than in mature flowers. Pin and thrum pollen grains germinate and grow in aqueous media, thrum tubes growing longer than pin. The presence of H₃BO₄ and CaCl₂ in the growth medium promotes tube elongation and lengths equivalent to compatible styles can be obtained. The pollen grains have proteinaceous materials in their walls which diffuse out on moistening. Prolonged washing in aqueous media removes these materials but the incompatibility reaction remains unchanged. Thus the incompatibility reaction is between pollen tubes and stigmatic tissue and differs from the homomorphic, sporophytic system where pollen wall proteins elicit the incompatibility response.     

Heterostyly and pollen flow in Hypericum aegypticum (Guttiferae)

Distyly in Hypericum aegypticum is associated with a moderately strong incompatibility system. Pollen size is dimorphic and pin flowers produce more pollen grains than thrum flowers. A population studied in Morocco has plants with pin flowers and those with thrum flowers present in a 1: 1 ratio. In the field, stigmas of pin flowers receive 1.5 times as many pollen grains as those of thrum flowers. At least half the pollen grains in the pollen load on stigmas of both forms are incompatible grains originating from the same floral form. Although ample compatible pollen is received by stigmas of both forms to account for a full seed set, the overall pattern of pollen flow in the species does not fit the Darwinian ideal. In Hypericum , the unique occurrence of distyly in H. aegypticum, H. aciferum and H. russeggeri , the three species comprising section Adenotrias , and the derivative nature of these species within the genus, indicate that heterostyly has evolved within the genus and is not a primitive trait.     

Sequential variation in the components of reproductive success in the distylousJasminum fruticans (Oleaceae)

A 2-year study of three natural populations of the distylousJasminum fruticans showed that mean fruit and seed production were significantly greater in shortstyled plants (thrums) than in long-styled plants (pins). In this study, we investigated the role of four sequential factors which may differentially influence fruit and seed set in the two floral morphs: (1) differences in flowering phenology, (2) a limitation of pollen transfer towards pins, (3) a differential capacity of the two morphs to act through famale and male function and (4) differential fruit abortion in the two morphs. Fruit set was significantly influenced by differences in flowering phenology although there were no differences in flowering time between the two morphs. supplementary pollinations in a natural population significantly increased fruit set and reduced the difference in fruit set between the two morphs in relation to controls, indicating a limitation on pollen transfer which was most severe towards pin stigmas. In reciprocal crosses, seed set was significantly dependent on the paternal and maternal identity of the pin parent. There was no significant variation among thrums for their performance as male or female parent. Furthermore, individual pin plants with relatively high percentage seed set as female parents gave poor seed set as male parents and vice-versa. Whereas fruit removal had no effect on seed number in thrum plants, a greater proportion of viable seeds were produced on pin plants which were left to naturally mature their fruits than on pins which had fruits artificially removed, suggesting the occurrence of selective fruit abortion in pins but not in thrums. The initially greater maternal fitness of thrums due to their greater success as pollen recipients may thus be opposed by increased viable seed set in the pins due to factors acting after the pollination stage. The relative reproductive success of floral morphs in the distylousJ. fruticans is thus differentially influenced by ecological factors occurring at different stages of the reproductive process.     

甜荞pin型花与thrum型花雌雄蕊发育的比较研究

为从形态上研究甜荞(Fagopyrum esculentum)二型花发育的差异性,该文运用石蜡切片技术对甜荞pin型花和thrum型花大、小孢子发生和雌、雄配子体的发育过程进行观察比较.结果表明:(1)甜荞2种花的雌蕊、雄蕊发育的细胞学特征有很高的相似性,具直生胚珠、双珠被、厚珠心;大孢子四分体直线型排列,合点端为功能...     

Heterostyly inPrimula. 3. Pollen water economy: a factor in the intramorph-incompatibility response

Summary The pollens from pin (long-styled) and thrum (short-styled) flowers ofPrimula differ markedly in water economy. While pin pollen is little affected by atmospheric humidity, the germinability of thrum pollen in liquid medium is sensitive to the conditions experienced during the immediately preceding period, being depressed when the grains are partly desiccated, although capable of being restored with subsequent controlled rehydration. The tubes produced by incompletely rehydrated thrum pollen show abnormal growth forms, suggesting that the effect is on the membranes of the vegetative cell, a conclusion supported by observations on membrane state using the fluorochromatic reaction. Thrum pollen stripped of part of the material carried in the cavities of the exine by rinsing with a lipid solvent loses much of its capacity for the uptake of atmospheric water, indicating that, in this morph, some factor facilitating hydration is transferred from the sporophytic parent during pollen maturation.Implications of these differences in the physiology of the pin and thrum pollens for the functioning of the intramorph-incompatibility system are discussed.     

Heterostyly and Pollen-tube Interactions in Luculia gratissima (Rubiaceae)

Observations on the floral biology of Luculia gratissima (Rubiaceae)showed that this species is distylous with complementary positioningof anthers and stigmas in the two floral forms. Unusual featuresof distyly in this species include the larger size of the corolla,the stigma surface and the stigmatic papillae in the thrum flowerscompared to the pin ones. Stigmatic surfaces have similar secretionsbut they appear more copious in thrum than pin. The floral dimorphismwas accompanied by a very effective self-incompatibility systemand no seed was set on selfing. Seed number per capsule on crossingwas significantly greater in thrum flowers compared to pin.Incompatible pollen tubes were inhibited within 24 h at thebase of the stigma/top of the style in both morphs. Amputationof this region of the gynoecium removed the self-incompatibilityreaction in thrum but not pin flowers. Pollination with a mixtureof compatible and incompatible pollen and sequential pollinationwith self followed by cross pollen showed that there were interactionsbetween the two types of pollen tube. The presence of compatibletubes was found to cause the excessive swelling of the pollen-tubetip of the incompatible ones. The incompatible tubes did notappear to have any effect on the growth of compatible ones. Luculia gratissima, distyly, floral biology, self-incompatibility, pollen-tube interactions     

Pollen flow in a population of Primula vulgaris Huds.

A British population of Primula vulgaris was visited four times between 1971 and 1976 for study of the nature and functioning of distyly. The stainability and production of pollen from pins exceeded those of thrums. About 20% of pin pollen and 48% of thrum pollen was removed from anthers by insect visitors. Pins and thrums were present in a 1:1 ratio in 1971 but pins outnumbered thrums in 1976. Thrums produced more seeds per flower than pins though the number of ovules produced by each was similar. Two methods for collecting stigmas from open flowers and analyzing them for pollen loans produced somewhat different results. For pin stigmas, the pollen load consisted of 2–23% thrum pollen; for thrum stigmas, the pollen load consisted of 0–71% pin pollen with most stigmas having less than 50% pin pollen. In general, intermorph pollen flow is less than would be expected if pollen flow were random. It is probable that most intramorph pollen on stigmas is a result of self- or geitonogamous pollination. The extensive literature concerning the natural pollinators of the primrose is reviewed. Although Darwin's hypothesis concerning the functional significance of distyly in promoting intermorph pollination was never quantified, the pollen flow patterns observed in P. vulgaris are unexpectedly deviant and are similar to those patterns observed in several unrelated heterostylous species in other plant families.     

Mutual reproductive dependence of distylic Cordia leucocephala (Cordiaceae) and oligolectic Ceblurgus longipalpis (Halictidae, Rophitinae) in the Caatinga

Background and Aims

The close relationship between distylic Cordia leucocephala and the bee Ceblurgus longipalpis, both endemic to the Caatinga, north-east Brazil, was investigated, emphasizing reproductive dependence, morphological adaptations of the partners, and pollen flow.

Methods

In the municipality of Pedra, in the Caatinga of Pernambuco, the breeding system and reproductive success of C. leucocephala, its interaction with flower visitors and inter- and intramorph pollen flow were determined.

Key Results

The bee Ceblurgus longipalpis, the unique flower visitor and effective pollinator of self-incompatible Cordia leucocephala, presents morphological features adapted to exploit hidden pollen and nectar in the long and narrow corolla tubes. Pollen of low-level anthers is collected with hairs on prolonged mouthparts and pollen of high-level anthers with clypeus, mandibles, and labrum, showing pollen removal from both levels with the same effectiveness. In both morphs, this results in similar legitimate, i.e. intermorph cross-pollen flow. Illegitimate pollen flow to stigmas of pin flowers, however, was much higher than to stigmas of thrum flowers. Moreover, more illegitimate pollen was transported to stigmas of pin and less to those of thrum flowers when compared with legitimate pollen flow.

Conclusions

The study reveals a one-to-one reproductive inter-dependence between both partners. Data indicate that this relationship between bee species and plant species is one of the rare cases of monolecty among bees. Monotypic Ceblurgus longipalpis, the only rophitine species of Brazil, evolved prolonged mouthparts rare among short-tongued bees that enable them to access pollen from flowers with short-level anthers hidden for bees of other species, and nectar at the base of the flower tube.     

Stigma morphology in distylous and non-heterostylous species ofVillarsia (Menyanthaceae)

Stigma morphology was examined with the SEM in 14 of the 16 species ofVillarsia. In nine of the ten distylous species studied, stigmas of the floral morphs were strongly dimorphic in length, shape, configuration of the receptive surface, and in the size and density of their papillae. Thrum stigmas ofVillarsia, in contrast to those of most other distylous species, are not simply smaller versions of the conspecific pin stigmas, but generally exhibit an array of morph-specific characters. Thrum stigma lobes may be broader than those of pins, they may have undulate margins, lobes subdivided into secondary lobes, papillae more extensively distributed than in pins, and various combinations of these traits occur. The traits that distinguish thrum from pin stigmas achieve an increase in the receptive area and may enhance more efficient pollen capture by the shorter and less accessible thrum stigmas. The morphogenesis of the stigma shape dimorphism appears to involve processes more complex than inhibition of elongation in thrum styles. InVillarsia, the stigma dimorphisms are species-specific. No correlations were found between morphologies of the stigma and the different breeding systems in distylous species. Stigmas of the four non-heterostylous species examined resemble the thrum stigma type found in most distylousVillarsia species.     

Pollination biology and the impact of floral display, pollen donors, and distyly on seed production in Arcytophyllum lavarum (Rubiaceae)

In animal-pollinated plants, two factors affecting pollen flow and seed production are changes in floral display and the availability of compatible mates. Changes in floral display may affect the number of pollinator visits and the availability of compatible mates will affect the probability of legitimate pollination and seed production. Distyly is a floral polymorphism where long-styled (pin) and short-styled (thrum) floral morphs occur among different individuals. Distylous plants frequently exhibit self and intra-morph incompatibility. Therefore changes in morph abundance directly affect the arrival of compatible pollen to the stigmas. Floral morph by itself may also affect female reproductive success because floral morphs may display differences in seed production. We explored the effects of floral display, availability of neighboring compatible mates, and floral morph on seed production in the distylous herb ARCYTOPHYLLUM LAVARUM. We found that floral display does not affect the mean number of seeds produced per flower. There is also no effect of the proportion of neighboring legitimate pollen donors on seed production in pin or thrum flowers. However, floral morphs differed in their female reproductive success and the thrum morph produced more seeds. Hand pollination experiments suggest that differences in seed production between morphs are the result of pollen limitation. Future research will elucidate if the higher seed production in thrum flowers is a consequence of higher availability of pollen donors in the population, or higher efficiency of the pin morph as pollen donor.     

The distyly in Primula elatior (L.) Hill (Primulaceae), with a study of flowering phenology and pollen flow

Flowers of Primula elatior exhibit all the dimorphic traits typical of distyly. The difference in pollen production between pin and thrum flowers is not thought to be caused by the pollen size dimorphism. The percentage of pin pollen which is probably viable exceeds that of thrum pollen. In the population studied the morph ratio is 1:1, and plants are randomly dispersed with regard to morph type. Bumblebees are the main pollinators, and analysis of the stigmatic pollen load in naturally |xjllinated flowers shows that pin stigmas receive many more pollen grains than thrum stigmas. Intramorph pollination is considerable in pins, while thrums are subject to some differential pollination. Emasculation experiments have shown that intraflower pollination in the thrum morph is negligible. Aging of pin flowers has a reducing effect on their total pollen loads, while in thrums there is no change in total pollen load after the first days of anthesis.     

AN UNUSUAL KIND OF DISTYLY IN QUINCHAMALIUM CHILENSE (SANTALACEAE) ON VOLCÁN CASABLANCA,SOUTHERN CHILE

In mature flowers of the southern Andean parasitic herb, Quinchamalium chilense (Santalaceae), the stigmas and anthers are closer together in the pin morph than in the thrum morph. While the stigmas and anthers of the two morphs are in reciprocal positions as the flowers open, such reciprocity is lost as the result of post-anthesis allometric growth of the styles and stamens. Experimental pollinations reveal that both morphs of Q. chilense are self-compatible. Natural fruit set is higher on the pin morph. The latter is also statistically under-represented in natural populations with respect to a 1:1 ratio for pins and thrums. Pin flowers produce larger numbers of pollen grains than thrum flowers and pollen of pin flowers is smaller in size than that of thrum flowers. Higher fruit set on the pin morph is consistent with some tendency towards subdioecious breeding behavior, although an expected excess of geitonogamous pollinations on the pin morph might also be contributing to the difference in fruit set on the two morphs. The unusual floral morphology of Q. chilense could have evolved as a result of selection for larger flowers by certain pollinator groups less likely to effect geitonogamous pollination. Alternatively, extended development of post-anthesis flowers might be a reflection of selection for an array of flower sizes on individual inflorescences, producing a target effect for pollinator attraction. The evolution of such inflorescence morphology would have been facilitated by the fact that a trend in the direction of subdioecious breeding behavior accrues the same outcrossing advantages as strict distyly. Precise information on periods of stigma receptivity is required to further our understanding of the floral morphology of Q. chilense.     

Reproductive conflicts ofPalicourea padifolia (Rubiaceae) a distylous shrub of a tropical cloud forest in Mexico

We studied a population of the distylousPalicourea padifolia (Rubiaceae) in a cloud forest remnant near Xalapa City, Veracruz, México to explore possible asymmetries between floral morphs in the attractiveness to pollinators, seed dispersers, nectar robbers, floral parasites, and herbivores. We first assessed heterostyly and reciprocal herkogamy by measuring floral attributes such as corolla length (buds and open flowers), style and anther heights, stigma and stamen lengths and the distance between the anther tip to the stigma lobe. We then estimated floral and fruit attributes such as flower size, anther height, number and size of pollen grains, fruit size, seed size, nectar production, and flower and fruit standing crops to assess differences between floral morphs in attracting and effectively using mutualistic pollinators and seed dispersers. Also, floral parasitism and nectar robbing were assessed in this study as a measure of flower attractiveness to antagonists. The system seems to conform well to classical heterostyly (e.g. reciprocal stamen/style lengths, pollen and anther dimorphism, intramorph incompatibility) yet, there were several tantalizing differences observed between pin and thrum morphs. Thrum flowers have longer corollas and larger but fewer pollen grains than pin flowers. Both morphs produced the same total number of inflorescences, developed the same number of buds, and opened the same number of flowers per inflorescence during the flowering season. Nectar production and sugar concentration were similar between floral morphs but the reward was not offered symmetrically to floral visitors throughout the day. Nectar concentration was higher in pin flowers in the afternoon. The numbers of developing, fully developed, and ripe fruits were the same between floral morphs, however, fruits and seeds were larger than those of thrums. The incidence of fly larvae was higher among thrum flowers and damage by nectar robbing was the same between floral morphs. Fruit abortion patterns of flowers manually pollinated suggest intra-morph sterility (self and intramorph incompatibility). There were no differences between morphs in fruit and seed set per flower following legitimate pollination although thrums were more leaky than the pins (intramorph compatibility).