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.     

The control of incompatibility in distylous Pulmonaria affinis Jordan (Boraginaceae)

In P. affinis, pin pollen is shorter on average than thrum pollen. Pins have more coronal hooks on stigmatic papillae than thrums, but gaps between papillae are relatively smaller for thrums. Pin stigmas receive more pollen than thrum stigmas. Thrum stigmas receive more (dissortive) pin pollen, but pin stigmas are assortively pollinated. Pollen only germinates when trapped below papilla coronas. On thrum stigmas, most trapped pollen is pin. Pollen germination is better on thrum stigmas than pin stigmas, and thrum stigmas show a close relationship between numbers of legitimate pollen grains, numbers of germinating grains, and numbers of pollen tubes in the style. There is no inhibition of illegitimate pollen germination. Illegitimate pollen tubes are inhibited in the style. Incompatibility operates by a combination of dissortive pollination, dissortive pollen trapping, and stylar pollen tube inhibition. All heteromorphic features differing between pins and thrums are implicated in the inhibition of within-morph fertilization in thrums.     

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.     

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.     

Pollen Flow,Fecundity, and the Adaptive Significance of Heterostyly in Palicourea padifolia (Rubiaceae)1

Palicourea padifolia is a distlous shrub visited primarily by hummingbirds and bees in mid-elevation rain forests in Costa Rica. At Las Cruces Biological Station, the population of P. padifolia is composed of equal numbers of pin and thrum plants and morphs are randomly distributed. Like the majority of distylous species, P. padifolia exhibits a self and intramorph-incompatible mating system. The analysis of stigmatic pollen loads obtained from emasculated flowers shows that pollen flow between floral morphs is disassortative, which supports the Darwinian hypothesis concerning the adaptive significance of heterostyly. Pins experience greater disassortative pollination than thrums. Pins also set more seed than thrums, suggesting that the higher frequency of compatible pollen deposited on pin stigmas results in greater fecundity; alternatively, greater seed set in pins could be due to the differential allocation of resources to male and female function between morphs. Overall, seed set for the Las Cruces popularion of P. padifolia is much lower than the potential maximum. Factors which could contribute to seed set limitation include the frequency and/or spatial pattern of pollinator visits, pollen availability, and resource availability.     

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.     

FEATURES OF POLLEN FLOW IN DIMORPHIC SPECIES OF LYTHRUM SECTION EUHYSSOPIFOLIA

The North American Lythrum lineare L., L. alatum Pursh, L. curtissii Fernald, and L. californicum T. & G. have distylous flowers that differ in a number of traits. In the two species examined, pins have a stronger incompatibility system than thrums. Pins outnumber thrums in natural populations, but the ratio of the two may change radically during the course of a year, probably as a result of sexual reproduction. Exotic honeybees visiting L. californicum exhibited preferential collection of pin pollen over thrum pollen. The relative proportion of pin and thrum pollen grains transferred to stigmas is not dependent upon the proportion in which these pollen grains are produced in a population. Analyses of stigmatic pollen loads of L. lineare and L. californicum indicate very high levels of intramorph pollen flow. Although distyly is likely derived from tristyly in Lythrum, pollen flow patterns in trimorphic species seem to operate more “efficiently” than in dimorphic ones. It is probable that distyly has evolved from tristyly several times in the Lythraceae, but comparisons between pollen flow patterns in distylous species and those in a tristylous species provide no clear insights into the selective pressures that have led to this fundamental change in floral morphology and reproductive system.     

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).     

Pollen flow in the distylous<Emphasis Type="Italic"> Palicourea fendleri</Emphasis> (Rubiaceae): an experimental test of the Disassortative Pollen Flow Hypothesis

The Disassortative Pollen Flow Hypothesis proposed by Darwin postulates that the relative position of anthers and stigmas in distylous flowers enhances pollen flow between flowers of different morphs (legitimate pollination), in comparison to flow between flowers of the same morph (illegitimate pollination). In order to test this hypothesis, we measured pollen transport, mediated by a trained Copper-rumped Hummingbird (Amazilia tobaci), between flowers of the distylous Palicourea fendleri under laboratory conditions. In individual tests, we offered to the hummingbird a pollen donor flower and two emasculated recipient flowers in a controlled sequence. After each foraging bout, we counted the number of pollen grains transported from the donor flower to the stigmas of both recipient flowers. In agreement with Darwin's hypothesis, we found that hummingbirds transport pollen of "pin" flowers in significantly higher numbers to legitimate "thrum" stigmas, even if previously visiting a "pin" flower. However, "thrum" pollen was deposited in greater numbers on illegitimate "thrum" stigmas. We interpret this asymmetry largely as the consequence of floral morphology; pollen flow was greater between anthers and stigmas that exhibit greater spatial matching. In P. fendleri, the position of floral organs along the corolla tube does not always precisely correspond. In our experimental system, the probability that the pollinator extracts a pollen grain from the anther and the probability of self-pollination were both dependent on the type of floral morph. We discuss the relevance of the latter findings in relation to other studies of pollen flow in heterostylous species.     

An unusual homostyle inHedyotis caerulea (Rubiaceae)

Hedyotis caerulea, a spring flowering herb widely distributed in eastern North America, has distylous flowers that differ by a number of morphological and physiological traits. The presence of a strong incompatibility system is indicated by the fact that intramorph crosses or self-pollinations produced little or no seed and intermorph crosses produced copious seed. An unusual homostyle was located that had most floral characters intermediate between pin and thrum flowers, although its pollen size was that of pin. The homostyle was only moderately self-compatible, and its pollen did not behave as pin pollen on thrum stigmas. It appears that, despite their intermediate position and morphology, the homostyle stigmas were fundamentally pin. Although the exceptional rarity of the homostyle suggests that it is an inadaptive failure, workers should watch for its further occurrence since additional study of it may provide insights into the genetic and physiological basis of heterostyly in theRubiaceae.     

REPRODUCTIVE BIOLOGY OF DISTYLOUS PARTRIDGEBERRY,MITCHELLA REPENS

Long-styled (pin) and short-styled (thrum) plants in populations of Mitchella repens from North Carolina and New York displayed strongly clumped spatial dispersion. This distribution pattern results from the tendency of these prostrate perennials to spread by production of trailing stems with adventitious roots. Both morphs, in both populations, exhibited natural fruit set exceeding 86%. This percentage was not increased by hand-pollination. Although the number of ovules per pair of ovaries was fixed at eight in each morph, numbers of seeds per fruit in naturally pollinated flowers differed significantly between pins (4.3) and thrums (6.4) in the North Carolina population. In the New York population, no significant differences were found (pins had 5.0 seeds per fruit; thrums, 4.4). Artificial pollinations in both populations showed low seed set in intramorph cross-pollinations as compared with intermorph crosses. The flowers of M. repens were visited by native species of Bombus, which visited many flowers in each patch of plants. These insects moved frequently from patch to patch, effecting intermorph cross-pollination and maintaining high levels of seed set. Movement among patches may be promoted by the dispersion of nectar rewards, with flowers about to open or just opened providing maximum amounts of nectar. Calculations of functional gender suggested that in the North Carolina population, thrums contributed more than 75% of the genes transmitted by ovule production. This contrasts strongly with previous studies of unequal sexual contributions in distylous taxa, which have demonstrated greater female contributions by pins. In the New York population, however, nearly equal contributions by pins and thrums through pollen and ovule production occurred, a situation similar to that found in most distylous species. This appears to be the first demonstration of variation in functional gender between populations of a single species.     

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.     

Quantitative evaluation of reciprocal herkogamy in the distylous species, Hedyotis caerulea (Rubiaceae)

Hedyotis caerulea possesses two distinct floral morphs that are generally found in equal numbers in naturally occurring populations. Flowers either possess a relatively long style and short anthers, called a “pin,” or a short style and long anthers, called a “thrum.” This placement of reproductive organs is considered herkogamous and distylous, as it encourages outcrossing by restricting pollination to individuals of the alternate morph. Numerous species have been described as distylous without quantitative data establishing stigma-anther reciprocity. Here we assess those assumptions in H. caerulea by measuring stigma height, anther height and a suite of additional floral traits across multiple localities. All populations surveyed were isoplethic, although variation among them was present in all floral traits measured as well as for pollen diameter, pollen count, flower dry weight, and seed set. Pins produced smaller pollen than thrums, but made more of them. Thus, the total volume of pollen was similar for pins and thrums, and seed set was similar, suggesting that each morph has equal male and female fitness with no movement towards dioecy. Given a significant degree of variation found in the morphometric analysis, and that two of the three measures used to assess reciprocity were not consistent with predictions of precise symmetry, extensive change is possible where selection is acting on these traits. Even so, the distylous mating system in H. caerulea appears to be stable.     

POLLEN FLOW AND FECUNDITY IN POPULATIONS OF LITHOSPERMUM CAROLINIENSE

Stigmatic pollen loads of pin and thrum forms of distylous Lithospermum caroliniense (Walt.) MacMill. generally have very large proportions of incompatible pollen grains. Assortative pollination probably results from large components of self-pollination rather than geitonogamous pollinations, because pollen loads of large and small individuals are the same, although large individuals would be expected to experience more geitonogamous pollinator flights than small individuals. The distylous reproductive system appears relatively insensitive to changes in pollinator activity and preferential pollen flow between pins and thrums cannot be demonstrated. In contrast to the relatively uniform proportions of pin and thrum pollen on stigmas, absolute pollen loads vary substantially in different years and localities. Extremely low fecundity, which appears to be characteristic of this species, may result in part from lack of pollinator activity. However, even under optimal conditions for pollination, fecundity is less than 20%. Although L. caroliniense appears to have an inefficient pollination system, intrinsic low fecundity may represent a more critical feature of the life history.     

Pollen donation patterns in a tropical distylous shrub (PSYCHOTRIA SUERRENSIS; RUBIACEAE)

Selection on male function has been invoked to explain various floral features, including number of flowers, flower size, and flower color. Here I describe two experiments designed to examine the efficiency of distyly in promoting male floral function, as measured by successful pollen dispersal to stigmas. In both experiments, I performed emasculations to control the type of pollen locally available in a natural population of Psychotria suerrensis, a tropical shrub. In the “natural-recipients” experiment, I allowed each floral morph to donate pollen on alternate days to emasculated flowers of each morph. In the “paired-recipients” experiment, I attached paired cuttings of each morph to individual donor plants. The results of both methods were consistent. Pollen borne on low anthers (from pin plants) was transferred most efficiently to low stigmas (on thrum plants). Pollen borne on high anthers (from thrum plants) was dispersed in equal amounts to flowers of both morphs. The results suggest that distyly is only partially effective in achieving efficient pollen donation. Male function of pins is enhanced by the polymorphism, but male function of thrums is not. A supplemental pollination experiment illustrates that seed set in this species is predominantly pollen limited, reducing the importance of male function, in comparison with species where seed set is primarily resource limited.     

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.     

Gender specialization and distyly in hoary puccoon,LITHOSPERMUM CROCEUM (Boraginaceae)

This 2-yr study of gender and its relation to the sizes of pin and thrum plants in Lithospermum croceum was performed in central Michigan. The population was composed of 51-52% thrums, 42-43% pins, and ≈6% homostyles in 1988 and 1989. Pins produced more flowers and fruits than thrums, and a greater proportion of their ovaries produced more than one nutlet. However, the number of fruits produced by pins and thrums in 1988 did not differ when plant size is a covariate in ANCOVA. The number of seeds produced by plants in 1989 is also unaffected by floral morph when size is a covariate. Instead, plant size is the most important predictor of fecundity in both years. The average percent fruit sets (fruits/ovaries) of the morphs did not differ in either year. Herbivory was more common in 1988 than in 1989, but there was no difference in the frequency with which pins and thrums were attacked. Furthermore, the effect of herbivory on fecundity did not differ for the morphs. The fecundity of neither morph was limited by pollen in 1989. Apparent gender specialization was a consequence of subtle differences in the vegetative sizes of the morphs.     

濒危植物安徽羽叶报春两种花型的繁育特性及其适应进化

二型花柱的维持机制和自然选择压力多年来一直是生态学和进化学研究领域的热点之一。通过实验室栽培和野外观察统计相结合的方法,对安徽羽叶报春两种花型(长柱花和短柱花)的形态特征、花粉活力、柱头可授性、花粉/胚珠比、自然授粉及结籽能力、自交亲和性等繁育特性进行了比较研究。结果表明:长、短柱花的花冠直径和裂片宽无明显差异,而花冠筒、雌蕊和雄蕊高、花粉数目及大小、P/O比均有显著差异。在自然条件下,长柱花所接受的总花粉数要明显高于短柱花的总花粉数,但所接受的异型花花粉数和平均每果结籽数两者无显著差异。长柱花和短柱花的花粉和柱头活力相似,均能在较长时间内维持较高活力,仅在开花末期显著下降。两种花型的花在自花授粉、同型异花授粉、异型花授粉条件下均能结籽,但异型花授粉的结籽数均明显高于自花授粉和同型异花授粉结籽数。在长柱花各种授粉方式中,花粉萌发率无明显差异,但异型花花粉管的生长速度明显比同型异花花粉和自花花粉的快,而在短柱花柱头上表现为异型花授粉的萌发率最高,但只要萌发后在花柱中的生长速度无显明差异。此外,综合上述结果,对二种花型花部综合征的维持机制及自然选择压力进行了探讨。     

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.     

HETEROSTYLY IN LITHOSPERMUM COBRENSE (BORAGINACEAE)

Lithospermum cobrense Greene exhibits the floral dimorphisms and strong self-incompatibility system typical of most distylous plants. Flowers of the long styled (pin) form produce smaller pollen grains but more pollen per flower than flowers of the short styled (thrum) form. Corollas of pins and thrums are equal in size. The breeding system of L. cobrense is less specialized than, and probably ancestral to, that of L. caroliniense.