Pollinator response to female and male floral display in a monoecious species and its implications for the evolution of floral dimorphism

Pollinator-mediated selection has been hypothesized as one cause of size dimorphism between female and male flowers. Flower number, ignored in studies of floral dimorphism, may interact with flower size to affect pollinator selectivity. In the present study, we explored pollinator response, and estimated pollen receipt and removal, in experimental populations of monoecious Sagittaria trifolia, in which plants were manipulated to display three, six, nine or 12 female or male flowers per plant. In this species, female flowers are smaller but have a more compressed flowering period than males, creating larger female floral displays. Overall, pollinators preferred to visit male rather than female displays of the same size. Both first visit per foraging bout and visitation rates to female displays increased with display size. However, large male displays did not show increased attractiveness to pollinators. A predicted relationship that pollen removal, rather than pollen receipt, is limited by pollinator visitation was confirmed in the experimental populations. The results suggest that the lack of selection on large male displays may affect the evolution of floral dimorphism in this species.     

Pollinator responses to variation in floral display and flower size in dioecious Sagittaria latifolia (Alismataceae)

In animal-pollinated plants with unisexual flowers, sexual dimorphism in floral traits may be the consequence of pollinator-mediated selection. Experimental investigations of the effects of variation in flower size and floral display on pollinator visitation can provide insights into the evolution of floral dimorphism in dioecious plants. Here, we investigated pollinator responses to experimental arrays of dioecious Sagittaria latifolia in which we manipulated floral display and flower size. We also examined whether there were changes in pollinator visitation with increasing dimorphism in flower size. In S. latifolia, males have larger flowers and smaller floral displays than females. Visitation by pollinators, mainly flies and bees, was more frequent for male than for female inflorescences and increased with increasing flower size, regardless of sex. The number of insect visits per flower decreased with increasing floral display in males but remained constant in females. Greater sexual dimorphism in flower size increased visits to male inflorescences but had no influence on the number of visits to female inflorescences. These results suggest that larger flower sizes would be advantageous to both females and males, and no evidence was found that females suffer from increased flower-size dimorphism. Small daily floral displays may benefit males by allowing extended flowering periods and greater opportunities for effective pollen dispersal.     

When looks can kill: the evolution of sexually dimorphic floral display and the extinction of dioecious plants

Dioecious plants (with separate male and female individuals) more often have drab, inconspicuous flowers than related bisexual plants. Models indicate, however, that similar conditions favour the evolution of showy floral displays in dioecious and bisexual plants. One difference, however, is that dioecious plants may evolve floral displays that are sexually dimorphic. We show that males are more likely to evolve showy flowers than females in animal-pollinated plants, especially when pollinators are abundant. We demonstrate that this dimorphism places showy dioecious plants at a much higher risk of extinction during years of low pollinator abundance because pollinators may fail to visit female flowers. The higher extinction risk of showy dioecious plants provides an explanation for the fact that dioecious plants that do persist tend to have inconspicuous flowers and are more often wind pollinated. It may also help explain why dioecious plants are less species-rich than related bisexual plants.     

Pollinator response to male floral display size in two Sagittaria (Alismataceae) species

One hypothesis for the evolution of maleness in plants postulates the following: male plants appear that have re-allocated resources from female parts into a larger number of male flowers, creating a larger floral display. Pollinators respond “dramatically” to the increased display, driving the spread of males in the population (Bawa, K. S., 1980, Annual Review of Ecology and Systematics 11:15–40). To test this, we measured the total number of flowers and the size of male displays in dioecious Sagittaria latifolia and monoecious S. australis. We also measured how fast visitors arrived at “target” flowers in the displays. Then we used the Cox Model, a failure time analysis procedure, to analyze the relationship between visitor arrival and display size. We found that male display sizes were somewhat larger in the dioecious than the monoecious plants, but this was due to more compressed blooming rather than to a larger total number of flowers. The visitors to both plants were similar arrays of generalist bees. Visitors did not show the predicted “dramatic” response, however, but rather a plateauing response to larger display sizes, so our results do not support the hypothesis. Reviewing the literature, we found no reports of the “dramatic” response the hypothesis asserts. Instead, relative insensitivity to display size is the rule.     

The role of resources and architecture in modeling floral variability for the monoecious amphicarpic Emex spinosa (Polygonaceae)

Determining the sources of floral variation is crucial to the understanding of floral evolution. Architectural effects and phenotypic plasticity in development can play an important role in intraplant floral variation, giving rise to gender dimorphism or sexual specialization. Amphicarpic plants have another source of floral variation that could also be influenced by positional effects. We studied the effects of resource availability and architecture in intraplant floral variability in two ecotypes of the amphicarpic Emex spinosa. Male flowers were smaller than females, irrespective of position or resource availability. Emex spinosa shows gender dimorphism not influenced by positional effects. Flower size differences among positions were mainly due to architecture, because the effects of resources on flower size were minimal. Architectural effects caused a decrease in female flower size from ground to apical positions but an increase in most male traits that resulted in sexual specialization at the end of flowering. In general, the ecotypes were similarly affected by resources or architecture. Differences between subterranean and aerial female flowers seem also to be a consequence of architecture. Our results contribute to the evidence that resource limitation is an overestimated effect and that architectural effects must be considered in studies of floral or fruit variation.     

Size and sex of floral displays affect insect visitation rates in the dioecious Australian alpine herb, Aciphylla glacialis

Differences in floral display size between male and female plants in dioecious species are often considered to be the result of competition within and between male and female plants to attract insects, although this hypothesis is rarely tested. In a field study of the alpine dioecious herb Aciphylla glacialis , insect visitation rates were found to increase with increasing floral display, as predicted. Dipterans were the most common visitors to male and female inflorescences, both in terms of individuals visits (2083 out of 2581 total visits by insects), and species number (20 morphospecies, potentially 22 species). Larger male inflorescences attracted 1.7 times as many insects in total, and 3.1 times more visits by the most common flower visitor, Musca vetustissima than did female inflorescences, but equal number of visits by the next most common flying visitors, Poecilohetaerus aquilius and Tephritis poenia. There was no difference in the amount of time M. vetustissima individuals spent on male and female inflorescences, even though male inflorescences have more flowers. Larger displays (four and eight inflorescences) of either sex attracted more visits than smaller ones (one inflorescence), although the rate of increase in visitation rate with increasing floral display declined. The response of insects to increasing floral display does not support the predicted escalating or proportionate increasing rate of visitation of some models for the evolution of dimorphism in floral displays in dioecious plants.     

Small but attractive: female‐biased nectar production and floral visitors in a dimorphic shrub

• In sexually dimorphic species, hermaphrodite flowers in gynodioecious species or male flowers in dioecious species are often larger and produce more nectar than their conspecific female flowers. As a consequence, hermaphrodite or male flowers frequently receive more pollinator visits.
• Sex ratio, flower size, floral display, nectar production and floral visits were evaluated in two natural populations of Fuchsia thymifolia, a morphologically gynodioecious but functionally subdioecious insect‐pollinated shrub.
• Sex ratio did not differ from the expected 1:1 in the two studied populations. As expected, hermaphrodite flowers were larger than female flowers, but in contrast to the general pattern, hermaphrodite flowers did not produce nectar or produced much less than female flowers. Flower visitors were flies (68%) and bumblebees (24%), both of which showed a preference for female flowers. No sex difference was detected in either flower longevity or floral display across the flowering season.
• Higher nectar production by females may attract more pollinators, and may be a strategy to enhance female reproductive success in this species. Finally, floral dimorphism and insect preferences did not seem to hamper the maintenance of sub‐dioecy or prevent the evolution of dioecy in F. thymifolia.

     

雌雄异熟植物露蕊乌头开花时间对雌雄功能期及表型性别的影响

开花时间决定了植物雌雄功能的交配机会, 最终影响繁殖成功。交配环境假说认为雌雄异熟植物开花时间的差异能引起植物表型性别的变异, 改变种群内的交配环境, 影响植物对雌雄功能的最佳性分配。为了研究开花时间对雌雄异熟植物的雌雄性别时期及表型性别的影响, 本文以毛茛科雄性先熟植物露蕊乌头(Aconitum gymnandrum)为实验材料, 记录了雄性和雌性功能期, 分析了植株开花时间、花的雌雄功能期和表型性别的关系。结果表明: 在植物同一花序内, 较晚开放的花有更长的雄性期和更短的雌性期, 性分配在时间上偏雄。雌雄功能期在时间上的相对分配随植物开花时间的变化表现出相似的趋势： 较晚开的花或较晚开花的个体, 花的雄性功能期相对于雌性功能期更长, 在时间上更偏向雄性功能。而且, 开花时间的差异影响种群内花的性比和植物个体的表型性别动态。随着开花时间由早到晚的变化, 种群内早期以雄花为主,末期以雌花为主, 种群内性别环境由偏雄向偏雌变化, 因此植株个体的平均表型性别则从偏雌转向偏雄。本文结果支持交配环境假说, 雄性先熟的露蕊乌头开花早期, 种群内花的性别比偏雄, 种群表型性别环境偏雄, 因而植物个体平均表型性别偏雌, 性别分配(即时间分配)偏向雌性功能, 而晚开花个体的平均性别偏雄, 更偏向雄性功能的分配。     

Phenotypic and genetic correlations among floral traits in two species of Thalictrum

The evolution of dioecy in plants is expected to be followed by sex-specific selection, leading to sexual dimorphism. The extent of the response to selection depends on the genetic covariance structure between traits both within and between the sexes. Here I describe an investigation to determine phenotypic and genetic correlations between reproductive traits within cryptically dioecious Thalictrum pubescens and within morphologically dioecious T. dioicum. Females of T. pubescens produce flowers having stamens and pistils, appearing hermaphroditic. Genetic correlations were estimated as family-mean correlations among paternal half-sib families. Positive phenotypic and genetic correlations between parts of the same reproductive organs, as the anther and filament of the stamen, indicate developmental associations between these traits in both species. Negative genetic correlations were detected between pistil number and size of reproductive organs in T. dioicum and showed the same direction, but not significance, in T. pubescens. There was a negative phenotypic correlation between the number of stamens and the number of pistils within female flowers of T. pubescens. Within T. pubescens, there was a positive genetic correlation between the number of stamens in males and the number of pistils in females, indicating that floral evolution in males and females may not be independent in this species.     

Selection on floral characters in natural Spanish populations of Silene latifolia

In insect-pollinated plants, floral characters are expected to play an important role in paternal and maternal reproductive success. Bateman's principle states that male reproductive success increases with more mating opportunities, while female reproductive success is limited by the amount of resources available to produce progeny, thus there should be greater selection on male floral characters than on female. In the case of the dioecious plant Silene latifolia, floral characters are likely to be influenced by its association within its native European range with moths of the genus Hadena, which serve as both pollinators and seed predators. The present study addresses relationships between male and female reproductive success, spatial location and floral characters (corolla, calyx and claw) over a 2-year period in two Spanish populations of S. latifolia in the presence of Hadena moths. A maximum likelihood paternity analysis using genetic variation at six allozyme markers showed heterogeneity in male reproductive success. There was much less variation in female reproductive success. When this analysis was extended to include interplant distance as a causal factor underlying variation in male success, we found that successful pollination tended to be limited to nearby females, in accordance with exponential decay of pollen dispersal with increasing distance. When the paternity analysis included floral characters as a causal factor underlying variation in male success, our data showed little evidence for directional selection, but there was stabilizing selection in one of the two years for calyx diameter. Selection on female characters varied widely between sites and years, in most of the site/year combinations there was little selection on female floral characters; however, in one site/year there was evidence for selection on all three floral characters. We conclude that pollinators visit flowers that are close together, and that while floral characters are important for the attraction of pollinators, larger flowers do not necessarily attract more pollinators at all sites and that variation among sites and years makes difficult any conclusions about the long-term importance of the predictions suggested by Bateman's principle.     

Effects of floral herbivory, limited pollination, and intrinsic plant characteristics on phenotypic gender in Sanicula arctopoides

Sexual expression in hermaphroditic plants is often a function of environmental factors affecting individuals before or during flowering. I tested for the effects of floral herbivory and lack of pollination in early umbels on the relative proportions of hermaphroditic and staminate (male) flowers produced on later umbels by Sanicula arctopoides, a monocarpic, andromonoecious perennial. Neither floral herbivory or lack of early pollination had a significant effect on the ratio of the two floral morphs, but the probability of producing staminate flowers on late umbels was strongly and positively related to plant size measured just prior to floral initiation and prior to herbivory. Plant size was also negatively correlated with flowering date. I suggest that producing staminate flowers on late umbels should benefit large early-blooming plants more than small late-blooming plants because more mating opportunities occur during the period when these flowers release pollen. Although herbivory did not cause labile changes of sex, whole plant phenotypic gender was still strongly affected by various forms of treatment. Sex-biased herbivory or lack of pollination rendered plants more or less phenotypically male, depending on which tissues were affected. Deer and pollen-feeding mites preferentially remove male tissues while hymenopteran seed predators preferentially remove female tissues. I conclude that combinations of herbivores could have counteracting or compounding effects on plant gender, and these effects may change the rankings of male and female reproductive success within populations. Received: 20 February 1996/Accepted: 30 July 1996     

Active pollination favours sexual dimorphism in floral scent

Zoophilous flowers often transmit olfactory signals to attract pollinators. In plants with unisexual flowers, such signals are usually similar between the sexes because attraction of the same animal to both male and female flowers is essential for conspecific pollen transfer. Here, we present a remarkable example of sexual dimorphism in floral signal observed in reproductively highly specialized clades of the tribe Phyllantheae (Phyllanthaceae). These plants are pollinated by species-specific, seed-parasitic Epicephala moths (Gracillariidae) that actively collect pollen from male flowers and pollinate the female flowers in which they oviposit; by doing so, they ensure seeds for their offspring. We found that Epicephala-pollinated Phyllanthaceae plants consistently exhibit major qualitative differences in scent between male and female flowers, often involving compounds derived from different biosynthetic pathways. In a choice test, mated female Epicephala moths preferred the scent of male flowers over that of female flowers, suggesting that male floral scent elicits pollen-collecting behaviour. Epicephala pollination evolved multiple times in Phyllantheae, at least thrice accompanied by transition from sexual monomorphism to dimorphism in floral scent. This is the first example in which sexually dimorphic floral scent has evolved to signal an alternative reward provided by each sex, provoking the pollinator''s legitimate altruistic behaviour.     

How to be an attractive male: floral dimorphism and attractiveness to pollinators in a dioecious plant

Background  

Sexual selection theory predicts that males are limited in their reproductive success by access to mates, whereas females are more limited by resources. In animal-pollinated plants, attraction of pollinators and successful pollination is crucial for reproductive success. In dioecious plant species, males should thus be selected to increase their attractiveness to pollinators by investing more than females in floral traits that enhance pollinator visitation. We tested the prediction of higher attractiveness of male flowers in the dioecious, moth-pollinated herb Silene latifolia, by investigating floral signals (floral display and fragrance) and conducting behavioral experiments with the pollinator-moth, Hadena bicruris.     

SEX ALLOCATION IN THE MONOECIOUS HERB BEGONIA SEMIOVATA

Sex-allocation models predict that the evolution of self-fertilization should result in a reduced allocation to male function and pollinator attraction in plants. The evolution of sex allocation may be constrained by both functional and genetic factors, however. We studied sex allocation and genetic variation for floral sex ratio and other reproductive traits in a Costa Rica population of the monoecious, highly selfing annual Begonia semiovata. Data on biomass of floral structures, flower sex ratios, and fruit set in the source population were used to calculate the average proportion of reproductive allocation invested in male function. Genetic variation and genetic correlations for floral sex ratio and for floral traits related to male and female function were estimated from the greenhouse-grown progeny of field-collected maternal families. The proportion of reproductive biomass invested in male function was low (0.34 at flowering, and 0.07 for total reproductive allocation). Significant among-family variation was detected in the size (mass) of individual male and female flowers, in the proportion of male flowers produced, and in the proportion of total flower mass invested in male flowers. Significant among-family variation was also found in flower number per inflorescence, petal length of male and female flowers, and petal number of female flowers. Except for female petal length, we found no difference in the mean value of these characters between selfed and outcrossed progeny, indicating that, with the possible exception of female petal length, the among-family variation detected was not the result of variation among families in the level of inbreeding. Significant positive phenotypic and broad-sense genetic correlations were detected between the mass of individual male and female flowers, between male and female petal length, and between number of male and number of female flowers per inflorescence. The ratio of stamen-to-pistil mass (0.33) was low compared to published data for autogamous species with hermaphroditic flowers, suggesting that highly efficient selfing mechanisms may evolve in monoecious species. Our results indicate that the study population harbors substantial genetic variation for reproductive characters. The positive genetic correlation between investment in male and female flowers may reflect selection for maximum pollination efficiency, because in this self-pollinating species, each female flower requires a neighboring male flower to provide pollen.     

Sexual dimorphism in white campion: deletion on the Y chromosome results in a floral asexual phenotype

White campion is a dioecious plant with heteromorphic X and Y sex chromosomes. In male plants, a filamentous structure replaces the pistil, while in female plants the stamens degenerate early in flower development. Asexual (asx) mutants, cumulating the two developmental defects that characterize the sexual dimorphism in this species, were produced by gamma ray irradiation of pollen and screening in the M1 generation. The mutants harbor a novel type of mutation affecting an early function in sporogenous/parietal cell differentiation within the anther. The function is called stamen-promoting function (SPF). The mutants are shown to result from interstitial deletions on the Y chromosome. We present evidence that such deletions tentatively cover the central domain on the (p)-arm of the Y chromosome (Y2 region). By comparing stamen development in wild-type female and asx mutant flowers we show that they share the same block in anther development, which results in the production of vestigial anthers. The data suggest that the SPF, a key function(s) controlling the sporogenous/parietal specialization in premeiotic anthers, is genuinely missing in females (XX constitution). We argue that this is the earliest function in the male program that is Y-linked and is likely responsible for "male dimorphism" (sexual dimorphism in the third floral whorl) in white campion. More generally, the reported results improve our knowledge of the structural and functional organization of the Y chromosome and favor the view that sex determination in this species results primarily from a trigger signal on the Y chromosome (Y1 region) that suppresses female development. The default state is therefore the ancestral hermaphroditic state.     

The allometry of flower size dimorphism in dioecious Dombeya species on La Réunion

In this paper we examine whether variation in male and female flower size follows an allometric relation for 10 dioecious species in the genus Dombeya endemic to La Réunion. Male flowers are significantly larger than female flowers and the degree of dimorphism varies significantly across species. There is a significant allometric relationship between male and female flower size: as mean flower size decreases the degree of flower size dimorphism increases. This is the first study to document an allometric relationship between male and female flower size in unisexual plants. We discuss this allometric relationship in relation to two characteristics frequently observed in dioecious flowers: flower size dimorphism is common in unisexual plants and dioecious species often have smaller flowers than hermaphrodites.     

Variation in floral sex allocation in Polygonatum odoratum (Liliaceae)

BACKGROUND AND AIMS: It is well known that resource allocation to male and female functions can be highly variable in hermaphroditic plants. The purpose of this study was to investigate variations in sexual investment at different levels (flower, plant and population) in Polygonatum odoratum, a plant with sequentially opening flowers. METHODS: Pollen and ovule production in base, middle and top flowers of P. odoratum flowering shoots from two natural populations were quantified. Plant measurements of phenotypic and functional gender were calculated in both populations. Total leaf number was used to investigate the relationship between gender assessments and plant size. KEY RESULTS: Pollen and ovule production varied depending on flower position, although the precise pattern differed between both studied populations; only investment in female floral function decreased markedly from base to top flowers in both populations. The frequency distribution of phenotypic gender and their relationship with plant size differed between populations. Phenotypic and functional gender were correlated in both populations. CONCLUSIONS: Sexual investment in P. odoratum has shown a marked variability within plants, among plants, and between populations, which confirms the importance of analysing sex expression in plants of this type. Differences in relative investment in male and female components (phenotypic gender) are reflected in the functional gender and it would be expected that the evolution of sexual specialization in Polygonatum odoratum would be promoted.     

Floral biology and pollination mechanisms of four Mexico-endemic Fuchsia species with contrasting reproductive systems

Aims The evolution of the outstanding variation of reproductive systems in angiosperms has been considered an important driver of lineage diversification. Closely related hermaphroditic and dioecious species with biotic pollination provide the opportunity to study and compare traits related to pollinator attraction and their consequences on reproductive components. A higher predictability of pollination syndromes is expected in dioecious species, which are dependent on pollinators, than in self-compatible hermaphroditic taxa. Dioecious species may suffer pollen limitation depending on the quality of floral rewards and the kind and abundance of pollinators, whereas no pollen limitation is expected in hermaphroditic species with autonomous self-pollination. Additionally, in the absence of pollen limitation, more or better seeds are expected in dioecious species, according to the sexual specialization hypothesis.Methods In natural populations of the hermaphroditic Fuchsia fulgens and Fuchsia arborescens and dioecious Fuchsia parviflora and Fuchsia obconica, all endemic to Mexico, we first described flower phenology, flower production and longevity and nectar volume and concentration. Then, we evaluated the correspondence between floral visitors and pollination syndromes. In hermaphrodite plants, we determined the level of herkogamy and the potential for autonomous self-pollination. Finally, we evaluated the effect of pollen limitation on fruit set and seed number and assessed seed germination for all species.Important findings In contrast to our prediction, dioecious species did not show a higher correspondence between pollination syndromes and floral visitors than did hermaphrodites; however, male flowers exhibited a higher correspondence than female flowers. No pollen limitation was detected in dioecious species, for which visitation rate did not differ between male and female flowers. The hermaphroditic F. fulgens showed pollen limitation for seed number, despite the presence of autonomous selfing. Fruit set from autonomous pollination was higher in F. arborescens, which showed a lower level of herkogamy compared with F. fulgens. Finally, dioecious species produced fewer but heavier seeds compared with hermaphrodite species. Although Fuchsia is classified as an outcrossing genus, both hermaphroditic species showed autonomous self-pollination. The heavier but lower number of seeds per fruit in dioecious species may be related to the more efficient resource allocation expected from sexual specialization. This could play an important role in the evolution of dioecy; however, a comparative phylogenetic approach is required to confirm this hypothesis.     

Polyploidization and sexual dimorphism of floral traits in a subdioecious population of Dasiphora glabra

银露梅亚雌雄异株种群的多倍化和花特征性二态 性二态是性别分离植物的常见性状,对植物的雌性和雄性功能可能产生不同的影响。本文以青藏高原特有植物银露梅(Dasiphora glabra)为研究对象,利用银露梅同时存在两性、雌性和雄性植株的种群,探讨银露梅与传粉相关的花特征性二态现象及其对传粉者访问、花粉流和结实的影响。另外,本文还利用流式细胞仪检查了两性植株、雄性植株和雌性植株之间基因组大小的差异。研究结果表明：银露梅雌性植株和雄性植株数量约占种群中植株总数量的40%,表明银露梅两性植株数量多于雄性和雌性的植株数量。两性植株的花数量显著多于雄性和雌性植株的花数量。雄花的花大小显著大于雌花和两性花的花大小。雄花的花粉数量与两性花的花粉数量没有差异,但是雌花的胚珠数量显著高于两性花的胚珠数量。双翅目的蝇类是银露梅最主要的访花者,尽管访花者偏好访问更大的花,但是在花间连续访问对大花没有表现出偏好。模拟花粉流实验表明,两性植株和雄性植株的有效花粉转移都很低,从而导致较低的结实率。雌性植株和雄性植株的DNA含量约为两性植株的4倍,并且单性植株和两性植株之间相互授粉不能结实。以上结果表明,与两性花相比,雌花和雄花在与传粉相关的花特征二态性上分别在雌性和雄性功能上表现出优势,但这种优势在很大程度上被低效的花粉转移所掩盖。银露梅的雌性植株和雄性植株经历了多倍化事件,导致与两性植株之间存在繁殖隔离,从而维持了3种性别植株的共存。