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.     

Flower size dimorphism in diclinous plants native to La Réunion Island

Although many diclinous plants have a flower size dimorphism, the causes and ecological correlates of dimorphism in flower size remain poorly understood. In this paper we quantify the frequency and distribution of flower size dimorphism in the native flora of La Réunion Island. The frequency of flower size dimorphism is lower than in a previous global study suggesting that the dimorphism may limit colonisation success. Flower size dimorphism is significantly more frequent in endemic taxa compared to indigenous taxa, a trend that is particularly evident at the species level, due to the large number of species with male flowers bigger than female flowers and is more common in species-rich lineages. These results suggest that flower size dimorphism may be associated with species divergence. The direction of dimorphism varies between dioecious and monoecious species, suggesting that the mechanisms acting on flower size variation differ in species with these different sexual systems.We thank Jacques Figier and Dominique Strasberg for their encouragement and advice and anonymous reviewers for constructive comments. The Université de La Réunion and the Conseil Régional de La Réunion provided financial support.     

Impacts of floral gender and whole-plant gender on floral evolution in Ecballium elaterium (Cucurbitaceae)

Investigation of gender specialization in plants has led to several theories on the evolution of sexual dimorphism: reproductive compensation, based on enhanced reproductive efficiency with gender specialization (flowers should be larger on dioecious plants); Bateman's Principle, based on sex-specific selection (display for pollinator attraction in males and seed set in females); and intersexual floral mimicry, based on mimicry of a reward-providing gender by a non-reward providing gender (reduced dimorphism in dioecious plants due to increased spatial separation of male and female flowers). These theories were evaluated in Ecballium elaterium, which contains two subspecies, elaterium (monoecious) and dioicum (dioecious). Our results show that flowers of the dioecious subspecies are larger and allocate more to reproductive organs than do flowers of the monoecious subspecies. Both subspecies are sexually dimorphic (male flowers larger than female flowers). Variance in flower size among populations is greater in the dioecious subspecies. Finally, there is sufficient genetic variation to enable ongoing response to selection; genetic correlation constraints on independent response of female and male flowers may be stronger in the monoecious subspecies. Our findings provide support for aspects of all three theories, suggesting that the evolution of floral dimorphism is based on a complex interplay of factors.     

Architectural effects mimic floral sexual dimorphism in Solanum (Solanaceae)

Factors underlying apparent floral sexual dimorphism were examined in six species of andromonoecious Solanum section Lasiocarpa (Solanaceae). Both multivariate and univariate analyses show that hermaphroditic flowers are significantly larger than staminate flowers for all features measured. Thus, flowers could be characterized as sexually size dimorphic. However, when size variation due to flower position (architecture) is controlled experimentally, differences between the floral genders for the nongynoecial characters disappear; there is no difference in corolla or androecium size. Staminate flowers appear to be generally smaller than hermaphroditic flowers, not because of any difference related to primary sexual function, but because they tend to occur in the distal regions of each inflorescence. In contrast, significant differences between hermaphroditic and staminate flowers for primary female traits (ovary, style, and stigma) remain after controlling for position: the two floral types are truly dimorphic for these characters. We show that consideration of architectural effects can direct and refine hypotheses concerning the evolution of andromonoecy. More generally, if architectural effects on flower size are common among taxa with unisexual flowers, then these effects may contribute to the common perception of size dimorphism in taxa with unisexual flowers.     

Anther-smut infection of Silene alba caused by Ustilago violacea: factors determining fungal reproduction

Summary The anther-smut fungus Ustilago violacea sporulates in flowers of the dioecious host plant Silene alba. Growth chamber comparisons of healthy and diseased plants, with the genetic background of host and pathogen controlled, revealed that fungal infection increases the number of flowers produced per plant and decreases the size of individual flowers. There were few consistent effects of plant genotype or fungal isolate on diseased flower traits, but differences between the plant sexes were apparent. Stimulation of flower production is proportionally greater in females than males: thus, although healthy male plants produce many more flowers than healthy females, sexual differences in diseased flower number are reduced. Sexual differences in diseased flower size also exist, with male flowers smaller than females. A field inoculation study confirmed dimorphism in diseased flower size and demonstrated that spore production per flower was greater for males than females for all flower size classes.     

Reproductive ecology of dioecious Siparuna (Monimiaceae) in Ecuador–a case of gall midge pollination

The reproductive ecology of the dioecious genus Siparuna , belonging to the primitive family Monimiaceae, was investigated in Ecuador. Thirteen species were studied, and species growing at high altitudes (above 500 m) were compared with species growing at lower altitudes. The genus has specialized flowers pollinated by Cecidomyiidae (Asynapta sp. and other genera) that lay eggs chiefly in male flowers since these are more easily accessible than female flowers due to their morphology. Several traits ensure that pollen transfer is accomplished: 1. long flowering of individuals and single flowers; 2. specific floral morphology (unisexuality, landing platform, restricted pore) allowing the flowers to be visited by Cecidomyiidae seeking egg-laying sites, and 3. a low number of ovules that have to be pollinated in each flower. The low number of ovules per flower results in a high pollen-ovule (P/O) ratio even though pollen production in male flowers is only moderate.
High altitude species had larger flowers, higher pollen-ovule ratios, fewer ovules per female flower, and longer periods of anthesis. Gender differences were seen in the longer functionality of female flowers; the larger numbers of male flowers produced; and the average diameter at breast height (DBH) biased for one of the two sexes depending on the species investigated, with no clear trend in the size distributions of individuals of both sexes. Sex ratios departed significantly from unity both to male and female bias but usually were in favour of males. There were no general differences in the ratio of functional male to female flowers at the time of observation nor in the sizes of male and female flowers. The evolution of unisexual flowers in Siparuna can be explained as a result of the differential predation by larvae: unimportant in male flowers, destructive if occurring in female flowers.     

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.     

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     

Sex Determination by Sex Chromosomes in Dioecious Plants

Abstract: Sex chromosomes have been reported in several dioecious plants. The most general system of sex determination with sex chromosomes is the XY system, in which males are the heterogametic sex and females are homogametic. Genetic systems in sex determination are divided into two classes including an X chromosome counting system and an active Y chromosome system. Dioecious plants have unisexual flowers, which have stamens or pistils. The development of unisexual flowers is caused by the suppression of opposite sex primordia. The expression of floral organ identity genes is different between male and female flower primordia. However, these floral organ identity genes show no evidence of sex chromosome linkage. The Y chromosome of Rumex acetosa contains Y chromosome-specific repetitive sequences, whereas the Y chromosome of Silene latifolia has not accumulated chromosome-specific repetitive sequences. The different degree of Y chromosome degeneration may reflect on evolutionary time since the origination of dioecy. The Y chromosome of S. latifolia functions in suppression of female development and initiation and completion of anther development. Analyses of mutants suggested that female suppressor and stamen promoter genes are localized on the Y chromosome. Recently, some sex chromosome-linked genes were isolated from flower buds of S. latifolia.     

The arrest of development of abortive reproductive organs in the unisexual flower of<Emphasis Type="Italic"> Vitis vinifera</Emphasis> ssp.<Emphasis Type="Italic"> silvestris</Emphasis>

During the first stages of development, flowers of most dioecious species are hermaphroditic, with their transition to unisexual flowers being the result of the developmental arrest of one set of reproductive organs. In this work, we describe the development of male and female flowers of the dioecious wild grape species Vitis vinifera ssp. silvestris through scanning electron microscopy analysis and cytological observations, focusing our attention on the transition from bisexual to unisexual development. We divide floral development of the wild grape into eight stages. Differences between male and female flowers appear first at stage 6, when the style and stigma start to differentiate in female but not in male flowers. Cytological analysis of the slowly growing abortive pistil of male flowers shows that megagametophyte formation is, surprisingly, not inhibited. Instead of pistil abortion in the male flower, sexual determination is accomplished through programmed death of external nucellus cells and some layers of integumentary cells. Sterility of male structures in female flowers follows a different pattern, with microspore abnormalities evident from the time of their release from the tetrad. Sterile microspores and pollen grains in female flowers display an abnormal round shape, lacking colpi and possessing uniformly thickened cell walls that impede germination.     

Variation in inflorescence size in a dioecious fig tree and its consequences for the plant and its pollinator fig wasp

The host-specific relationship between fig trees (Ficus) and their pollinator wasps (Agaonidae) is a classic case of obligate mutualism. Pollinators reproduce within highly specialised inflorescences (figs) of fig trees that depend on the pollinator offspring for the dispersal of their pollen. About half of all fig trees are functionally dioecious, with separate male and female plants responsible for separate sexual functions. Pollen and the fig wasps that disperse it are produced within male figs, whereas female figs produce only seeds. Figs vary greatly in size between different species, with female flower numbers varying from tens to many thousands. Within species, the number of female flowers present in each fig is potentially a major determinant of the numbers of pollinator offspring and seeds produced. We recorded variation in female flower numbers within male and female figs of the dioecious Ficus montana growing under controlled conditions, and assessed the sources and consequences of inflorescence size variation for the reproductive success of the plants and their pollinator (Kradibia tentacularis). Female flower numbers varied greatly within and between plants, as did the reproductive success of the plants, and their pollinators. The numbers of pollinator offspring in male figs and seeds in female figs were positively correlated with female flower numbers, but the numbers of male flowers and a parasitoid of the pollinator were not. The significant variation in flower number among figs produced by different individuals growing under uniform conditions indicates that there is a genetic influence on inflorescence size and that this character may be subject to selection.     

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.     

Sex ratio variation in dioecious plant species: A comparative ecological study of six species of Lindera (Lauraceae)

Sex ratio variation was investigated in natural populations of six dioecious shrub species of Lindera in Japan. Interspecific differences in sex ratio were examined in relation to patterns of population structure, floral dimorphism, fruit production and intersexual differences in herbivory. Sex ratios tended towards equality or bias in favour of males, except for populations of L. glauca , in which no male plants were found. Sex switching in individual plants was not observed. Although male flowers were generally larger in size than flowers of conspecific females, costs of flowering did not appear to influence sex ratio. However, a relation was found between high allocation to fruit production and increasing male fraction of populations. In addition, girths of flowering plants tended to be larger in females, which may indicate delay in age of the first reproduction compared to males. No intersexual difference was found in degree of leaf damage due to herbivory. Results of this study are discussed in the light of other studies on sex ratio variation in dioecious plant species.     

Sexual dimorphism and sex ratios of two Australian dioecious species of alpine pineapple grass, Astelia alpina var. novaehollandiae and Astelia psychrocharis (Asteliaceae)

Sexual dimorphism and male biased sex ratios have been predicted for dioecious plants experiencing the limited conditions for growth and reproduction found in many alpine environments. To test these predictions, the reproductive ecology of two congeneric, co-occurring, dioecious, clonal, species was examined in the subalpine and alpine zones of Kosciuszko National Park, southeastern Australia. Specifically, plant size (vegetative cover of plants in quadrats), floral display (number of flowers per inflorescence, number of inflorescences per quadrat) and sex ratios (proportion of females in quadrats with flowers) were examined in ten populations of Astelia psychrocharis (Asteliaceae) and nine populations of Astelia alpina var. novae-hollandiae (Asteliaceae). Sexual dimorphism did occur, with males having more flowers per inflorescence (106% more flowers for A.alpina males and 12% more for A.psychrocharis males compared to females) and more inflorescences per quadrat than females (78% more inflorescences for A.alpina males and 46% more inflorescences for A.psychrocharis males compared to females). Plant size did not differ between male and female quadrats of either species, nor were there male biased sex ratios. However, plant size was related to flowering status in A.psychrocharis with the 65 quadrats that did not flower having lower vegetative cover than the 175 flowering quadrats indicating that there may be a minimum size/ cover required prior to flowering in this species. For A.alpina, all but two of the 185 quadrats randomly sampled flowered. There was no effect of altitude on plant size and very little effect of altitude on floral display for either species, apart from a slight increase in the number of inflorescences per quadrat with increasing altitude for A.psychrocharis, and slight decrease in number of flowers per inflorescence with increasing altitude for A.alpina females.     

Functional analysis of B and C class floral organ genes in spinach demonstrates their role in sexual dimorphism

Background  

Evolution of unisexual flowers entails one of the most extreme changes in plant development. Cultivated spinach, Spinacia oleracea L., is uniquely suited for the study of unisexual flower development as it is dioecious and it achieves unisexually by the absence of organ development, rather than by organ abortion or suppression. Male staminate flowers lack fourth whorl primordia and female pistillate flowers lack third whorl primordia. Based on theoretical considerations, early inflorescence or floral organ identity genes would likely be directly involved in sex-determination in those species in which organ initiation rather than organ maturation is regulated. In this study, we tested the hypothesis that sexual dimorphism occurs through the regulation of B class floral organ gene expression by experimentally knocking down gene expression by viral induced gene silencing.     

Multiple developmental processes underlie sex differentiation in angiosperms

The production of unisexual flowers has evolved numerous times in dioecious and monoecious plant taxa. Based on repeated evolutionary origins, a great variety of developmental and genetic mechanisms underlying unisexual flower development is predicted. Here, we comprehensively review the modes of development of unisexual flowers, test potential correlations with sexual system, and end with a synthesis of the genetics and hormonal regulation of plant sex determination. We find that the stage of organ abortion in male and female flowers is temporally correlated within species and also confirm that the arrest of development does not tend to occur preferentially at a particular stage, or via a common process.     

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.     

Sex-specific cell division during development of unisexual flowers in the dioecious plant Silene latifolia

We analyzed cell division patterns during the differentiation of unisexual flowers of the dioecious plant Silene latifolia using in situ hybridization with histone H4 and cyclin A1 genes. The gene expression patterns indicated that the activation of cell divisions in whorls 3 and 4 was reversed in young male and female flower buds. During maturation of flower buds, a remarkable reduction in cell division activity occurred in the male gynoecium primordium and female stamen primordia. Our analyses showed that differential activation and reduction of cell division strongly correlated with sex-specific promotion and cessation in the sex differentiation of unisexual flowers.     

Modification of flower sex and acid phosphatase activity by phthalimides in female plants of Morus nigra L.

Phthalimide treatments at 125, 250 and 500 mg 1^–1 to female plants of dioecious Morus nigra L. induced intersex and male flowers. Qualitative and quantitative analyses of acid phosphatase in male and female flower buds showed that the male flower had significantly higher levels of the enzyme activity than the female flower buds. The level of acid phosphatase activity significantly increased in intersex and male flowers induced on female plants after phthalimide treatments.     

Sexual dimorphism in pollen grain size in cryptically dioecious Thalictrum macrostylum

While several plant species are initially described as androdioecious, upon more thorough investigation, many of these are found to be cryptically dioecious with functionally male flowers and perfect flowers that produce inaperturate pollen or are otherwise functionally female on separate plants. The change in function of pollen produced by perfect flowers opens up the possibility for the evolution of sexual dimorphism in pollen grain size. We found that Thalictrum macrostylum (Ranunculaceae) is cryptically dioecious, and produces apparently inaperturate pollen in perfect flowers. In four field sites throughout North Carolina, inaperturate grains are larger than grains from staminate flowers and also show a greater variance in size. We also found substantial variation in pollen grain size among plants. The sites with lower soil nutrient content also had smaller pollen grains of both types, although local adaptation or genetic drift may also be causing among-site variation.