Fertility of exceptional bisexual individuals in four dioecious plant species

Exceptional, very rare, bisexual (hermaphroditic or monoecious) individuals have been detected in strictly dioecious populations of Rhamnus alaternus, R. palaestinus, Bryonia syriaca and Populus euphratica (a single individual in each species). While ordinary male plants in each species exhibited fully normal pollen, and female individuals set a considerable amount of fruit, the exceptional bisexual plants showed a reduction in male or female fertility, or both. This inability of the rare bisexual individuals to fully invest in the two genders suggests that trade-offs between male and female functions possibly play a major role in the breeding systems of these dioecious species, and probably implicates resource allocation (among other factors) as a selective force in the evolution of dioecy. Received: 5 April 1999 / Revision accepted: 30 June 1999     

Sex in advertising: dioecy alters the net benefits of attractiveness in Sagittaria latifolia (Alismataceae)

The flowers and inflorescences of animal-pollinated dioecious plants are generally small and inconspicuous in comparison with outcrossing cosexual species. The net benefits of an attractive floral display may be different for dioecious compared to cosexual populations because dioecious species experience a more severe reduction in pollen delivery when pollinators forage longer on fewer individuals. Here, we develop a model that predicts the decrease in pollen delivery in dioecious relative to cosexual populations from female-female, female-male and male-male visit sequences as the number of individuals visited varies. To evaluate the predictions of our model we conducted a common garden experiment with dioecious and monoecious (cosexual) arrays of the insect-pollinated herb Sagittaria latifolia. We find that, although increasing the advertisements of floral rewards (i.e. increasing floral display) attracts more pollinators to individuals, the probability that these pollinators subsequently deliver pollen to neighbouring plants depends on sexual system. Because the number of individual plants visited per foraging trip did not increase significantly with floral display, the relative pollination success of dioecious versus monoecious populations decreases with increased floral display. We propose that this could explain why dioecy is strongly correlated with reduced floral display among angiosperm species.     

Breeding systems in a secondary deciduous forest in Venezuela: The importance of life form, habitat, and pollination specificity

Breeding systems and mating systems of plants in a previously studied secondary deciduous forest were reanalysed in the context of new data. In this analysis, we increased the number of plant species (up to approximately 25% of the plant species in the community), included other life forms (23 annual and perennial species, plus habitat disturbance categories), and considered information about pollinator specificity. The frequencies of species with different sexual systems in a sample of 51 species were 82% hermaphrodite, 14% monoecious, and 4% dioecious. The frequencies of breeding systems in the sample of 49 hermaphroditic and monoecious species were 53% self-incompatible and 47% self-compatible. Self-compatible species included seven partially self-compatible, three self-compatible non-autogamous, and 13 self-compatible autogamous species. None of the species evaluated proved to be agamospermous. Fifty-five percent of the species tested were obligate outbreeders. The proportion of self-incompatible species was higher among trees and shrubs than among annual herbs. The proportion of self-compatible species for perennial herbs and lianas was not different. The association between annual herbs and autogamy was not strong: seven of 13 species were autogamous, five were partially self-compatible, and one was self-incompatible. The main characteristics or factors associated with breeding system were life cycle and successional stage. Short-lived species were mostly self-compatible, and xenogamy tended to be associated with forest and forest-border. In contrast, pollination specificity and life form were not consistently related to breeding system (self-compatibility or self-incompatibility) and mating system (xenogamy or autogamy).     

Complex sex determination in the stinging nettle Urtica dioica

The dioecious species Urtica dioica harbours wide variation in sex ratio of seeds. We conducted a series of crosses to analyse the genetic basis of sex determination in this species. Dutch populations of U. dioica contain low proportions of monoecious individuals beside male and female plants. Self-pollination of monoecious plants always yielded female, male and monoecious plants, generally in a ratio of one female to three male/monoecious individuals. This motivated us to write down a simple model in which gender is determined by one major sex-determination locus with four alleles. In the model males and monoecious plants have distinct genotypes but are both heterozygous at the sex-determination locus. We first made crosses among progeny obtained after self-pollination of monoecious plants. These crosses showed that the monoecious trait generally showed Mendelian inheritance and was passed on to the next generation via both pollen and seeds. Further crosses between monoecious plants and plants from dioecious system indicated that alleles from the dioecious system are often dominant. However, many exceptions to our genetic model are observed which suggest that dominance is incomplete and/or that more genes are involved in sex determination. We discuss to what extent sex determination genes explain the strongly biased seed sex ratios and argue that additional genes, for instance genes for female choice, must also be involved.     

海南尖峰岭热带山地雨林60 ha大样地木本植物性别系统数量特征

热带山地雨林中植物不同性别系统的数量和空间分布特征如何? 是否受自然环境条件影响? 这些问题的回答有助于更深入理解群落物种多样性是如何形成的。本文以海南尖峰岭热带山地雨林60 ha大样地中胸径大于1 cm的木本植物为研究对象, 描述了样地内木本植物性别系统的数量特征, 分析了雌雄异株植物空间分布与地形因子的相关关系。结果表明: 大样地内289种木本种子植物中有两性花植物176种, 单性花植物113种; 在单性花植物中, 51种为雌雄同株, 62种为雌雄异株。单性花植物植株数占所有植株总数的36.2%; 雌雄异株植物植株数占所有植株总数的21.5%, 占单性花植物植株数的59.5%。在20 m × 20 m样方的空间尺度, 雌雄异株植物呈现聚集分布的物种共有31种。以20 m × 20 m样方为分析单元, 雌雄异株植物种类的性别比例与海拔、凹凸度和坡度呈弱正相关; 个体相对多度仅和海拔呈弱正相关, 与坡度和凹凸度无相关; 而3个性别系统多样性指数与海拔、凹凸度和坡度均无显著关联。可见雌雄异株植物在海南热带山地雨林中占据了较大的比例, 但大部分种类种群较小, 其数量分布特征与地形因素紧密相关, 雌雄异株植物的存在对群落物种多样性的形成有较大贡献。     

Phylogenetic analysis of sexual systems in Inuleae (Asteraceae)

From an ancestor with bisexual flowers, plants with unisexual flowers, or even unisexual individuals have evolved in different lineages of angiosperms. The Asteraceae tribe Inuleae includes hermaphroditic, monoecious, dioecious, and gynomonoecious species. Gynomonoecy, the sexual system in which female and bisexual flowers occur on the same plant, is prevalent in the Asteraceae. We inferred one large gene phylogeny (ndhF) and two supertrees to investigate whether gynomonoecy was a stage in the evolution from hermaphroditism to monoecy. We identified transitions in sexual system evolution using the stochastic character mapping method. From gynomonoecious ancestors, both hermaphroditic and monoecious descendants have evolved. Gynomonoecy was not restricted to a stage in the evolution toward monoecy because the number of transitions and the rate of change from monoecy to gynomonoecy were much higher than the opposite. We also investigated one hypothesized association among female flowers and the development of a petaloid ray as an explanation of gynomonoecy maintenance in Asteraceae. We found that peripheral female flowers and petaloid rays were phylogenetically correlated. However, empirical evidence shows that a causal relationship between these traits is not clear.     

THE CONSEQUENCES OF DIOECY FOR SEED DISPERSAL: MODELING THE SEED-SHADOW HANDICAP

Abstract.— Recent evidence has suggested that clades of dioecious angiosperms have fewer extant species on average than those of cosexual (hermaphroditic and monoecious) relatives. Reasons for the decrease in speciation rates and/or increase in extinction rates are only beginning to be investigated. One possibility is that dioecious species suffer a competitive disadvantage with cosexuals because only half of the individuals in a dioecious population are seed bearing. When only females produce seed, offspring will be more spatially clumped and will experience more local resource competition than when every individual produces seed. We examine two spatially explicit models to determine the effect of a reduction in seed dispersers on the invasibility and persistence of dioecious populations. Even though dioecious females were allowed to produce twice as many seeds as cosexuals, our results show that a reduction in the number of seed dispersers causes a decrease in the ability of dioecious progeny to find uninhabited sites, thus reducing persistence times. These results suggest that the maintenance of dioecy in the presence of hermaphroditic competitors requires a substantial increase in relative fitness and/or a large dispersal advantage of dioecious seeds.     

REPRODUCTIVE BIOLOGY OF TROPICAL LOWLAND RAIN FOREST TREES. I. SEXUAL SYSTEMS AND INCOMPATIBILITY MECHANISMS

Sexual systems of tropical lowland rain forest trees were investigated to estimate the relative proportions of hermaphroditic, monoecious, and dioecious species. Controlled hand pollinations were performed on hermaphroditic species to determine the proportions of self-compatible and self-incompatible species. A total of 333 species was examined; 65.5% species were found to be hermaphroditic, 11.4% monoecious, and 23.1% dioecious. There were no differences between canopy and subcanopy habitats in the distribution of various sexual systems. Out of the 28 species subjected to controlled pollinations, 24 showed the presence of self-incompatibility. The site of the incompatibility barrier in distylous species was either in the stigma or in the style. In most of the monomorphic species, the incompatibility barrier was in the ovary. Although a majority of tree species in the rain forest appear to be obligate outcrossers (xenogamons), the potential for inbreeding due to small effective population size still remains to be explored.     

High abundance of dioecious plants in a tropical coastal vegetation

We examined the frequency of hermaphroditic, monoecious, and dioecious species of angiosperms in restinga (sandy coastal plain) vegetation in SE Brazil. The study site was a vegetation mosaic comprising nine plant formations, ranging from open types to forest. Dioecy (14% of 566 species) was similar to other tropical vegetations and strongly associated with woodiness and entomophily. However, more interestingly, there was an exceptionally high percentage (35%) of dioecious species among the dominant woody plants. This pattern has not been previously reported, and we discuss the extent to which it is ecologically driven. We argue that the high abundance of dioecious plants in this resource-poor environment can be attributed to ecological traits related to long-distance dispersal, ecological vigor, and possibly, vegetative reproduction.     

Plant sexual systems correlated with morphological traits: Reflecting reproductive strategies of alpine plants

Plant sexual systems can be affected by various environmental factors, and thus show a range of morphological differences. The associations between plant sexual systems and morphology are unique, for example, the subnival belt of the Hengduan Mountains has harsh climatic conditions, but hosts remarkable biodiversity. However, these associations have received surprisingly little attention. We analyzed the associations in this region, and compared the pattern of sexual systems with that of other floras, and we also reviewed the breeding system of 36 alpine species. Information on plant sexual systems and these traits were mainly based on published information, herbarium collections, and field observations. The results showed that there was a high proportion of hermaphroditic species and a low proportion of dioecious and monoecious species. Hermaphroditism was strongly associated with showy floral displays, specialist entomophily, and perennial forbs. Dioecy was strongly associated with inconspicuous, pale-colored flowers, anemophily, and shrubs, whereas monoecy was strongly associated with inconspicuous, pale-colored flowers, generalist entomophily, and perennial grasses. Although no association was found between sexual systems and fruit type, plants with dry fruits (98.1%) were predominant in our study region. With respect to the plant breeding systems in the alpine region of southwest China, we predicted that pollination service might be particularly low; most of the plants lacked enough outcrossing pollinators. Our data revealed that 97.1% of the hermaphroditic species were self-compatible, and 88.2% of them showed autonomous or facilitated selfing. The plant sexual systems identified might serve to optimize the probability of pollination and thus ensure reproductive success.     

The incidence and pattern of copollinator diversification in dioecious and monoecious figs

Differences in breeding system are associated with correlated ecological and morphological changes in plants. In Ficus, dioecy and monoecy are strongly associated with different suites of traits (tree height, population density, fruiting frequency, pollinator dispersal ecology). Although approximately 30% of fig species are pollinated by multiple species of fig‐pollinating wasps, it has been suggested that copollinators are rare in dioecious figs. Here, we test whether there is a connection between the fig breeding system and copollinator incidence and diversification by conducting a meta‐analysis of molecular data from pollinators of 119 fig species that includes new data from 15 Asian fig species. We find that the incidence of copollinators is not significantly different between monoecious and dioecious Ficus. Surprisingly, while all copollinators in dioecious figs are sister taxa, only 32.1% in monoecious figs are sister taxa. We present hypotheses to explain those patterns and discuss their consequences on the evolution of this mutualism.     

The evolution of reproductive systems and sex-determining mechanisms within rumex (polygonaceae) inferred from nuclear and chloroplastidial sequence data

The genus Rumex includes hermaphroditic, polygamous, gynodioecious, monoecious, and dioecious species, with the dioecious species being represented by different sex-determining mechanisms and sex-chromosome systems. Therefore, this genus represents an exceptional case study to test several hypotheses concerning the evolution of both mating systems and the genetic control of sex determination in plants. Here, we compare nuclear intergenic transcribed spacers and chloroplast intergenic sequences of 31 species of Rumex. Our phylogenetic analysis supports a systematic classification of the genus, which differs from that currently accepted. In contrast to the current view, this new phylogeny suggests a common origin for all Eurasian and American dioecious species of Rumex, with gynodioecy as an intermediate state on the way to dioecy. Our results support the contention that sex determination based on the balance between the number of X chromosomes and the number of autosomes (X/A balance) has evolved secondarily from male-determining Y mechanisms and that multiple sex-chromosome systems, XX/XY1Y2, were derived twice from an XX/XY system. The resulting phylogeny is consistent with a classification of Rumex species according to their basic chromosome number, implying that the evolution of Rumex species might have followed a process of chromosomal reduction from x = 10 toward x = 7 through intermediate stages (x = 9 and x = 8).     

Chloroplast haplotype variation among monoecious and dioecious populations of Sagittaria latifolia (Alismataceae) in eastern North America

Aquatic plants commonly have extensive geographical distributions, implying few restrictions to dispersal. Here we investigate the postglacial history of an aquatic plant with contrasting sexual systems (monoecy and dioecy), which are predicted to affect dispersal ability. We examined the distribution of cpDNA haplotypes using polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) among 76 populations (32 monoecious, 38 dioecious, two mixed and four undetermined populations) of Sagittaria latifolia sampled throughout eastern North America. We also use these data to investigate the polarity of the evolutionary transition between monoecy and dioecy. Using PCR-RFLP, we identified eight cpDNA haplotypes. All haplotypes were found in unglaciated areas of the species' range, clustered primarily in the southeastern United States, providing evidence that glacial refugia probably occurred in this area. Genetic diversity (hT) was more than six times greater among monoecious compared to dioecious populations. All seven of the haplotypes for which the sexual system could be determined were represented among monoecious populations. In contrast, only four haplotypes were detected in dioecious populations and 94% of individuals from dioecious populations possessed a single haplotype. Monoecious populations possessing this widespread haplotype were restricted to the southern portion of the range, indicating that dioecy probably originated in this region and then spread northwards. The distribution of cpDNA haplotypes in dioecious populations represents a subset of the variation found in monoecious populations, a pattern expected if dioecy has evolved from monoecy in S. latifolia.     

The Effect of Breeding System on Polymorphism in Mitochondrial Genes of Silene

Gynodioecy is a breeding system characterized by the co-occurrence of hermaphrodite and female individuals, generally as the result of nuclear–cytoplasmic interactions. The question remains whether the genetic factors controlling gynodioecy are maintained in species over long evolutionary timescales by balancing selection or are continually arising and being replaced in epidemic sweeps. If balancing selection maintains these factors, then neutral cytoplasmic diversity should be greater in gynodioecious than hermaphroditic species. In contrast, epidemic sweeps of factors controlling gynodioecy should decrease cytoplasmic diversity in gynodioecious relative to hermaphroditic species. We took a comparative approach in which we sequenced two mitochondrial genes, cytochrome b (cob) and cytochrome oxidase (cox1), for multiple populations of several hermaphroditic, gynodioecious, and dioecious species in the genus Silene. Breeding system was predictive of polymorphism. Gynodioecious species harbor many old haplotypes while hermaphroditic and dioecious species have little to no nucleotide diversity. The genealogical structure of neither gene departed from neutral expectations. Taken together, our results suggest that balancing selection acts on cytoplasmic male-sterility factors in several gynodioecious species in the genus.     

Study on the Flexistyly Pollination Mechanism in Alpinia Plants (Zingiberaceae)

Temporal dioecy, a flowering mechanism of synchronous alternation of pistillate and staminate phases in hermaphroditic (bisexual) flowers or monoecious individuals, decreases the probability of self-fertilization in self-compatible (SC) species. The authors report the prevalence of flexistyly in native species of Alpinia Roxb. in Xishuangbanna, Southwest China, resulted in dimorphism with two temporal dioecious floral phenotypes that facilitates out-crossing. Populations of ginger plants Alpinia have two specific phenotypes that differ in flowering behavior: (1)“cataflexistyle”individuals with the stigma held erect beyond dehiscent anther when anthesis begins in the morning and becoming decurved under the anther at noon; (2)“hyperflexistyle” individuals with the receptive stigma decurved under the indehiscent anther first and moving into a reflexed superior position above the anther as it begins to shed pollen at midday. The stigmatic movements in the two floral phenotypes, which occur in a ratio of 1∶1 in natural populations, are synchronous and pollination is effected only between floral forms. Field experiments indicate that species of Alpinia are self-compatible and insect dependent fertilization plants.     

Flower structure and sex expression of leaky dioecy in Eurya obtusifolia

The genus Eurya is described as strictly dioecious, but rare leaky plants have been found in some species, causing much confusion about the sex expression of the genus. Through field investigations from 2009 to 2011, morphologically hermaphroditic flowers in Eurya obtusifolia were discovered. In order to understand the sex expression of these plants, their stamens, pistils and ovules were carefully observed. Staining methods were used to assess the functional gender. The flowers of the leaky plants can be classified into six types: pistillate, staminate, cryptic pistillate, cryptic staminate, hermaphrodite and infertile. Leaky plants usually exhibit a combination of different kinds of flowers, making them either gynoecious, androecious, gynomonoecious or monoecious. Some individuals have infertile flowers. Bagging experiments verified the bisexual function of E. obtusifolia plants, some of which possess the ability to self‐pollinate. The flower morphology of leaky plants varied more than that of dioecious ones, and the number of ovules were significantly negatively correlated with the number of stamens. These plants show lower fitness than normal dioecious plants. This may owe to allocation tradeoffs or sexual genome conflicts. As leaky dioecy is rarely reported in this genus, E. obtusifolia is an important species to study in order to better understand the ecological adaptations and evolutionary pathways that lead to dioecy in Eurya. Our findings provide some evidence that dioecy of Eurya evolved from hermaphroditism, but further studies are still needed.     

Plant sexual systems, dichogamy, and herkogamy in the Venezuelan Central Plain

Sexual system, temporal variation in sex expression, and herkogamy were evaluated in 210 plant species in the Venezuelan Central Plain (VCP). This analysis was conducted considering the life forms, habitats, flowering time, pollination systems, and dispersal syndromes of the plant species. Hermaphrodite species dominated the community (75.2%; N=158), followed by monoecious taxa (17.1%; N=36), and then dioecious (7.6; N=16). Most species were adichogamous (=homogamous) (75.2%; N=155), followed by protandrous (16.5%; N=34), and protogynous (8.3%; N=17). The frequency of herkogamous species was higher (N=124; 60.2%) than the non-herkogamous (N=82; 39.8%). The three reproductive traits interacted significantly in a way that complements their effectiveness in promoting cross-pollination and avoidance of pollen–stigma interference: hermaphrodite-adichogamous species occurred in similar frequency to herkogamous and non-herkogamous species; monoecious-adichogamous species were mostly herkogamous, and all hermaphrodite, functionally dioecious-adichogamous, species were herkogamous. Sexual system, herkogamy, and dichogamy are associated with habitats in the savanna-forest mosaic of the VCP. The proportion of dioecious species decreased from trees to annual herbs and from forest to disturbed areas. Dichogamous species were most frequent for herbaceous plants, and non-herkogamous species dominated in annual herbs. The frequency of herkogamous species decreased from forest to disturbed areas. Sexual system was significantly associated with pollination system. Most dioecious and monoecious species had generalist pollination. A three-factor log linear analysis indicated that for any combination significantly. Sexual systems and herkogamy were associated with the respective seed dispersal syndrome. Most dioecious and herkogamous species were dispersed by frugivores, while monoecious plants tended to be dispersed by granivores and wind. Flowering time of dioecious species peaked during the dry–rainy transition period, whereas that of monoecious species was greatest during the rainy season. Therefore, specific biotic and abiotic conditions may enforce the occurrence of unisexuality in the community. In a similar way, dichogamous species tend to flower during the rainy season, associated with herbaceous life form and wind pollination. These results are discussed in the context of evolutionary and ecological trends.     

Dioecy,more than monoecy,affects plant spatial genetic structure: the case study of Ficus

In this analysis, we attempt to understand how monoecy and dioecy drive spatial genetic structure (SGS) in plant populations. For this purpose, plants of the genus Ficus were used as a comparative model due to their particular characteristics, including high species diversity, variation in life histories, and sexual systems. One of the main issues we assessed is whether dioecious fig tree populations are more spatially genetically structured than monoecious populations. Using the Sp statistic, which allows for quantitative comparisons among different studies, we compared the extent of SGS between monoecious and dioecious Ficus species. To broaden our conclusions we used published data on an additional 27 monoecious and dioecious plant species. Furthermore, genetic diversity analyses were performed for two monoecious Ficus species using 12 microsatellite markers in order to strengthen our conclusions about SGS. Our results show that dioecy, more than monoecy, significantly contributes to SGS in plant populations. On average, the estimate of Sp was six times higher for dioecious Ficus species than monoecious Ficus species and it was two times higher in dioecious than monoecious plant species. Considering these results, we emphasize that the long‐distance pollen dispersal mechanism in monoecious Ficus species seems to be the dominant factor in determining weak spatial genetic structure, high levels of genetic diversity, and lack of inbreeding. Although Ficus constitute a model species to study SGS, a more general comparison encompassing a wider range of plants is required in order to better understand how sexual systems affect genetic structure.     

The oogonial aperture of Oedogonium decipiens var. decipiens (Oedogoniales, Chlorophyta) and its systematic significance

Pollen morphology of ten Brazilian species within the South American clade (ca. 20 species) of Symplocos section Barberina (Symplocaceae) was analyzed with scanning electron microscopy to assess their reported androdioecious breeding system. All species exhibited pollen dimorphism. Pollen from male individuals is well developed and 3-colporate, whereas that from morphologically hermaphroditic individuals is malformed, often completely fragmented, lacks cytoplasm, and has no germination pores. Our results suggest that the morphologically hermaphroditic species of S. section Barberina with malformed pollen are cryptically dioecious.     

Sexual selection and simultaneous hermaphroditism among the Unionidae (Bivalvia: Mollusca)

Simultaneous hermaphroditism is an infrequent mode of reproduction among bivalves of the family Unionidae: only five of the 220 North American species are simultaneous hermaphrodites. However, hermaphroditic individuals of otherwise predominantly dioecious species have been encountered in 30 of I01 species examined. These hermaphroditic individuals as well as simultaneous hermaphrodites can exhibit considerable variability in the ratio of spermatogenic: oogenic tissue within the gonad, and the purposes of this paper are to determine the underlying causes of both this variability and the occurrence of occasional hermaphroditic individuals among dioecious species. Results indicate that the ratio of male: female gonodal tissue of a simultaneous hermaphrodite is bimodally distributed, and several hypotheses to account for this observation are presented. It is proposed that populations occurring in different habitats and under conditions of different individual density are subject to fundamentally different sexual selection pressures acting on ratios of allocation to male and female gametes. Occasional hermaphroditism among otherwise predominantly dioecious species was in this study associated with infection of the gonads by digenean trematodes. A model of sexual determination among unionids presented in this paper proposes that sex is determined by genetically controlled hormone levels: occasional hermaphrodites result from alterations in these hormone levels caused by developmental errors and trematodal infections which mimic the results of such errors. Predictions of this model are consistent with observed levels of variability in male: females gonadal tissue among occasional hermaphrodites.