Dioecy in the Caatinga,a Brazilian tropical dry forest: typical reproductive traits of a low frequent sexual system

Dioecy is a rare sexual system among angiosperms whose occurrence and frequency depend on the kind and geographical location of the ecosystem. We evaluate the frequency of dioecy in the Caatinga, a special semi-arid vegetation type in Brazil. We compare the floral traits and other ecological characteristics usually related to dioecy between the Caatinga and other tropical ecosystems. Dioecious species of the Caatinga were compiled based on 24 published floristic lists including most of the Caatinga domain. These lists were compared with publications comprising data on sexual systems in different kinds of vegetation in the world. Sexual system confirmation and the database of the reproductive traits of the dioecious species were made by consulting herbaria, literature, and field observations. We registered 22 dioecious species occurring in the Caatinga. The overall dioecy frequency was 2.36 %, considering all Caatinga species, and 6.91 % within woody species. Most dioecious species exhibited traits related to this sexual system (e.g., woody habit, greenish inconspicuous flowers, generalistic pollination syndrome, and zoochory). The distribution of dioecy across the Caatinga plant community exhibited a very low level of phylogenetic signal (D = ?0.145), indicating a phylogenetic structure under Brownian evolution (p = 0.671). The frequency of dioecy in the Caatinga (2.36 %) proved lower than reported for angiosperms in general (ca. 6 %) and for other tropical ecosystems. This low frequency can be related to particular ecological characteristics of the Caatinga, such as low percentage of trees >3–4 m tall (13–18.7 %), low rainfall (50 % of the Caatinga vegetation with annual rainfall lower than 750 mm), and strong seasonality (6–9 months of dry season). Dioecious species of the Caatinga exhibited typical reproductive traits for this sexual system, similar to what has been reported for dioecious species of other tropical ecosystems in the world.     

Patterns of plant sexual systems in subtropical evergreen broad-leaved forests in Ailao Mountains,SW China

Aims Sexual systems influence many components of the ecology and evolution of plant populations and have rarely been documented in subtropical evergreen broad-leaved forests (SEBLF). Here we report frequency distribution and ecological correlates of plant sexual systems in SEBLF at Ailao Mountains, and compare our results with that of tropical and cool temperate forests.Methods We examine the sexual systems of 703 species of woody angiosperms belonging to 103 families and 296 genera based on a comprehensive survey of SEBLF at Ailao Mountains Natural Reserve. Information of plant sexual systems and ecological traits were mainly based on published literatures and specimens as well as our field observations. The associations between plant sexual system and ecological traits were assessed with chi-square tests.Important findings Among these species, 60.2% were hermaphroditic, 15.8% were monoecious and 24.0% were dioecious. The percentage of dioecious sexual system among tree species (22.2%) in SEBLF was comparable to those of tropical tree floras, but much higher than those of temperate forests at North America. The percentage of monoecious sexual system among tree species (30.1%) in SEBLF was higher than that of tropical tree floras, but much lower than those of temperate forests at North America. Monoecy was significantly associated with the tree growth form and was relatively common in temperate genera. Dioecy was significantly associated with fleshy fruits and monoecy was significantly associated with dry fruit type in SEBLF. The high percentage of diclinous sexual systems (monoecy and dioecy) in SEBLF may be associated with the origin of the flora and the prevalence of relatively small inconspicuous flowers of the forests in the Oriental Region.     

The role of diversification in causing the correlates of dioecy

Dioecy is reported to be correlated with a number of ecological traits, including tropical distribution, woody growth form, plain flowers, and fleshy fruits. Previous analyses have concentrated on determining whether dioecy is more likely to evolve in lineages possessing these traits, rather than considering the speciation and extinction rates of dioecious lineages with certain combinations of traits. To address the association between species richness in dioecious lineages as a function of the ecological traits, we compared the evolutionary success (i.e., relative species richness) of dioecious focal lineages with that of their nondioecious sister groups. This test was repeated for the evolutionary success of randomly chosen nondioecious lineages (control lineages) compared with their nondioecious sister groups. If the possession of certain ecological traits enhances the evolutionary success of dioecious lineages, we predict an association between the presence of these traits and relative species richness in the former, but not latter, set of sister-group comparisons. Dioecious focal lineages with a higher number of these traits experienced higher evolutionary success in sister-group comparisons, whereas no trend was found for the control focal lineages. The increase in evolutionary success was especially true for dioecious focal lineages that had a tropical distribution or fleshy fruit. We discuss how these results provide strong support for differential evolutionary success theories for the correlations between dioecy and the ecological traits considered.     

Present day risk of extinction may exacerbate the lower species richness of dioecious clades

Dioecious clades have been observed to have lower species richness than their non‐dioecious sister groups indicating that dioecious species experience higher extinction rates and (or) lower speciation rates. To determine whether current threats to biodiversity may exacerbate this pattern, we examined the threat to exclusively dioecious families of angiosperms among the 13,013 species of threatened plants included in the IUCN Red List of Threatened Species. When examined phylogenetically, dioecious families had proportionally more species listed than their sister groups. We then examined whether ecological traits correlated with dioecy, namely tropical distribution, woody growth form, and fleshy fruits, are associated with having higher proportions of threatened species. Ignoring breeding system, woody growth form was the only trait that was associated with a greater than expected proportion of threatened species per family. Red‐Listed dioecious families were more likely to have a woody growth form than non‐dioecious families. Woody growth habit is likely contributing to the higher incidence of dioecious species being at risk of extinction but is not solely responsible for the pattern because higher risk within dioecious groups was also apparent in a comparison of exclusively woody sister‐group pairs. Our results indicate that dioecious plants may warrant special attention in conservation practices.     

The frequency, distribution and reproductive biology of dioecious species in the native flora of Britain and Ireland

The proportion of dioecious species in the flora of the British Isles has been underestimated in the past, partly because the total number of native species was overestimated and partly because some dioecious species were omitted for various reasons. We estimate that, in a total native angiosperm flora of 1377 species and species-equivalents, 4.3% (59 species) are dioecious, a substantially higher percentage than the previous estimates of 2, 3.1 and 3%. If gymnosperms are included, 4.4% (61 of 1380 species of seed plant) are dioecious. A review of published work shows that few of these dioecious species have been well-studied, and that for some little or no information is available about their sex ratios and reproductive biology.     

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.     

Dioecious plants are more precocious than cosexual plants: A comparative study of relative sizes at the onset of sexual reproduction in woody species

The reproductive capacities of dioecious plant species may be limited by severe pollen limitation and narrow seed shadows for the two reasons. First, they are unable to self‐pollinate, and seed production occurs only with pollinator movement from males to females. Second, only 50% of the individuals in populations contribute to seed production. Despite these handicaps, dioecious plants maintain their populations in plant communities with cooccurring cosexual plants, and no substantial difference in population growth rates has been found between dioecious and cosexual plants. Hence, dioecious plants are thought to mitigate these disadvantages by adopting ecological traits, such as insect pollination, animal‐dispersed fleshy fruits, and precocious flowering. We studied the relationship between flowering and plant size in 30 woody species with different sex expressions, leaf habits, fruit types, and maximum plant sizes. The study site was located in an evergreen broad‐leaved forest on the island of Honshu, Japan. A phylogenetic linear regression model showed that dioecious species tended to mature at smaller sizes than did cosexual taxa. At the population level, given equal plant densities and reproductive efforts, the precocity of dioecious plants could serve as one of the factors that mitigate the limitations of pollen and seed‐shadow handicaps by increasing the density of reproductive individuals in the population. At the individual level, smaller size of onset of flowering may play a role in enhancing reproductive success over a lifetime by increasing reproductive opportunities. We discussed the possible effect of the relationship between precocity and some ecological traits of dioecious plants, such as small flowers pollinated by unspecialized insects, fleshy fruit dispersed by animals, and their preferential occurrence in the tropics and in island habitats. The universality of precocity among dioecious plants should be investigated in diverse plant communities. Such studies will increase our understanding of the evolution of plant breeding systems.     

Quantified ecology and co-occurrence of Mediterranean woody species in a landscape context

Understanding co-occurrence and ecological affinities of plant species is essential in vegetation and landscape ecology. In a case study, we analysed distribution records with high data density of all commonly occurring tree and shrub species of Crete (Greece) with offshore islands. We present the ecological range of widespread and more range-restricted species in the Mediterranean area, visualising their affinities for macroclimate, topoclimate and geology by means of an ecological heatmap. Complete linkage classification of combined ecological spectra revealed groups of generalist species with broad ecological amplitude, groups related to zonal vegetation and chiefly dependent on elevation, and species of azonal vegetation grouped mainly by topography and substrates. Species and ecological groups with high affinity may be indicative of (a combination of) site features. Our re-evaluation of plant distribution records links plant geographical and ecological information, and thereby complements expert habitat and species assessments. Our case study provides deeper understanding of ecological patterns, and at the same time allows for comparison and extrapolation to other biomes.     

Sexual Systems and Ecological Correlates in an Azonal Tropical Forests, SW China

Unlike the seriate lowland rain forests in SE Asia, the tropical vegetation of Xishuangbanna (SW China) has developed in habitats with comparatively lower temperatures and precipitation. Consequently, although most of the families and genera of the flora are components of tropical ecosystems, many have reached their distribution limits in latitude. Selection pressures on sexual systems in these environments may be different from that experienced in lowland tropical regions. Here, we examine the sexual systems of 685 species of flowering plants belonging to 109 families and 356 genera based on 42 plots with a total area of 15.4 ha and compare our results with surveys of sexual systems from other tropical ecosystems. Among these species, 60.6 percent were hermaphroditic, 14.3 percent were monoecious, and 25.1 percent were dioecious. The percentage of dioecious sexual system among tree species (26.1%) was similar or higher than that of other tropical tree floras. Monoecy was significantly associated with the tree growth form and was relatively common in seasonal forest vegetation. Sexual systems involving unisexual flowers (dicliny) are particularly well represented in the tropical forests of Xishuangbanna accounting for 39.4 percent of all species surveyed. This pattern may be associated with the prevalence of relatively small inconspicuous flowers in the tropical forests of SE Asia and their correlation with diclinous sexual systems generally.     

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.     

Low fruit set in the abundant dioecious tree Clusia hilariana (Clusiaceae) in a Brazilian restinga

Clusia hilariana (Clusiaceae), a dioecious tree, is an important nurse plant in the open, patchy restinga vegetation of coastal sandy plains in northern Rio de Janeiro (SE-Brazil). Although highly abundant locally, we found low production of fruit and viable seeds in open-pollinated as compared to hand-pollinated flowers. Reward from flowers of both sexes was resin, which was produced in higher quantities in male flowers. Flower visitors, including honeybees, were infrequent. We argue that low sexual reproductive success was due to inefficient pollen transport, and that vegetative propagation may contribute significantly to the high abundance of plants of this species.     

Life-history differentiation and the maintenance of monoecy and dioecy in Sagittaria latifolia (Alismataceae)

The existence of monoecious and dioecious populations within plant species is rare. This limits opportunities to investigate the ecological mechanisms responsible for the evolution and maintenance of these contrasting sexual systems. In Sagittaria latifolia, an aquatic flowering plant, monoecious and dioecious populations exist in close geographic proximity but occupy distinct wetland habitats differing in the relative importance of disturbance and competition, respectively. Life-history theory predicts contrasting evolutionary responses to these environmental conditions. We propose that the maintenance of monoecy and dioecy in S. latifolia is governed by ecological selection of divergent life-history strategies in contrasting habitats. Here we evaluate this hypothesis by comparing components of growth and reproduction between monoecious and dioecious populations under four conditions: natural populations, a uniform glasshouse environment, a common garden in which monoecious and dioecious populations and their F1 progeny were compared, and a transplant experiment using shaded and unshaded plots in a freshwater marsh. Plants from dioecious populations were larger in size and produced heavier corms in comparison with monoecious populations. Monoecious populations flowered earlier and produced more flowers, clonal ramets, and corms than dioecious populations. The life-history differences between the sexual systems were shown to have a quantitative genetic basis, with F1 progeny generally exhibiting intermediate trait values. Survival was highest for each sexual system in field plots that most closely resembled the habitats in which monoecious (unshaded) and dioecious (shaded) populations grow. These results demonstrate that monoecious and dioecious populations exhibit contrasting patterns of investment in traits involved with growth and reproduction. Selection for divergent life histories between monoecious and dioecious populations of S. latifolia appears to be the principal mechanism maintaining the integrity of the two sexual systems in areas of geographic overlap.     

The role of breeding system in community dynamics: Growth and mortality in forests of different successional stages

Plant sexual systems appear to play an important role in community assembly: Dioecious species are found to tend to have a higher propensity to colonize communities in early successional stages. Here, we test two demographic hypotheses to explain this pattern in temperate forests. First, we test demographic differences between hermaphrodite and dioecious species in stressful younger successional stages: Previous theory predicts that hermaphrodite seed production is more harmed in stressful environments than that of dioecious populations leading to an advantage for females of dioecious species. Second, in primary forest, we hypothesized that dioecious species would show demographic advantage over monomorphic ones. We used data from two temperate forest plots in Northeast China surveyed over 10 years to compare the rates of growth and mortality of tree species with contrasting breeding systems in both secondary and primary forests. We assessed the effect of breeding system on the growth‐mortality trade‐off, while controlling for other traits usually considered as correlates of growth and mortality rates. We show that in the secondary forest, dioecious species showed weak advantage in demographic rates compared with monomorphic species; dioecious species showed considerably both lower relative growth and mortality rates compared to the hermaphrodites in the primary forest over 10 years, consistent with a priori predictions. Hermaphrodites showed strong growth‐mortality trade‐offs across forest stages, even when possibly confounding factors had been accounted for. These results suggest that sexual system influences community succession and assembly by acting on the rates of growth and mortality, and the trade‐off between them. As vegetation develops, the demographic differences between breeding systems are much larger. Our results demonstrate the association between breeding system, succession, and community assembly and that this relationship is succession‐stage dependent. Our findings support the suggestion that the demographic advantage of dioecious species facilitates the coexistence of sexual systems in primary forest.     

Seed dispersal spectra: a comparison of temperate plant communities

Abstract. We compare the dispersal spectra of diaspores from varied plant communities in Australia, New Zealand, and North America, assigning dispersal mode to each diaspore type on the basis of apparent morphological adaptations. Species with ballistic and external dispersal modes were uncommon in most communities we surveyed. Ant dispersal was also rather uncommon, except in some Australian sclerophyll vegetation types. The frequency of vertebrate dispersal ranged up to 60% of the flora, the highest frequencies occurring in New Zealand forests. Wind dispersal ranged as high as 70% of the flora, with the highest values in Alaska, but usually comprised 10–30% of the flora. Many species in most communities had diaspores with no special morphological device for dispersal. Physiognomically similar vegetation types indifferentbiogeographic regions usually had somewhat dissimilar dispersal spectra. The frequency of dispersal by vertebrates often increased and the frequency of species with no special dispersal device decreased along gradients of increasing vertical diversity of vegetation structure. Elevation and moisture gradients also exhibited shifts in dispersal spectra. Within Australia, vertebrate- and wind-dispersal increased in frequency along a soil-fertility gradient, and dispersal by ants and by no special device decreased. Habitat breadths (across plant communities) and microhabitat breadths (within communities) for species of each major dispersal type did not show consistent differences, in general. Ant-dispersed species often had lower cover-values than other species in several Australian vegetation types. We discuss the ecological bases of these differences in dispersal spectra in terms of the availability of dispersal agents, seed size, and other ecological constraints. Seed size is suggested to be one ecological factor that is probably of general relevance to the evolution of dispersal syndromes.     

Reproductive uncertainty and the relative competitiveness of simultaneous hermaphroditism versus dioecy

Hermaphroditism is typically associated with a sedentary existence, whereas dioecy is associated with mobility. This pattern is reflected within flowering plants, as dioecious species commonly possess traits that promote high dispersal. We investigated these associations with three population dynamics models (an individual-based simulation and two mathematical models, one deterministic and the other stochastic) that allowed us to examine competition for space between a hermaphroditic and dioecious species from different perspectives. The competing species are identical in every way but their sexual system. Separation of the sexes increases the variances of pollen import and seed dispersal for the dioecious species. These variances propagate through subsequent reproductive processes and ultimately reduce mean recruitment as a result of nonlinear averaging (Jensen's inequality). A dioecious species could overcome this disadvantage simply by producing more gametes than hermaphrodites; however, in line with the association with mobility, selection on dioecious species should also favor traits that reduce reproductive uncertainty, such as extensive dispersal.     

Spatial congruence between ecotones and range-restricted species: implications for conservation biogeography at the sub-continental scale

Aim To examine whether at a sub‐continental scale range‐limited species tend to occur close to areas of transition between vegetation boundaries more often than expected by chance. Location South Africa and Lesotho. Methods We examined the relationship between the distance of a grid square to ecological transition areas between vegetation types and both avian and frog range‐limited species richness in the quadrat. We used quadrats at a spatial resolution of quarter degree (15′ × 15′≈ 676 km²). Spatial congruence between areas representing range‐restricted species and those representing ecological transition zones was assessed using a random draw technique. Results Species richness and range size rarity are generally negatively correlated with distance to transition areas between vegetation communities when analysed for the whole region for both groups. Although this relationship becomes weaker after controlling for environmental energy and topographical heterogeneity, the explanatory power of distance to transition areas remains significant, and compared to the different biomes examined, accounts for most of the variation in bird richness (20%), frog richness (18%), range‐restricted bird species (17%) and range‐restricted frog species (16%) in the savanna biome. The random draw technique indicated that areas representing range‐restricted species were situated significantly closer in space to those areas representing transition areas between vegetation communities than expected by chance. Main conclusions We find that at the sub‐continental scale, when examined for South Africa, areas of transition between vegetation communities hold concentrations of range‐limited species in both birds and frogs. We find that South African endemic/range‐limited birds and frogs are located closer to ecological transition zones than endemics and non‐endemics combined. This has important implications for ongoing conservation planning in a biogeographical context.     

Population structure, physiology and ecohydrological impacts of dioecious riparian tree species of western North America

The global water cycle is intimately linked to vegetation structure and function. Nowhere is this more apparent than in the arid west where riparian forests serve as ribbons of productivity in otherwise mostly unproductive landscapes. Dioecy is common among tree species that make up western North American riparian forests. There are intrinsic physiological differences between male and female dioecious riparian trees that may influence population structure (i.e., the ratio of male to female trees) and impact ecohydrology at large scales. In this paper, we review the current literature on sex ratio patterns and physiology of dioecious riparian tree species. Then develop a conceptual framework of the mechanisms that underlie population structure of dominant riparian tree species. Finally, we identify linkages between population structure and ecohydrological processes such as evapotranspiration and streamflow. A more thorough understanding of the mechanisms that underlie population structure of dominant riparian tree species will enable us to better predict global change impacts on vegetation and water cycling at multiple scales.     

Effects of successional status, habit, sexual systems, and pollinators on flowering patterns in tropical rain forest trees

Based on data from observations of 302 tree species at La Selva, Costa Rica, we tested a range of hypotheses about the relationship between flowering parameters such as time, frequency, and duration and ecological features such as successional status, habit, sexual systems, and pollen vectors with and without considering the effect of family membership. We predicted that early successional species would flower any time of the year, but species pollinated by different vectors as well as dioecious species would flower nonrandomly across seasons. However, there was little evidence that flowering time varied with successional status, pollen vectors, and sexual systems. As we predicted, supra-annual flowering was proportionately less common in early successional species as compared to late ones, in understory species as compared to canopy species, and in dioecious species as compared to those with hermaphroditic flowers. When considering phylogeny, however, supra-annual flowering in the understory was not as rare as predicted. Our prediction of longer flowering in the early successional species as compared to late successional species was also supported. Predictions about longer flowering of dioecious species as compared to hermaphroditic species and of species pollinated by generalist vectors as compared to the specialists were not supported, though there was a trend in the expected direction.     

Sexual systems in gymnosperms: A review

The aim of this study was to update figures for the presence of dioecy among the gymnosperms and investigate its correlation with climate, growth form, pollination and seed dispersal syndromes, and risk of extinction. Dioecy was found in almost 65% of contemporary gymnosperm species, a higher percentage than previous estimates. It dominates in 8 of the 12 families. As in angiosperms, dioecious gymnosperms are particularly common in climbers and are more commonly found in tropical climates. Analysis of the degree of threat using IUCN red list categories showed that the proportion of threatened species is higher in dioecious than in monoecious species only in temperate climate. The high sensitivity of dioecious species to environmental changes associated with human activity in temperate climate may explain this phenomenon. The monophyly of extant gymnosperms and the relatively small number of species (about 1000) create the possibility of treating them as a model group in investigating the evolution of sexual systems.     

Dioecy Is Associated with High Genetic Diversity and Adaptation Rates in the Plant Genus Silene

About 15,000 angiosperm species (∼6%) have separate sexes, a phenomenon known as dioecy. Why dioecious taxa are so rare is still an open question. Early work reported lower species richness in dioecious compared with nondioecious sister clades, raising the hypothesis that dioecy may be an evolutionary dead-end. This hypothesis has been recently challenged by macroevolutionary analyses that detected no or even positive effect of dioecy on diversification. However, the possible genetic consequences of dioecy at the population level, which could drive the long-term fate of dioecious lineages, have not been tested so far. Here, we used a population genomics approach in the Silene genus to look for possible effects of dioecy, especially for potential evidence of evolutionary handicaps of dioecy underlying the dead-end hypothesis. We collected individual-based RNA-seq data from several populations in 13 closely related species with different sexual systems: seven dioecious, three hermaphroditic, and three gynodioecious species. We show that dioecy is associated with increased genetic diversity, as well as higher selection efficacy both against deleterious mutations and for beneficial mutations. The results hold after controlling for phylogenetic inertia, differences in species census population sizes and geographic ranges. We conclude that dioecious Silene species neither show signs of increased mutational load nor genetic evidence for extinction risk. We discuss these observations in the light of the possible demographic differences between dioecious and self-compatible hermaphroditic species and how this could be related to alternatives to the dead-end hypothesis to explain the rarity of dioecy.