Determinants of sex allocation in a gynodioecious wild strawberry: implications for the evolution of dioecy and sexual dimorphism

One evolutionary pathway from plants with combined male and female functions (hermaphroditism) to those with separate sexes (dioecy) involves females coexisting with hermaphrodites (gynodioecy). The research presented here explores sex allocation in Fragaria virginiana (a gynodioecious wild strawberry), within the context of theory on the gynodioecy–dioecy transition. By growing clonally replicated plants in the greenhouse and surveying six populations in situ, I evaluated the effects of plant size, genotype, sexual identity, population of origin and female frequency on sex allocation. I found significant positive effects of plant size on most sex allocation traits studied. In addition to strong sex-specific allocation patterns, I found significant broad-sense heritabilities for all traits, suggesting that plants could respond to selection. Moreover, there was a negative genetic correlation between pollen production and fruit set per flower within hermaphrodites, lending support to a basic assumption of sex allocation theory. On the other hand, several sex allocation traits, namely pollen and ovules per flower in hermaphrodites, were positively genetically correlated, suggesting that they may act to constrain the evolution of sexual dimorphism. Populations differed in the frequency of females, and females were more prevalent on sites with lower soil moisture and where hermaphrodites were least likely to produce fruit, suggesting that females’ seed fitness relative to that of hermaphrodites may be strongly environment-dependent in this species.     

'Inconstant males' and the maintenance of labile sex expression in subdioecious plants

* Here, we evaluate the role of pollen limitation and selfing in the maintenance of labile sex expression in subdioecious plant species. * We used a literature survey to explore which factors correlated with a significant occurrence of hermaphrodites in dioecious species. We developed models to explore the selective maintenance of labile sex expression. The models had similar ecological assumptions but differed in the genetic basis of sex lability. * We found that a significant frequency of hermaphrodites was associated with animal pollination, and that hermaphrodites were 'inconstant' males with perfect flowers, suggesting evolution through the gynodioecious pathway. Models showed that a modifier converting pure males into inconstant males could be maintained under a wide range of reduction in both male and female fitness. Pollen limitation and self-fertilization facilitated invasion of the modifier. Depending on the genetics of sex determination, we found pure dioecy, stable subdioecy (trioecy), and situations where inconstant males coexisted with either pure females or pure males. Under selfing and pollen limitation, certain conditions selected for inconstant males which will drive populations to extinction. * We discuss our results in relation to the evolution towards, and the breakdown of, dioecy, and the ecological and evolutionary implications of labile sex expression.     

Sex‐specific reproductive components and pollination ecology in the subdioecious shrub Fuchsia microphylla

In subdioecious populations, functional female, male and hermaphrodite individuals coexist. Subdioecy may be a transitional state towards dioecy or a breakdown of dioecy, although lability in sex expression may maintain subdioecy as a stable condition. To better understand the ecological aspects involved in sex ratio dynamics and breeding system evolution, we studied the pollination and female fitness components of female and hermaphrodite individuals of the subdioecious shrub Fuchsia microphylla. In two natural populations at the Trans‐Mexican Volcanic Belt we estimated female frequency and several reproductive components of female and hermaphrodite plants under natural pollination and experimental pollination treatments. Average female frequency was 42%, and on average, 42.5% of hermaphrodites produced fruits. Female plants showed a 17‐fold female fertility advantage over hermaphrodites through increased fruit production, as the number of seeds and germination rates did not differ between morphs. Hermaphrodite flowers were larger, with similar nectar production and concentration to female flowers, and pollinators did not show consistent morph preferences. Some hermaphrodites produced fruits autonomously, and female flowers excluded from pollinators produced fruits putatively by apomixis. Fruit production in hermaphrodites, but not in females, was related to height, suggesting increased investment of hermaphrodites in the female function at higher resource status. For sex ratios to be at equilibrium, the female fertility advantage should be reduced about eightfold. However, it may be that hermaphrodites are maintained by producing fruits at no cost to the male function at higher resource status, as the gender plasticity hypothesis proposes.     

Gender variation inSilene acaulis (Caryophyllaceae)

Silene acaulis (Caryophyllaceae) is an alpine-arctic plant with a gynodioecious breeding system, but significant variation in sex expression has been reported. In addition, population sex ratio may be modified by the anther-smutMicrobotryum violaceum (Pers.)Deml & Oberwinkler, which sterilizes individuals of both sexes. A survey was undertaken at several sites on Baffin Island, Canada, to determine sex ratio and assess variation in female function among morphologically hermaphroditic individuals. The degree of anthersmut infection was also measured. Six sites had high female frequencies ranging from 72–80% and < 2% smut infection. High female frequencies may indicate cytoplasmic control of male-sterility. A seventh site from a mesic habitat had only 50% females and a higher rate of smut infection (22%). Of the three sites studied in detail, 84% of females set at least one capsule compared to only 25% of the hermaphrodites, indicating reduced female function. Hermaphrodites displayed significant variability in female function. Flowers with short styles (< 4.0mm) had degenerated ovules, and field estimates confirmed that only 5% of these individuals set capsules, but comprised the majority (> 55%) of hermaphrodites. Although hermaphrodites with short-styled flowers functioned solely as males, there was no increase in pollen production compared to long-styled hermaphrodites. Long-styled hermaphrodites produced the same number of ovules as females, and all set at least one capsule but these plants were uncommon (< 11%) at all sites.     

Reproductive biology of the dioecious Canary Islands endemic Withania aristata (Solanaceae)

We confirmed functional dioecy of Withania aristata via field and greenhouse studies. Male flowers are significantly larger. Female flowers bear stamens with no pollen; males bear 220?000 grains. Stigmata of male flowers senesce in buds. Anatomical observations confirm more ovules in females and an ovarian nectary in both sexes. We detected nectar in female flowers in the greenhouse but found no nectar in males. Thus, males offer pollen and females nectar. Females bear large numbers of fruits and, infrequently, male plants bear few significantly smaller fruits with few seeds. Outcrosses of females (self crosses impossible without pollen) yielded fruits in young buds, older buds, and open flowers. Self crosses of male flowers succeeded only with very young buds. Although functionally dioecious, this species manifests self-compatibility; however, no fruits are produced autonomously. Bee species (Lassioglossum, Amegilla, Apis) visit flowers and mature buds. Bud visits in which bees force petal tips apart, coupled with self-compatibility, may explain infrequent fruit on males. Thus, dioecy in W. aristata seems to have evolved from self-compatible ancestors, that leaky dioecy may have been favored during colonization, and, that despite autogamy and a low floral visition rate, this endemic enjoys a high rate of reproductive success.     

Reproductive biology and relative male and female fitness in a trioecious cactus,Pachycereus pringlei (Cactaceae)

We describe the breeding system of an autotetraploid trioecious cactus, Pachycereus pringlei, provide estimates of the fitnesses of males and females relative to that of hermaphrodites, and discuss the role played by pollinators in the maintenance of three sexual morphs. Relatively high frequencies of females (45%) and males (26%) exist in coastal desert populations around Bahia Kino, Sonora, Mexico. They differ from hermaphrodites in flower size (females only), initiation of the flowering season, number of flowers produced per night and per season, sucrose content of nectar, and, in females, number of fruits produced per season under open pollination and in response to hand-pollination. Major similarities between the sex classes include overall plant size, nectar volume per flower, percent fruit set in open-pollinated flowers of females and hermaphrodites, seed mass and number of seeds per fruit, and pollen mass per flower in males and hermaphrodites. Hermaphrodites are self-compatible, and the selfing rate is high (65%). Levels of inbreeding depression in selfed fruits and seeds appear to be low. Fruit set is strongly pollinator-dependent in females but much less so in hermaphrodites. Relative fitness of males and females, as measured by annual production of pollen or seeds, is at least 1.5 times higher than that of the corresponding sex function in hermaphrodites. Given the high selfing rate and apparent lack of inbreeding depression, these fitness differences are insufficient to explain the occurrence of trioecy in this species.     

Differences in female reproductive success between female and hermaphrodite individuals in the subdioecious shrub Eurya japonica (Theaceae)

Subdioecy is thought to occupy a transitional position in the gynodioecy–dioecy pathway, explaining one of the evolutionary routes from hermaphroditism to dioecy. Quantifying any female reproductive advantage of females versus hermaphrodites is fundamental to examining the spectrum between subdioecy and dioecy; however, this is challenging, as multiple interacting factors, such as pollen limitation and resource availability, affect plant reproduction. We compared the female reproductive success of females and hermaphrodites via a field experiment in which we hand‐pollinated individuals of the subdioecious shrub Eurya japonica of similar size growing under similar light conditions. Effects of pollen limitation and seed quality were also evaluated through comparing the results of hand‐ and natural‐pollination treatments and performing additional laboratory and greenhouse experiments. Overall, females had higher fruit set and produced heavier fruit and more seeds than hermaphrodites, and these results were more pronounced for hand‐pollinated than for natural‐pollinated plants of both sexes. We also found that seeds naturally produced by females had a higher mean germination rate. These results indicate that females had a pronounced advantage in female reproductive success under conditions of no pollen limitation. The sexual difference in the degree of pollen limitation suggests a pollinator‐mediated interaction, whereas the higher female reproductive success of females even under natural conditions implies that E. japonica is a good model species for elucidating the later stages of the gynodioecy–dioecy pathway.     

Selfish male‐determining element favors the transition from hermaphroditism to androdioecy

According to the current, widely accepted paradigm, the evolutionary transition from hermaphroditism toward separate sexes occurs in two successive steps: an initial, intermediate step in which unisexual individuals, male or female, sterility mutants coexist with hermaphrodites and a final step that definitively establishes dioecy. Two nonexclusive processes can drive this transition: inbreeding avoidance and reallocation of resources from one sexual function to the other. Here, we report results of controlled crosses between males and hermaphrodites in Phillyrea angustifolia, an androdioecious species with two mutually intercompatible, but intraincompatible groups of hermaphrodites. We observed different segregation patterns that can be explained by: (1) epistatic interactions between two unlinked diallelic loci, determining sex and mating compatibility, and (2) a mutation with pleiotropic effects: female sterility, full compatibility of males with both hermaphrodite incompatibility groups, and complete male‐biased sex‐ratio distortion in one of the two groups. Modeling shows that these mechanisms can explain the high frequency of males in populations of P. angustifolia and can promote the maintenance of androdioecy without requiring inbreeding depression or resource reallocation. We thus argue that segregation distortion establishes the right conditions for the evolution of cryptic dioecy and potentially initiates the evolution toward separate sexes.     

Floral development in the androdioecious tree Tapiscia sinensis: Implications for the evolution to androdioecy

The evolutionary pathway between hermaphroditism and dioecy (females and males in a single population) draws widespread interests, and androdioecy (bisexuals and males in a single population) is rarely achieved as an intermediate state between the two breeding systems. Flower bud differentiations in the pistils of hermaphrodites and the pistillodes of males in androdioecious Tapiscia sinensis Oliv. are investigated by routine paraffin section technology, light microscopy, and scanning electron microscopy. A phylogenetic approach is used to analyze the origin of androdioecy. In T. sinensis, hermaphroditic flowers (HF) and male flowers (MF) experienced a similar development pattern in early flower bud differentiation, including the initiation of tepals and stamens. However, the carpel differentiation of MF and HF proceed in different patterns. In HF, the central zone bulges out and produces a ring meristem on which two to three carpel primordia emerge, which eventually developed into a normal pistil with a stigma, a style, and an ovary. However, in most MF, vestigial pistils are stem‐like (type I), and very few have an empty ovary (type II) or a sterile ovule (type III). Moreover, the evolution of sexual systems within the Huerteales indicates that hermaphroditism is the primitive character of T. sinensis. Tapiscia sinensis shows different degrees of reduction between male flowers and bisexual ones in the evolution to dioecy. Functional androdioecy originated from a hermaphroditic ancestor in T. sinensis and, as an intermediate sexual system, involves evolution from hermaphrodites to dioecy.     

On the possible role of nonreproductive traits for the evolution of unisexuality: Life‐history variation among males,females, and hermaphrodites in Opuntia robusta (Cactaceae)

In angiosperms, dioecy has arisen in 871–5,000 independent events, distributed in approximately 43% of the flowering families. The reproductive superiority of unisexuals has been the favorite explanation for the evolution of separate sexes. However, in several instances, the observed reproductive performance of unisexuals, if any, does not seem to compensate for the loss of one of the sex functions. The involvement of fitness components not directly associated with reproduction is a plausible hypothesis that has received little attention. Life‐history traits recently recognized as predictors of plant performance were compared among males, females, and hermaphrodites of a rare trioecious Opuntia robusta population in the field, using the cladode as the study unit. Cladode mortality by domestic herbivores was common and higher in females and hermaphrodites than in males. Males, females, or both displayed lower shrinkage and higher rates of survival, growth, and reproductive frequency than hermaphrodites. Unisexuals simultaneously outperformed hermaphrodites in demographic traits known to compete for common limiting resources, such as the acceleration of reproductive maturation (progenesis) and survival. A meta‐analysis combining the outcomes of each of the analyzed life‐history traits revealed a tendency of males (d₊₊ = 1.03) and females (d₊₊ = 0.93) to outperform hermaphrodites in presumably costly demographic options. Clonality is induced by human or domestic animal plant sectioning; and males and females highly exceeded hermaphrodites in their clonality potential by a factor of 8.3 and 5.3, respectively. The performances of unisexuals in the analyzed life‐history traits may enhance their reproductive potential in the long run and their clonality potential and could explain the observed increase of unisexuality in the population. Life‐history traits can be crucial for the evolution of unisexuality, but their impact appears to be habitat specific and may involve broad ontogenetic changes.     

The Evolution of Dicliny in Schiedea (Caryophyllaceae), an Endemic Hawaiian Genus

Abstract The evolution of dioecy was studied in Schiedea (Caryophyllaceae), a genus endemic to the Hawaiian Islands. Eight of the 22 species are diclinous, possessing gynodioecious, subdioecious, or dioecious breeding systems. A biogeographic analysis of the genus indicates that the ancestor of Schiedea colonized early in the history of the Hawaiian Islands. Subsequently, hermaphroditic species appear to have engaged in inter-island colonization more frequently than diclinous species. For this reason, single-island endemism and dicliny are more common on the older Hawaiian Islands. Strong inbreeding depression was detected in three species of Schiedea , indicating that genetic factors have played a role in the evolution of dicliny. Depending on the level of natural selfing, the expression of inbreeding depressioin may have favored the outcrossed progeny of rare females in populations, and eventually the evolution of dioecy. In contrast to evidence for inbreeding depression, there was very little evidence that resource allocation, sex lability, or habitat partitioning have played an important role in the evolution of dioecy. In subdioecious S. globosa hermaphrodites were largely male in function, and in gynodioecious S. salicaria females and hermaphrodites were equivalent in nearly all aspects of female function that could be measured. Variation in breeding systems in Schiedea and the closely related Alsinidendron may result from the past history of population bottlenecks that have resulted in varying levels of inbreeding depression.     

Evidence of gynodioecy and sex ratio variation in Wurmbea biglandulosa (Colchicaceae)

 A valuable approach to understanding the evolution of gender dimorphism involves studies of single species that exhibit intraspecific variation in sexual systems. Here we survey sex ratios in 35 populations of Wurmbea biglandulosa, previously described as hermaphroditic. We found pronounced intraspecific variation in sexual systems; populations in the northeastern part of the species' range were hermaphroditic, whereas other populations were gynodioecious and contained 2–44% females. Populations with lower annual rainfall were more likely to be gynodioecious, supporting the view that gender dimorphism evolves more frequently in harsher environments. In gynodioecious populations, however, female frequency was not related to either annual rainfall or habitat, indicating that other factors are important in determining sex ratio variation. Females had smaller flowers and shorter stems than did hermaphrodites, potentially providing a basis for resource compensation. A female fecundity advantage may contribute to the maintenance of females in populations because females produced more ovuliferous flowers and had more ovules per flower than did hermaphrodites. Received March 2, 2001 Accepted February 25, 2002     

Gynodioecy to dioecy: are we there yet?

Background

The ‘gynodioecy–dioecy pathway’ is considered to be one of the most important evolutionary routes from hermaphroditism to separate sexes (dioecy). Despite a large accumulation of evidence for female seed fertility advantages in gynodioecious species (females and hermaphrodites coexist) in support of the first step in the gynodioecy–dioecy pathway, we still have very little evidence for the second step, i.e. the transition from gynodioecy to dioecy.

Scope

We review the literature to evaluate whether basic predictions by theory are supported. To establish whether females'' seed fertility advantage and frequencies are sufficient to favour the invasion of males, we review these for species along the gynodioecy–dioecy pathway published in the last 5 years. We then review the empirical evidence for predictions deriving from the second step, i.e. hermaphrodites'' male fertility increases with female frequency, selection favours greater male fertility in hermaphrodites in gynodioecious species, and, where males and hermaphrodites coexist with females (subdioecy), males have greater male fertility than hermaphrodites. We review how genetic control and certain ecological features (pollen limitation, selfing, plasticity in sex expression and antagonists) influence the trajectory of a population along the gynodioecy–dioecy pathway.

Conclusions

Females tend to have greater seed fertility advantages over hermaphrodites where the two coexist, and this advantage is positively correlated with female frequency across species, as predicted by theory. A limited number of studies in subdioecious species have demonstrated that males have an advantage over hermaphrodites, as also predicted by theory. However, less evidence exists for phenotypic selection to increase male traits of hermaphrodites or for increasing male function of hermaphrodites in populations with high female frequency. A few key case studies underline the importance of examining multiple components of male fertility and the roles of pollen limitation, selfing and plasticity, when evaluating advantages. We conclude that we do not yet have a full understanding of the transition from gynodioecy to dioecy.     

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.     

Sexual and temporal variations in floral scent in the subdioecious shrub Eurya japonica Thunb

In many flowering plants, floral scents are a significant trait for visitors, playing an important role in attracting pollinators and/or detracting herbivores. The evolution of flowering plants from hermaphroditism to dioecy is often accompanied by sexual dimorphism in floral scent. In this study, floral scents emitted by different sexual morphs of the subdioecious shrub Eurya japonica Thunb. were collected using a dynamic headspace method, and sexual and temporal variations were evaluated by gas chromatography–mass spectrometry (GC–MS). Two volatiles, α‐pinene and linalool, were identified as the major components of floral scents in females, hermaphrodites, and males. The males emit higher amounts of floral scents, particularly α‐pinene, compared to females or hermaphrodites. Floral scents emitted by males generally decrease as flowers enter senescence, whereas those from females or hermaphrodites do not significantly differ. Intraspecific variations in floral scents of subdioecious species provided by this study would contribute to better understanding of sexual dimorphism in floral scent.     

FLOWERING,SEX RATIOS,POLLEN-OVULE RATIOS,FRUIT SET,AND REPRODUCTIVE EFFORT OF A DIOECIOUS TREE,MYRISTICA INSIPIDA (MYRISTICACEAE), IN TWO DIFFERENT RAIN FOREST COMMUNITIES

The flowering of Myristica insipida R. Br. was studied in two rain forest communities in northern Queensland. This dioecious, subcanopy tree had a male-biased sex ratio at both study sites. In the lowland population the male-bias could be attributed to males (trees producing staminate flowers) starting to flower at a smaller average size than females (trees producing pistillate flowers). There were no intersexual differences in spacing or distribution within the study sites. Males trees flowered earlier, flowered longer, and produced over twice as many flowers as females during the study season. Although the onset of flowering was rather variable, 18–22 days following heavy rains, most trees had a synchronous period of maximum flowering. Pollination manipulations determined that there was no fruit development without pollination, and that increasing pollen loads resulted in increased fruit set with diminishing effect. Taking into account the sex-ratios and intersexual differences in flower production, the pollen-ovule ratio was calculated to be 16,000–19,000. Male trees were found to expend more energy on flowering than female trees. Open-pollination resulted in 1.0% of female flowers setting fruit. The much greater cost of fruit production resulted in females expending 421% more energy on reproduction than males. Fruit and seed production were judged to be pollination-limited. Nonetheless, this species exhibited several characteristics that are predicted if dioecy evolved by means of sexual selection.     

Maintenance of gynodioecy in Wurmbea biglandulosa (Colchicaceae): gender differences in seed production and progeny success

 In gynodioecious species, females contribute genes to future generations only through ovules, and to persist in populations they must have a compensatory advantage compared with hermaphrodites that reproduce via ovules and pollen. This compensation can result from greater fecundity and/or superior success of progeny from females. We examined differences in seed production and progeny success between females and hermaphrodites in the geophyte Wurmbea biglandulosa to explain the maintenance of females. Females produced more ovuliferous flowers and had more ovules per flower than did hermaphrodites but this did not necessarily result in greater fecundity, in part because seed production of females was pollen-limited. Over four years in one population, open-pollinated females produced 1.32 more seeds than open-pollinated hermaphrodites (range 1.09–1.63). In two other populations examined for one year only females produced 1.07 and 0.79 as many seeds as hermaphrodites. Seed production of open-pollinated females and hermaphrodites was only 55% and 73% that of cross-pollinated plants, respectively, indicating that both genders were pollen-limited but females more so than hermaphrodites. Open-pollinated seeds from females were 1.18–1.27 times more likely to germinate than seeds from hermaphrodites. No gender differences existed in seedling growth or survival. Hermaphrodites were self-compatible, but selfed seed set was only 80% that of crossed seed set. Crossed seed set of females and hermaphrodites did not differ. Assuming nuclear control of male sterility, relative female fitness is insufficient to maintain females at their current frequencies of 17%, and substantial female fitness advantages at later life-cycle stages are required. Received May 4, 2001 Accepted February 25, 2002     

Androdioecy and hermaphroditism in five species of clam shrimps (Crustacea: Branchiopoda: Spinicaudata) from India and Thailand

Crustaceans in the order Spinicaudata display a broad range of reproductive strategies, ranging from pure hermaphroditism to pure dioecy (separate males and females), and intermediate combinations. One particularly interesting genus of these “clam shrimps” is Eulimnadia. Based on offspring sex ratios, it has been suggested that all members of the genus are androdioecious: populations consist of mixtures of males and hermaphrodites. However, only two of the ~40 species in this genus have been examined histologically to confirm the presence of ovotestes in the purported hermaphrodites of this group. Here, we report both sex ratio and histological evidence showing that populations of five additional Eulimnadia species from India and Thailand are indeed mixes of males and hermaphrodites (four species) or hermaphrodite only (one species). Sex ratios of adults and offspring from isolated hermaphrodites are in accordance with those previously reported for 15 Eulimnadia species, and histological assays of four of the five species show the presence of both testicular and ovarian tissue in these hermaphrodites. As has been previously reported, the testicular tissue in members of these Eulimnadia spp. is located in a small section at the distal end of the gonad. In addition, the sperm produced in these hermaphrodites forms distinct plaques of compacted chromatin. Overall, these data are consistent with a single origin of hermaphroditism in Eulimnadia, and support the notion that all members of the genus are either androdioecious or all‐hermaphroditic.     

Low siring success of females with an acquired male function illustrates the legacy of sexual dimorphism in constraining the breakdown of dioecy

Dioecy has often broken down in flowering plants, yielding functional hermaphroditism. We reasoned that evolutionary transitions from dioecy to functional hermaphroditism must overcome an inertia of sexual dimorphism, because modified males or females will express the opposite sexual function for which their phenotypes have been optimised. We tested this prediction by assessing the siring success of monoecious individuals of the plant Mercurialis annua with an acquired male function but that are phenotypically still female‐like. We found that pollen dispersed by female‐like monoecious individuals was ~ 1/3 poorer at siring outcrossed offspring than pollen from monoecious individuals with an alternative male‐like inflorescence. We conclude that whereas dioecy might evolve from functional hermaphroditism by conferring upon individuals certain benefits of sexual specialisation, reversion from a strategy of separate sexes to one of combined sexes must overcome constraints imposed by the advantages of sexual dimorphism. The breakdown of dioecy must therefore often be limited to situations in which outcrossing cannot be maintained and where selection favours a capacity for inbreeding by functional hermaphrodites.