Phylogenetic relationships of functionally dioecious FICUS (Moraceae) based on ribosomal DNA sequences and morphology

Figs (Ficus, Moraceae) are either monoecious or gynodioecious depending on the arrangement of unisexual florets within the specialized inflorescence or syconium. The gynodioecious species are functionally dioecious due to the impact of pollinating fig wasps (Hymenoptera: Agaonidae) on the maturation of fig seeds. The evolutionary relationships of functionally dioecious figs (Ficus subg. Ficus) were examined through phylogenetic analyses based on the internal transcribed spacer (ITS) region of nuclear ribosomal DNA and morphology. Forty-six species representing each monoecious subgenus and each section of functionally dioecious subg. Ficus were included in parsimony analyses based on 180 molecular characters and 61 morphological characters that were potentially informative. Separate and combined analyses of molecular and morphological data sets suggested that functionally dioecious figs are not monophyletic and that monoecious subg. Sycomorus is derived within a dioecious clade. The combined analysis indicated one or two origins of functional dioecy in the genus and at least two reversals to monoecy within a functionally dioecious lineage. The exclusion of breeding system and related characters from the analysis also indicated two shifts from monoecy to functional dioecy and two reversals. The associations of pollinating fig wasps were congruent with host fig phylogeny and further supported a revised classification of Ficus.     

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.     

Dioecy and its correlates in the flowering plants

Considerable effort has been spent documenting correlations between dioecy and various ecological and morphological traits for the purpose of testing hypotheses about conditions that favor dioecy. The data analyzed in these studies, with few exceptions, come from local floras, within which it was possible to contrast the subsets of dioecious and nondioecious taxa with regard to the traits in question. However, if there is a strong phylogenetic component to the presence or absence of dioecy, regional sampling may result in spurious associations. Here, we report results of a categorical multivariate analysis of the strengths of various associations of dioecy with other traits over all flowering plants. Families were scored for presence of absence of monoecy or dioecy, systematic position, numbers of species and genera, growth forms, modes of pollination and dispersal, geographic distribution, and trophic status. Seven percent of angiosperm genera (959 of 13,500) contain at least some dioecious species, and ≈6% of angiosperm species (14,620 of 240,000) are dioecious. The most consistent associations in the data set relate the presence of dioecy to monoecy, wind or water pollination, and climbing growth. At both the family and the genus level, insect pollination is underrepresented among dioecious plants. At the family level, a positive correlation between dioecy and woody growth results primarily from the association between dioecy and climbing growth (whether woody or herbaceous) because neither the tree nor the shrub growth forms alone are consistently correlated with a family's tendency to include dioecious members. Dioecy appears to have evolved most frequently via monoecy, perhaps through divergent adjustments of floral sex ratios between individual plants. Monoecy itself is related to abiotic pollination and climbing growth as revealed by multivariate analysis. Dioecy and monoecy are concentrated in the less advanced superorders of Thorne (1992) and subclasses of Cronquist (1988). The frequency of dioecy found in a local flora therefore reflects the level of dioecy in its particular pool of families as much as, or more than, local selective factors. The positive associations of dioecy with abiotic pollination and monoecy are related to floral developmental and morphological attributes, as is the negative association with bird and bat pollination; the positive association of dioecy with climbing growth is tentatively explained in terms of differential selection for optimal resource allocation to sexual function. If rapid upward growth is at a premium in climbers and if fruit set at least temporarily inhibits growth or requires the production of thicker, more slowly growing stems to support heavy fruits, it might be advantageous to postpone femaleness. If the effect is strong, this may favor male plants.     

Sexual specialization and inbreeding avoidance in the evolution of dioecy

Dioecy has evolved independently, many times, among unrelated taxa. It also appears to have evolved along two contrasting pathways: (1) from hermaphroditism via monoecy to dioecy and (2) from hermaphroditism via gynodioecy to dioecy. Most dioecious plants have close cosexual relatives with some means of promoting outcrossing (e.g., herkogamy, dichogamy, self-incompatibility, or monoecy). To the extent that these devices prevent inbreeding, the evolution of dioecy in these species cannot logically be attributed to selection for outcrossing. In these cases, the evolution of dioecy is, we believe, due to selection for sexual specialization. However, in other species, that lack outbreeding close relatives, dioecy may have evolved from gynodioecy (males and hermaphrodites) as an outbreeding device. Subsequent disruptive selection and selection for sexual specialization may have also shaped the evolution of dioecy from gynodioecy in these species, resulting in two genetically determined, constant sex morphs. Both pathways for the evolution of dioecy require the operation of disruptive selection, though the gynodioecy route involves more restrictive disruptive selection and a genetic designation of gender. In contrast, the monoecy route is not dependent on the genetic designation of two sex morphs, but, rather, allows the possibility of sexual intermediates and sexual lability. Both pathways produce one morph in which maleness is suppressed and another in which the female function is negligible or nonexistent—the reproductive mode recognized as dioecy. Evidence is presented here to support the thesis that instances of sexual lability, the presence of an array of sexual intermediates, sex-switching, and sexual niche segregation can be explained in terms of the pathway that was taken in the evolution of a particular dioecious species. In addition, the degree of sexual dimorphism seen in dioecious species is correlated with mode of pollination (insector wind-pollinated) and other ecological factors.     

Pollination and parasitism in functionally dioecious figs

Fig wasps (Agaonidae: Hymenoptera) are seed predators and their interactions with Ficus species (Moraceae) range from mutualism to parasitism. Recently considerable attention has been paid to conflicts of interest between the mutualists and how they are resolved in monoecious fig species. However, despite the fact that different conflicts can arise, little is known about the factors that influence the persistence of the mutualism in functionally dioecious Ficus. We studied the fig pollinator mutualism in 14 functionally dioecious fig species and one monoecious species from tropical lowland rainforests near Madang, Papua New Guinea. Observations and experiments suggest that (i) pollinating wasps are monophagous and attracted to a particular host species; (ii) pollinating and non-pollinating wasps are equally attracted to gall (male) figs and seed (female) figs in functionally dioecious species; (iii) differing style lengths between gall figs and seed figs may explain why pollinators do not develop in the latter; (iv) negative density dependence may stabilize the interaction between pollinating wasps and their parasitoids; and (v) seed figs may reduce the search efficiency of non-pollinators. This increased pollinator production without a corresponding decrease in seed production could provide an advantage for dioecy in conditions where pollinators are limiting.     

The evolution of dioecy, heterodichogamy, and labile sex expression in Acer

The northern hemisphere tree genus Acer comprises 124 species, most of them monoecious, but 13 dioecious. The monoecious species flower dichogamously, duodichogamously (male, female, male), or in some species heterodichogamously (two morphs that each produce male and female flowers but at reciprocal times). Dioecious species cannot engage in these temporal strategies. Using a phylogeny for 66 species and subspecies obtained from 6600 nucleotides of chloroplast introns, spacers, and a protein-coding gene, we address the hypothesis (Pannell and Verdú, Evolution 60: 660-673. 2006) that dioecy evolved from heterodichogamy. This hypothesis was based on phylogenetic analyses (Gleiser and Verdú, New Phytol. 165: 633-640. 2005) that included 29-39 species of Acer coded for five sexual strategies (duodichogamous monoecy, heterodichogamous androdioecy, heterodichogamous trioecy, dichogamous subdioecy, and dioecy) treated as ordered states or as a single continuous variable. When reviewing the basis for these scorings, we found errors that together with the small taxon sample, cast doubt on the earlier inferences. Based on published studies, we coded 56 species of Acer for four sexual strategies, dioecy, monoecy with dichogamous or duodichogamous flowering, monoecy with heterodichogamous flowering, or labile sex expression, in which individuals reverse their sex allocation depending on environment-phenotype interactions. Using Bayesian character mapping, we infer an average of 15 transformations, a third of them involving changes from monoecy-cum-duodichogamy to dioecy; less frequent were changes from this strategy to heterodichogamy; dioecy rarely reverts to other sexual systems. Contra the earlier inferences, we found no switches between heterodichogamy and dioecy. Unexpectedly, most of the species with labile sex expression are grouped together, suggesting that phenotypic plasticity in Acer may be a heritable sexual strategy. Because of the complex flowering phenologies, however, a concern remains that monoecy in Acer might not always be distinguishable from labile sex expression, which needs to be addressed by long-term monitoring of monoecious trees. The 13 dioecious species occur in phylogenetically disparate clades that date back to the Late Eocene and Oligocene, judging from a fossil-calibrated relaxed molecular clock.     

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.     

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.     

Clonal genetic structure and diversity in populations of an aquatic plant with combined vs. separate sexes

Clonality is often implicated in models of the evolution of dioecy, but few studies have explicitly compared clonal structure between plant sexual systems, or between the sexes in dioecious populations. Here, we exploit the occurrence of monoecy and dioecy in clonal Sagittaria latifola (Alismataceae) to evaluate two main hypotheses: (i) clone sizes are smaller in monoecious than dioecious populations, because of constraints imposed on clone size by costs associated with geitonogamy; (ii) in dioecious populations, male clones are larger and flower more often than female clones because of sex‐differential reproductive costs. Differences in clone size and flowering could result in discordance between ramet‐ and genet‐based sex ratios. We used spatially explicit sampling to address these hypotheses in 10 monoecious and 11 dioecious populations of S. latifolia at the northern range limit in Eastern North America. In contrast to our predictions, monoecious clones were significantly larger than dioecious clones, probably due to their higher rates of vegetative growth and corm production, and in dioecious populations, there was no difference in clone size between females and males; ramet‐ and genet‐based sex ratios were therefore highly correlated. Genotypic diversity declined with latitude for both sexual systems, but monoecious populations exhibited lower genotypic richness. Differences in life history between the sexual systems of S. latifolia appear to be the most important determinants of clonal structure and diversity.     

Repeated evolution of dioecy from monoecy in Siparunaceae (Laurales)

Siparunaceae comprise Glossocalyx with one species in West Africa and Siparuna with 65 species in the neotropics; all have unisexual flowers, and 15 species are monoecious, 50 dioecious. Parsimony and maximum likelihood analyses of combined nuclear ribosomal ITS and chloroplast trnL-trnF intergenic spacer sequences yielded almost identical topologies, which were used to trace the evolution of the two sexual systems. The African species, which is dioecious, was sister to all neotropical species, and the monoecious species formed a grade basal to a large dioecious Andean clade. Dioecy evolved a second time within the monoecious grade. Geographical mapping of 6,496 herbarium collections from all species sorted by sexual system showed that monoecy is confined to low-lying areas (altitude < 700 m) in the Amazon basin and southern Central America. The only morphological trait with a strong phylogenetic signal is leaf margin shape (entire or toothed), although this character also correlates with altitude, probably reflecting selection on leaf shapes by temperature and rainfall regimes. The data do not reject the molecular clock, and branch lengths suggest that the shift to dioecy in the lowlands occurred many million years after the shift to dioecy in the ancestor of the Andean clade.     

Nutritional Dimorphism in New Guinea Dioecious Figs

The life history of figs (Ficus, Moraceae) involves pollination by specialized insects and seed dispersal by vertebrate frugivores. This three-way interaction raises the possibility of conflict between pollinators and seed dispersers over fig resources. The conflict might be mediated in dioecious figs by the segregation of inflorescences with specialized male and female sexual functions, termed gall figs and seed figs, on separate trees. In dioecious figs, pollinators are intimately associated with gall figs, whereas vertebrate frugivores prefer seed figs and disperse the seeds they contain. Optimal foraging theory predicts that frugivore preference for ripe seed figs is associated with superior nutritional quality when compared to gall figs. We tested this prediction comparing nutrient and mineral properties of ripe figs in 12 functionally dioecious and two monoecious species from New Guinea. Analyses of variance indicated that gall figs contain more fiber and minerals, whereas seed figs contain significantly more carbohydrates and fat. Fruit bats, the primary dispersers of dioecious figs in New Guinea, prefer carbohydrate-rich diets, and from this perspective, seed figs offer a greater nutritional reward than gall figs. More nondigestible fiber in gall figs than seed figs would appear to discourage frugivory. Parallel differences between ripe gall figs and seed figs occur in each independent dioecious lineage whereas nutritional content in monoecious figs is more similar to seed figs. This suggests that sexual dimorphism in nutritional quality might be adaptive and associated with the maintenance of functional dioecy in figs.     

An angiosperm-wide analysis of the gynodioecy–dioecy pathway

Background and Aims

About 6 % of an estimated total of 240 000 species of angiosperms are dioecious. The main precursors of this sexual system are thought to be monoecy and gynodioecy. A previous angiosperm-wide study revealed that many dioecious species have evolved through the monoecy pathway; some case studies and a large body of theoretical research also provide evidence in support of the gynodioecy pathway. If plants have evolved through the gynodioecy pathway, gynodioecious and dioecious species should co-occur in the same genera. However, to date, no large-scale analysis has been conducted to determine the prevalence of the gynodioecy pathway in angiosperms. In this study, this gap in knowledge was addressed by performing an angiosperm-wide survey in order to test for co-occurrence as evidence of the gynodioecy pathway.

Methods

Data from different sources were compiled to obtain (to our knowledge) the largest dataset on gynodioecy available, with 275 genera that include at least one gynodioecious species. This dataset was combined with a dioecy dataset from the literature, and a study was made of how often dioecious and gynodioecious species could be found in the same genera using a contingency table framework.

Key Results

It was found that, overall, angiosperm genera with both gynodioecious and dioecious species occur more frequently than expected, in agreement with the gynodioecy pathway. Importantly, this trend holds when studying different classes separately (or sub-classes, orders and families), suggesting that the gynodioecy pathway is not restricted to a few taxa but may instead be widespread in angiosperms.

Conclusions

This work complements that previously carried out on the monoecy pathway and suggests that gynodioecy is also a common pathway in angiosperms. The results also identify angiosperm families where some (or all) dioecious species may have evolved from gynodioecious precursors. These families could be the targets of future small-scale studies on transitions to dioecy taking phylogeny explicitly into account.     

Plasticity and diversity of the phenology of dioecious Ficus species in Taiwan

While Ficus present a series of traits often associated with dioecy, the prevalence of dioecy in Ficus is atypical. In Asian floras, dioecious Ficus species generally outnumber monoecious ones. Further this is also true in relatively northerly locations for Ficus such as the island of Taiwan. Ficus are pollinated by species-specific wasps that use fig flowers as breeding sites. In dioecious fig species, pollinators develop only in the inflorescences of male fig trees. In this study, we investigated the reproductive phenology of four dioecious Ficus species with distinct ecologies in several locations in northern and southern Taiwan. The two first species (Ficus erecta and Ficus septica) were investigated in four locations. Reproductive phenology was quite different among sites, even within a single species. For example, F. erecta presented well-defined crops at the population level in its usual high-elevation habitat but continuous fig production at low elevations, especially in South Taiwan. The two other fig species (Ficus pedunculosa var. mearnsii and Ficus tinctoria subsp. swinhoei), are shrubs growing together along seashores in exposed locations on coral reef remnants. These two species presented quite different traits allowing the survival of pollinating wasp populations. Ficus pedunculosa var. mearnsii produced figs continuously so that fresh receptive figs were always available for the pollinating wasps while F. tinctoria subsp. swinhoei extended the period of receptivity of its figs, so that receptive figs that had been waiting for pollinating wasps were almost always available. In summary, dioecious figs in Taiwan showed remarkable variation in their phenology, within species among locations or among species within location. Nevertheless, despite this variation, the phenology of the trees always allowed survival of pollinating wasp populations. Dioecious figs seem to have adopted a differentiated set of strategies which result in high resilience of pollinator populations. This resilience could help explain the atypical prevalence of dioecy in Ficus.     

Sexual systems and population genetic structure in an annual plant: testing the metapopulation model

The need for reproductive assurance during dispersal, along with the pressure of local mate competition, means that the importance of frequent or repeated colonization is implicit in the literature on sexual system evolution. However, there have been few empirical tests of the association between colonization history and sexual system in plants, and none within a single species. Here we use patterns of genetic diversity to provide such a test in the Mercurialis annua species complex, which spans the range of systems from self-compatible monoecy through androdioecy to dioecy. This variation has been hypothesized to result from differing patterns of metapopulation turnover and recolonization. Because monoecy should be favored during colonization, androdioecy and dioecy will be maintained only in regions with low rates of local extinction and recolonization, and these differences should also be reflected in patterns of neutral genetic diversity. We show that monoecious populations of M. annua display lower within-population genetic diversity than androdioecious populations and higher genetic differentiation than dioecious and androdioecious populations, as predicted by metapopulation models. In contrast, regional diversity in M. annua appears to be primarily a product of postglacial range expansion from two refugia in the eastern and western Mediterranean Basin.     

Multiple nuclear gene phylogenetic analysis of the evolution of dioecy and sex chromosomes in the genus Silene

In the plant genus Silene, separate sexes and sex chromosomes are believed to have evolved twice. Silene species that are wholly or largely hermaphroditic are assumed to represent the ancestral state from which dioecy evolved. This assumption is important for choice of outgroup species for inferring the genetic and chromosomal changes involved in the evolution of dioecy, but is mainly based on data from a single locus (ITS). To establish the order of events more clearly, and inform outgroup choice, we therefore carried out (i) multi-nuclear-gene phylogenetic analyses of 14 Silene species (including 7 hermaphrodite or gynodioecious species), representing species from both Silene clades with dioecious members, plus a more distantly related outgroup, and (ii) a BayesTraits character analysis of the evolution of dioecy. We confirm two origins of dioecy within this genus in agreement with recent work on comparing sex chromosomes from both clades with dioecious species. We conclude that sex chromosomes evolved after the origin of Silene and within a clade that includes only S. latifolia and its closest relatives. We estimate that sex chromosomes emerged soon after the split with the ancestor of S. viscosa, the probable closest non-dioecious S. latifolia relative among the species included in our study.     

The functional implications of active and passive pollination in dioecious figs

Fig-pollinating wasps lay their eggs in fig flowers. Some species of fig-pollinating wasps are active pollinators, while others passively transfer pollen. In dioecious fig species, the ovules of male figs produce wasps but no seeds. By observations and experiments on four dioecious Ficus species we show that (i) passive pollinators distribute pollen haphazardly within figs, but fertilization of female flowers in male figs is inhibited. Consequently, wasp larvae will develop in nonfertilized ovules: they cannot benefit from pollination; (ii) active pollinators efficiently fertilize flowers in which they oviposit. Lack of pollination increases larval mortality. Hence, fig pollinators are not obligate seed eaters but ovule gallers. Active pollination has probably evolved as a way to improve progeny nourishment.
Comparison of pollination and oviposition process in male and female figs, suggests that stigma shape and function have coevolved with pollination behaviour, in relation to constraints linked with dioecy.     

Preference of an insular flying fox for seed figs enhances seed dispersal of a dioecious species

Interactions among multiple species form complex networks of interdependences and are considered primary factors in the generation and maintenance of biodiversity. Pteropodid bats are keystone species that provide important ecosystem services of pollination and seed dispersal in the tropics and subtropics. In this study, we investigated the utilization and preference of food resources by the insular frugivorous flying fox Pteropus dasymallus. We found that fig species constituted the major portion of the diet of the flying fox (94.6%). When foraging, the flying fox preferred seed figs from female trees over gall figs from male trees in functionally dioecious fig species. Germination experiments showed a significantly higher percentage of germination for fig seeds in feces than those from pellets and ripe figs (feces: 80.2%, pellets: 23.4%, ripe figs: 32.9%). Considering the active selection of seed figs and avoidance of gall figs by foraging flying foxes, we suggest that the abundance of seed figs accurately represents food availability for dioecy. This preference for seed figs or viable seeds can effectively promote the survival of pollinating wasps and might reinforce the evolution of dioecism in figs. In addition, the effects of gut passage on seed germination, in combination with the capacity of flying foxes to travel long distances, may substantially contribute to the efficiency of flying foxes as seed dispersers.     

A three-genome phylogeny of Momordica (Cucurbitaceae) suggests seven returns from dioecy to monoecy and recent long-distance dispersal to Asia

The bitter gourd genus Momordica comprises 47 species in Africa and 12 in Asia and Australia. All have unisexual flowers, and of the African species, 24 are dioecious, 23 monoecious, while all Asian species are dioecious. Maximum likelihood analyses of 6257 aligned nucleotides of plastid, mitochondrial and nuclear DNA obtained for 122 accessions of Momordica and seven outgroups show that Momordica is monophyletic and consists of 11 well-supported clades. Monoecy evolved from dioecy seven times independently, always in Africa and mostly in savanna species with low population densities. Leaky dioecy, with occasional fruit-producing males, occurs in two African species and might be the first step in an evolutionary transition towards monoecy. Dated biogeographic analyses suggest that Momordica originated in tropical Africa and that the Asian species are the result of one long-distance dispersal event about 19 million years ago. The pantropical vegetable Momordica charantia is of African, not Asian origin as had previously been suggested.     

Pollen morphology and functional dioecy inSolanum (Solanaceae)

Dioecy has evolved independently several times in the large, mostly tropical genusSolanum. In all cases of dioecy inSolanum functionally male flowers have normal anthers, normal pollen and reduced stigmas while functionally female flowers have stigmas and anthers that appear normal but contain non-functional, usually inaperturate pollen. The inaperturate pollen has living cytoplasm, but apparently never germinates and it has been hypothesised that the pollen in these functionally female flowers is retained as a pollinator reward. Pollen morphology is compared in twelve of the thirteen known dioecious species ofSolanum, and some stages in the the development of inaperturate pollen in the anthers of functionally female flowers ofSolanum confertiseriatum of Western Ecuador are examined. Observations on the development and morphology of inaperturate pollen in functionally female flowers ofSolanum are related to hypotheses about the evolution of dioecy in the genus.     

THE STABILITY OF THE SYMBIOSIS BETWEEN DIOECIOUS FIGS AND THEIR POLLINATORS: A STUDY OF FICUS CARICA L. AND BLASTOPHAGA PSENES L.

Each Ficus species depends on a specific mutualistic wasp for pollination. The wasp breeds on the fig, each larva destroying a female flower. It is, however, not known why the wasps have not evolved the ability to use all female flowers. In “dioecious” figs, the wasp can only breed in the female flowers of the “male” trees, so that pollination of a female tree is always lethal. The wasps should therefore be selected to avoid female trees. Field data is presented showing that the fruiting phenology of the dioecious fig Ficus carica is such that this selection does not occur: syconia are not receptive at the same time on “male” and female trees. Most wasps are forced to emerge from the syconia of “male” trees at a time when they will not be able to reproduce, whether they avoid female trees or not. This aspect of the life cycle of the wasp, although noticed, has been obscured in most previous studies. It is shown that the fruiting phenology of Ficus carica, which stabilizes the symbiosis, is the result of short-term selective pressures on the male function of the trees. Such selective pressures suggest a possible pathway from monoecy to dioecy in Ficus under seasonal climates.