Sexual dimorphism in the andromonoecious Euphorbia nicaeensis: effects of gender and inflorescence development

BACKGROUND AND AIMS: In andromonoecious taxa with separate floral types along the inflorescence, architectural or plastic effects can simulate floral sexual dimorphism. Both the primary and secondary sexual characteristics of the cyathia of the protogynous andromonoecious species Euphorbia nicaeensis were analysed according to their sex and arrangement on the inflorescence. METHODS: The production of male and hermaphrodite cyathia at each inflorescence level was surveyed in two natural populations. The longevity, size, pollen production and viability, and nectar secretion of both types of cyathia were checked between inflorescence levels and between sexes at the only level at which they occur together. This sampling method makes it possible to know whether differences between cyathia types are based on sex or are attributable to inflorescence development. KEY RESULTS: Male cyathia were produced predominantly at the first and second inflorescence levels, whereas at levels 3-5, the cyathia were almost exclusively hermaphrodite. Viable pollen production by male cyathia at the second inflorescence level was higher than that of hermaphrodite cyathia at the third level but, when males and hermaphrodites at the same level were compared, their pollen production was similar. Male and hermaphrodite cyathia were similar in size, irrespective of the inflorescence level, although the exclusively hermaphrodite cyathia of the last level were smaller. Both cyathium types produced similar amounts of sugar. However, male cyathia produced nectar during their whole lifespans, whereas hermaphrodites produced it exclusively during their male phase. Moreover, the nectary activity of male cyathia started earlier in the day than that of hermaphrodites. CONCLUSIONS: An apparent floral dimorphism exists in the primary sexual characteristics of Euphorbia nicaeensis because differences in pollen production between cyathium types are due to theirs positions. Similarly, differences affecting most secondary sexual characteristics are only apparent between the two cyathium types. However, E. nicaeensis shows a true but slight floral dimorphism in some of the secondary sex characters related to nectar secretion. The lack of nectar production by the female phase of the hermaphrodite cyathia of E. nicaeensis indicates that this is a deceit-pollinated species.     

Functional andromonoecy in Euphorbia (Euphorbiaceae)

The occurrence of cyathia containing staminate flowers but lacking a pistillate flower was studied in 17 species of Euphorbia. Male cyathia were found in the majority of species studied (88.2%) giving functional andromonoecy. In the male cyathia, the pistillate flower is generally totally absent, but sometimes a vestigial pistillate flower with a non-functional ovary is present. The proportion of male cyathia varied at both the population and species level. The position of male cyathia within the inflorescence showed a constant pattern among species: the proportion of male cyathia decreased from the first to the last levels of the pleiochasia. In general, perennial species had significantly higher proportions of male cyathia than annual species (mean 20 and 2.3%, respectively). In annual species there was a trend for production of male cyathia only in the first level of the inflorescence, whereas in perennials production up to the fourth level of the inflorescence was usual. Functional andromonoecy is common in Euphorbia and represents a new sex segregation in the genus. The selective forces causing this secondary sex segregation in Euphorbia, such as improved pollination or increased outcrossing, are discussed.     

SEXUAL ALLOCATION AND ANDROMONOECY: RESOURCE INVESTMENT IN MALE AND HERMAPHRODITE FLOWERS OF SOLANUM CAROLINENSE (SOLANACEAE)

Male and hermaphrodite flowers from the andromonoecious perennial Solanum carolinense were compared. Hermaphrodite flowers were 11–16% heavier than males, and this difference was consistent for two clones studied. Hermaphrodite flowers contained a greater amount of nitrogen than did male flowers, but males had higher percent nitrogen. Male and hermaphrodite flowers had equal investment in male structures: stamen mass, number of pollen grains, mass of pollen grains ejected by vibration, and pollen size were all similar for the two flower types. In contrast, male flowers had reduced masses of disfunctional female structures: ovaries of males were ⅓ as massive, and styles 1/7; as massive, as those of hermaphrodites. These results are consistent with the hypothesis that male flowers (which occur where fruit set is unlikely) increase male fitness through pollen donation, while saving resources that would otherwise be invested in hermaphrodite flowers that abscise.     

Males outcompete hermaphrodites for seed siring success in controlled crosses in the polygamous Fraxinus excelsior (Oleaceae)

Polygamy (including trioecy and subdioecy), the co-occurrence of males, hermaphrodites, and females in natural populations, is a rare and poorly studied breeding system expressed in Fraxinus excelsior L. (Oleaceae), a wind-pollinated tree. Here we investigate siring ability of pollen from male vs. hermaphrodite individuals to better understand this sex polymorphism. We conducted single-donor and two-donor pollination experiments and compared both fruit set and seed siring success, assessed with polymorphic microsatellite markers, of male and hermaphrodite individuals. Single pollen donor crosses allowed us to verify the male function of hermaphrodites. However, pollen from hermaphrodites was much less proficient than male pollen, with males siring 10 times as many fruits in single donor pollination treatments. This result was strengthened by the surprisingly low reproductive success of hermaphrodites in pollen competition conditions: of the 110 seedlings analyzed three were selfed and only one was sired by the hermaphrodite donor. The remaining 106 were sired by the male pollen donor. These results raise the question of the maintenance of male fertility in hermaphrodites in Fraxinus excelsior. Male function of hermaphrodites in this species now needs to be assessed under field conditions.     

Andromonoecy in an Old World Papilionoid legume,Erophaca baetica

Andromonoecy (i.e. the occurrence on individual plants of hermaphroditic and male flowers) is a rare sexual system among the angiosperms, regarded by some authors as a transitional stage from hermaphroditism to monoecy. Having discovered the occurrence of andromonoecy in Erophaca baetica (a Mediterranean shrubby legume with two subspecies), a novelty for Old World papilionoid legumes, we investigated the morpho‐functional correlates and the geographical distribution of this phenomenon in the species. The relative frequencies of hermaphrodite and male flowers were determined in two field and 111 herbarium populations. Biomass allocation within flowers, pollen production and viability, pollen tube growth, nectar production and the temporal pattern of male flower production were also studied in two nearby southern Spanish populations. Virtually all of the studied populations were andromonoecious. Male flowers tended to appear at apical positions within the inflorescence, and became more abundant by the end of the flowering season. Male flowers were externally similar to hermaphroditic flowers (although with less biomass and smaller parts) and released equivalent amounts of pollen and nectar; however, their pollen germinated significantly better. Erophaca is the first example of an andromonecious Papilionoid in the Old World. Since the main difference among floral morphs in this species is functional (i.e. pollen germination rate) rather than morphological, andromonoecy is not readily noticeable, and very careful inspection may be required to reveal it. The potential effect of andromonoecy in enhancing outcrossing rate in this species is discussed.     

Pattern of Flower and Fruit Production in Stryphnodendron adstringens, an Andromonoecious Legume Tree of Central Brazil

Abstract: Patterns of flower and fruit production in racemes of Stryphnodendron adstringens, an andromonoecious Brazilian savanna tree species, were studied in two natural areas near Uberlândia-MG. Racemes were divided in three parts: apex, centre, and base. Number of flowers, gender, and nectar and pollen production were analyzed for each section. Frequency of visitors to each part of the inflorescence was also quantified. Hand self- and cross-pollinations were performed in complete racemes and fruit set used to determine breeding system. The racemes produced a mean of 329 flowers, more densely packed in the central portion. Hermaphrodite and male flowers occur along the inflorescence but hermaphrodite flowers are more common in the centre. Fruit set was markedly low but does not seem to be limited by pollination service, since free open-pollinated racemes and hand cross-pollinated ones do not differ in fruit production rates. Fruits resulted mostly from cross-pollinated flowers and fruit production was biased to the central portion of the raceme. Nectar yield was higher in the central portion of the raceme and visitors arrived more commonly on this portion of the inflorescence. However, most flowers did not produce nectar. The pattern of fruit production seems to be a consequence of the hermaphrodite flower distribution in the raceme and it is not constrained by pollen flow or flower opening sequence.     

Self-Incompatibility and Male Fertilization Success in Phillyrea angustifolia (Oleaceae)

Androdioecy is a rare breeding system in which low male frequency is expected in populations because males require a strong increase in their fertility to be maintained by selection. Phillyrea angustifolia L. has previously been reported as possibly functionally androdioecious. However, 1&rcolon;1 sex ratios have been reported and suggest functional dioecy. In this article, we compared both pollen tube growth and siring success of male and hermaphrodite pollen in two single-donor pollination experiments. We verified at both pre- and postzygotic levels that hermaphrodites produce functional pollen. Self-incompatibility was also clearly established. However, pollen from hermaphrodites was less efficient than male pollen. The probability of a pollen tube growing through the style was higher for male than for hermaphrodite pollen donors, and males sired twice as many fruits as hermaphrodites. The twofold male advantage in relative fecundity was mainly because of lower pollen fertility of hermaphrodites and possible cross-incompatibility among hermaphrodites.     

Pollination context alters female advantage in gynodioecious Silene vulgaris

Gynodioecy, the co‐occurrence of females and hermaphrodites, is arguably the most common angiosperm gender polymorphism in many florae. Females’ ability to invade and persist among hermaphrodites depends, in part, on pollinators providing adequate pollination to females. We directly measured diurnal and nocturnal pollinators’ contributions to female and hermaphrodite seed production in artificial populations of gynodioecious Silene vulgaris by experimentally restricting pollinator access. We found that female relative seed production in this system depended strongly on pollination context: females produced more than twice as many seeds as hermaphrodites in the context of abundant, nectar‐collecting moths. Conversely, females showed no seed production advantage in the context of pollen‐collecting syrphid flies and bees due to acutely hermaphrodite‐biased visitation. We infer that variation in pollinator type, behaviour and abundance may be important for achieving the female relative fitness thresholds necessary for the maintenance of gynodioecy. Generally, our study illustrates how pollinator‐mediated mechanisms may influence the evolution of breeding systems and associated suites of floral traits. Segments of a pollinator community may facilitate gynodioecy by selecting for plant characteristics that increase the attractiveness of both sexes to pollinators, such as nectar rewards. Conversely, discriminating visitors in search of pollen may restrict gynodioecy in associated plant lineages by reducing male steriles’ fitness below threshold levels.     

Nectar Sugar Production across Floral Phases in the Gynodioecious Protandrous Plant Geranium sylvaticum

Many zoophilous plants attract their pollinators by offering nectar as a reward. In gynodioecious plants (i.e. populations are composed of female and hermaphrodite individuals) nectar production has been repeatedly reported to be larger in hermaphrodite compared to female flowers even though nectar production across the different floral phases in dichogamous plants (i.e. plants with time separation of pollen dispersal and stigma receptivity) has rarely been examined. In this study, sugar production in nectar standing crop and secretion rate were investigated in Geranium sylvaticum, a gynodioecious plant species with protandry (i.e. with hermaphrodite flowers releasing their pollen before the stigma is receptive). We found that flowers from hermaphrodites produced more nectar than female flowers in terms of total nectar sugar content. In addition, differences in nectar production among floral phases were found in hermaphrodite flowers but not in female flowers. In hermaphrodite flowers, maximum sugar content coincided with pollen presentation and declined slightly towards the female phase, indicating nectar reabsorption, whereas in female flowers sugar content did not differ between the floral phases. These differences in floral reward are discussed in relation to visitation patterns by pollinators and seed production in this species.     

Sexually dimorphic inflorescence traits in a wind-pollinated species: heritabilities and genetic correlations in Schiedea adamantis (Caryophyllaceae)

Sexual dimorphism may be especially pronounced in wind-pollinated species because they lack the constraints of biotically pollinated species that must present their pollen and stigmas in similar positions to ensure pollen transfer. Lacking these constraints, the sexes of wind-pollinated species may diverge in response to the different demands of pollen dispersal and receipt, depending on the magnitude of genetic correlations preventing divergence between sexes. Patterns of sexual dimorphism and genetic variation were investigated for inflorescence traits in Schiedea adamantis (Caryophyllaceae), a species well adapted to wind-pollination, and compared to S. salicaria, a species with fewer adaptations to wind pollination. For S. adamantis, dimorphism was pronounced for inflorescence condensation and its components, including lateral flower number and pedicel length. Within sexes, genetic correlations between traits may constrain the relative shape of the inflorescence. Correlations detected across sexes may retard the evolution of sexual dimorphism in inflorescence structure, including features favoring enhanced dispersal and receipt of pollen. Despite genetic correlations across sexes, common principal components analysis showed that genetic variance-covariance matrices (G matrices) differed significantly between the sexes, in part because of greater genetic variation for flower number in hermaphrodites than in females. G matrices also differed between closely related S. adamantis and S. salicaria, indicating the potential for divergent evolution of inflorescence structure despite general similarities in morphology and pollination biology.     

Do inbreeding depression and relative male fitness explain the maintenance of androdioecy in white mangrove, Laguncularia racemosa (Combretaceae)?

Mathematical models predict that to maintain androdioecious populations, males must have at least twice the fitness of male function in hermaphrodites. To understand how androdioecy is maintained in Laguncularia racemosa (white mangrove), outcrossing, inbreeding depression, and relative male fitness were estimated in two androdioecious populations and one hermaphroditic population. Outcrossing was estimated based on length of pollinator foraging bout and pollen carryover assumptions. Inbreeding depression was measured at three life stages: fruit set, seedling emergence, and seedling survivorship. The relative fitnesses of males and the male component of hermaphrodites were compared at these three stages and at the pollen production stage. Male frequency predictions generated by Lloyd's model were compared with observed frequencies in two androdioecious subpopulations. Outcrossing estimates were moderate for all populations (0.29-0.66). Inbreeding depression varied among populations (-0.03-0.86), but the strength of inbreeding depression did not increase with male frequency. Males produced significantly more flowers/inflorescence than hermaphrodites, but pollen production/flower did not differ. Male and hermaphroditic progeny did not differ significantly at other life stages. Populations of white mangrove with male plants were functionally androdioecious. Lloyd's model accurately predicted male frequency in one androdioecious subpopulation, but underestimated male frequency in the second subpopulation.     

Gynodioecy in Cirsium chikushiense Koidz. (Compositae)

A study of the morphology and function of flowers in Cirsiumchikushiense revealed that the species was distinctly gynodioecious.Self-incompatible hermaphrodite florets produced both seedsand pollen grains, while female ones produced seeds but no pollengrains at all. The degenerated stamens of females were not onlysmaller but also sometimes occurred at a lower position insidethe floral tube than in hermaphrodites. The stigmata of femalesoften developed more fully than those of hermaphrodites. Thefrequencies of female plants in natural populations varied from15·5 to 50%. Almost all the pollinators stayed on bothfemale and hermaphrodite heads only to collect nectar. The femaleplants of this species may be more specialized in their genderby saving the cost of not only pollen grains but also stamens,and may be maintained by sufficient pollinators in natural populations.This gynodioecy may provide an example of nuclear-cytoplasmicmale sterility.Copyright 1994, 1999 Academic Press Sex expression, gynodioecy, Cirsium chikushiense, Compositae, male sterility, degenerated stamen, female frequency     

Dissecting the causes of variation in intra-inflorescence allocation in a sexually polymorphic species, Fragaria virginiana (Rosaceae)

In this study we dissect the causes of variation in intra-inflorescence allocation in a sexually polymorphic species, Fragaria virginiana. We separated out the effects of resource competition during flowering from those of inflorescence architecture, as well as identified the effects of sex morph and genotype. We found position-based variation in petal length, ovule, pollen, and flower number to be influenced more by architecture than by our resource manipulations during flowering. We also found both genotype- and sex-specific intra-inflorescence patterns. Furthermore, our data indicate that the sex morph-specific intra-inflorescence patterns result from architectural modifications of the basic pattern. In fact, sex-differential intra-inflorescence patterns suggest that fitness through male and female function may be maximized by different resource distribution patterns within the inflorescence and may have been modified by past selection. Specifically, females invested heavily in ovules at positions where fruit set was most likely (primary and secondary), at the expense of flower number and allocation per flower at more distal positions. Whereas functional males invested minimally in ovules at all flower positions and produced the most abundantly flowered inflorescences, hermaphrodites, on the other hand, showed intermediate patterns, implying a compromise between sex functions. We suggest that consideration of intra-inflorescence allocation and inflorescence architecture may reveal the mechanism underlying sexual dimorphism in flower allocation and number.     

Nutrient sensitivity of the cost of male function in gynodioecious Phacelia linearis (Hydrophyllaceae)

Allocation trade-offs should be measured as opportunity costs, estimating what individuals sacrifice in one function by allocating to others. We investigated opportunity costs of male function in gynodioecious Phacelia linearis, asking whether nutrient limitation contributes to them. This hypothesis predicts that hermaphrodites experience greater nutrient stress than females, and that hermaphrodite disadvantages in production might decrease with nutrient supply. We cultivated hermaphrodites and females at two nutrient levels, scoring individuals for prereproductive leaf number at 5 wk, and biomass, nitrogen concentration, and fruit and seed production at 16 wk. Nutrient treatments caused final growth differences of two orders of magnitude. No gender difference appeared at 5 wk, but at 16 wk hermaphrodites produced less stem, leaf, and inflorescence biomass than females, and made fewer fruits. Hermaphrodites' shoot-size disadvantage was marginally significantly more severe at low nutrients than high nutrients. Significant gender x nutrient interactions for root fraction and whole-plant nitrogen concentration indicate greater nutrient stress in hermaphrodites than females. Hermaphrodites also acquired less total nitrogen than females. Nutrient limitation contributes to opportunity costs of male function, but there must be other contributors. Possibilities include limitations in other resources, gender effects on morphology, and genetic trade-offs not directly involving allocation or morphology.     

Male flowers in Tulipa pumila Moench (Liliaceae) potentially originate from gender diphasy

We found functionally male individuals in an otherwise hermaphroditic population of Tulipa pumila (Liliaceae) located in Tuscany (central Italy). We investigated the sex ratio of this population, followed by morphometric analyses of the scape, leaves and flowers, and tests on pollen germinability and seed number and mass, in order to infer which sexual strategy produced the observed co-occurrence of male and hermaphrodite individuals. We found that sex ratio deviated from 1:1, and functionally male individuals showed a smaller plant size and a reduced pollen fitness (germinability and siring ability) compared to hermaphrodites. These findings point to a resource-dependent sexual allocation strategy, probably associated with gender diphasy.     

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.     

Understanding the basis of pollinator selectivity in sexually dimorphic Fragaria virginiana

Pollinators of gender dimorphic (e.g., gynodioecious or dioecious) species often show a preference for hermaphrodite or male flowers over conspecific females, and such pollinator selectivity can have implications for the evolution of sexual dimorphism. However, because the sex morphs differ in several floral features, it is not readily apparent which specific traits generate differential pollinator service. In this study, we sought to understand the basis of pollinator preferences for hermaphrodites to females of gynodioecious Fragaria virginiana . We extend a previous study that revealed that lack of pollen-filled anthers and shorter petals were not solely responsible for small bee and fly discrimination against females, by investigating the roles of other morphological features, reward characters, and floral context in bringing about pollinator discrimination. Using floral manipulations we revealed that small bees preferentially visit flowers with wide petals, more nectar, intact stamens, as well as flowers located in hermaphrodite-dominated patches. Specifically, bees were able to remotely detect nectar presence. In addition, bees were attracted to both the anther sac and the filament regions of the stamen, indicating that not only anthers, but also filaments may function as visual or olfactory cues to pollen reward. Furthermore, pollinator preference for flowers in hermaphrodite-dominated patches serves to intensify their discrimination against female flowers which occur predominantly in female-dominated patches. For the most part, preferences of flies mirrored those of the bees with the exception that flies also showed a significant preference for flowers held high over those held closer to the ground. These results indicate that a suite of character differences contributes to pollinators' preferences for hermaphrodite to female flowers. Furthermore, they suggest pollinators could mediate selection on both floral morphology and reward in this species.     

Variation in reproductive success and gonadal allocation in the simultaneous hermaphrodite,Serranus fasciatus

Summary This paper examines the correlates of individual size, reproductive success, gonadal allocation, and growth in a hermaphroditic reef fish. Individuals in S. fasciatus mature as simultaneous hermaphrodites; large individuals subsequently lose female function and become functional males. Daily female reproductive success was highly correlated with both hermaphrodite size and amount of female gonadal tissue. Three separate comparisons gave a positive correlation between male reproductive success and male gonadal allocation: (1) Males had higher levels of male gonadal allocation and male reproductive success than hermaphrodites. (2) The percent of gonad allocated to male tissue in hermaphrodites was higher in the year they had higher male mating success. (3) Male gonadal tissue of hermaphrodites was positively correlated with male reproductive success in the year that male reproductive success by hermaphrodites was higher and more variable. There was no evidence for a trade-off between male function, female function, and growth among hermaphrodites. Many of these patterns have also been observed in plants, but the selective pressures leading to these patterns in S. fasciatus and plants are probably quite different.     

PATTERNS OF PRE- AND POSTFERTILIZATION RESOURCE ALLOCATION WITHIN AN INFLORESCENCE: EVIDENCE FOR INTEROVARY COMPETITION

I investigated the distribution of ovules and seeds on the inflorescence of Solanum Carolinense L. (Solanaceae). Ovules did not appear to vary in size, but the number of ovules per ovary and the size of ovaries decreased significantly along the inflorescence (from basal to distal positions). Experimental removal of basal ovaries at an early stage resulted in increased ovary size and number of ovules in distal ovaries, suggesting a dynamic system of control. Mature fruits displayed a similar pattern of decreasing mass and seed number with position along the infructescence. It is not clear whether the patterns of allocation to fruits are related to the patterns of allocation to ovaries in a simple cause-and-effect relationship. However, a satisfying hypothesis that explains these and other patterns of allocation is that they are all manifestations of, or adaptations to, interovary competition along the inflorescence.     

Sex determination in the androdioecious barnacle Scalpellum scalpellum (Crustacea: Cirripedia)

How androdioecy (coexistence of hermaphrodites and males) is maintained is still poorly understood. Therefore, sex determination was studied in the androdioecious barnacle Scalpellum scalpellum L. First, 247 cypris larvae from seven broods were investigated for sexual dimorphism in larval morphology and found to be all identical. Second, experiments with cyprids showed that males and hermaphrodites differ distinctly in morphology as soon as 4–5 days after settlement. Third, 14 252 cyprids were allowed to settle on the bottom of their culture cages, and all surviving larvae developed into hermaphrodites and none into dwarf males. Fourth, larvae settled in hermaphrodite receptacles (i.e. future males) were removed at increasing intervals after settlement to study if the male and hermaphrodite sexual expressions are fixed or plastic. All larvae became dwarf males if allowed to stay there for more than 8 h after settlement. But if removed within 3 h after settlement, half of them developed into hermaphrodites. We conclude that an environmental sex determination mechanism operates in S. scalpellum. Together with a 1:1 hermaphrodite/male ratio observed in previously reported experiments offering a free choice of settlement, we suggest that all larvae are potential hermaphrodites, but only 50% can settle in hermaphrodite receptacles and yield males.