Ecological context of breeding system variation: sex, size and pollination in a (predominantly) gynodioecious shrub

BACKGROUND AND AIMS: Species that exhibit among-population variation in breeding system are particularly suitable to study the importance of the ecological context for the stability and evolution of gender polymorphism. Geographical variation in breeding system and sex ratio of Daphne laureola (Thymelaeaceae) was examined and their association with environmental conditions, plant and floral display sizes, and pollination environment in a broad geographic scale was analysed. METHODS: The proportion of female and hermaphrodite individuals in 38 populations within the Iberian Peninsula was scored. Average local temperature and precipitation from these sites were obtained from interpolation models based on 30 years of data. Pollination success was estimated as stigmatic pollen loads, pollen tubes per ovule and the proportion of unfertilized flowers per individual in a sub-set of hermaphroditic and gynodioecious populations. KEY RESULTS: Daphne laureola is predominantly gynodioecious, but hermaphroditic populations were found in northeastern and southwestern regions, characterized by higher temperatures and lower annual precipitation. In the gynodioecious populations, female plants were larger and bore more flowers than hermaphrodites. However, due to their lower pollination success, females did not consistently produce more seeds than hermaphrodites, which tends to negate a seed production advantage in D. laureola females. In the northeastern hermaphroditic populations, plants were smaller and produced 9-13 times fewer flowers than in the other Iberian regions, and thus presumably had a lower level of geitonogamous self-fertilization. However, in a few southern populations hermaphroditism was not associated with small plant size and low flower production. CONCLUSIONS: The findings highlight that different mechanisms, including abiotic conditions and pollinator service, may account for breeding system variation within a species' distribution range and also suggest that geitonogamy may affect plant breeding system evolution.     

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.     

The functional ecology of gynodioecy in Eritrichum aretioides (Boraginaceae), the alpine forget-me-not

Eritrichum aretioides is a gynodioecious species with female and hermaphrodite individuals. In populations on Pennsylvania Mountain in central Colorado (USA), the frequency of females ranges from 22 to 41%. Flower number and the number of seeds produced per flower were similar in hermaphrodites and females. However, hermaphrodites produced larger flowers, while females produced larger seeds (P < 0.05 for both). In the field, seed germination was higher for seeds from females than for seeds from hermaphrodites (20 vs. 9% germination; P < 0.05). Unvisited flowers and open-pollinated flowers of hermaphrodites had similar pollen receipt (approx 20 pollen grains per stigma), but seed set following autogamous pollination was significantly lower than seed set following natural pollination. This finding indicates that hermaphrodites have a barrier to selfing and implies that the larger seed size and greater establishment advantage of offspring from females is unlikely to have resulted from female outcrossing advantage. Rather, differences in the quality of seed progeny between morphs probably reflect a trade-off in sexual allocation or pleiotropic effects of the sex-determining genes.     

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.     

Female reproductive success in gynodioecious Thymus vulgaris: pollen versus nutrient limitation and pollinator foraging behaviour

Gynodioecy is a dimorphic breeding system in which female individuals coexist with hermaphroditic individuals in the same population. Females only contribute to the next generation via ovules, and many studies have shown that they are usually less attractive than hermaphrodites to pollinators. Several mechanisms have been proposed to explain how females manage to persist in populations despite these disadvantages. The ‘resource reallocation hypothesis’ (RRH) states that females channel resources not invested in pollen production and floral advertisement towards the production of more and/or larger seeds. We investigated pollination patterns and tested the RRH in a population of Thymus vulgaris. We measured flower display, flower size, nectar production, visitation rates, pollinator constancy and flower lifespan in the two morphs. In addition, we measured experimentally the effects of pollen and resource addition on female reproductive success (fruit set, seed set, seed weight) of the two morphs. Despite lower investment in floral advertisement, female individuals were no less attractive to pollinators than hermaphrodites on a per flower basis. Other measures of pollinator behaviour (number of flowers visited per plant, morph preference and morph constancy) also showed that pollinators did not discriminate against female flowers. In addition, stigma receptivity was longer in female flowers. Accordingly, and contrary to most studies on gynodioecious species, reproductive success of females was not pollen limited. Instead, seed production was pollen limited in hermaphrodites, suggesting low levels of cross‐pollination in hermaphrodites. Seed production was resource limited in hermaphrodites, but not in females, thus providing support for the RRH. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 175 , 395–408.     

Dry environments promote the establishment of females in monomorphic populations of <Emphasis Type="Italic">Wurmbea biglandulosa</Emphasis> (Colchicaceae)

In flowering plants, the evolution of dimorphic breeding systems from monomorphic ancestors can be associated with dry environments. One hypothesis to explain this pattern is that seed fertility of hermaphrodites decreases more than seed fertility of females under dry conditions, so that females have greater relative fitness. This could occur if seed production of hermaphrodites is more resource-limited than that of females, or shifts in pollination increase levels of selfing and inbreeding depression in hermaphrodites. Here we assess the role of dry environments in promoting a female fitness advantage in Wurmbea biglandulosa by focusing on monomorphic and dimorphic populations that occur along a longitudinal gradient of decreasing rainfall. Dimorphic populations occurred in sites with higher temperatures, lower rainfall and lower soil moisture. Overall, females had greater seed fertility than did hermaphrodites from monomorphic populations, which in turn had greater seed fertility than hermaphrodites from dimorphic populations. Ovuliferous flower and ovule production by the three gender morphs and seed fertility of females and hermaphrodites in monomorphic populations did not vary with soil moisture. By contrast, seed fertility of hermaphrodites in dimorphic populations was positively related to soil moisture. Accordingly, female frequency was higher in those sites where hermaphrodites produced relatively fewer seeds. Taken together our results indicate that dry environments promote the establishment of females by decreasing the relative seed fitness of hermaphrodites. Moreover, because seed fertility of hermaphrodites in monomorphic populations did not vary with soil moisture, resource limitation of female function may play only a minor role in the establishment of females. Other factors such as shifts in pollination and mating patterns of hermaphrodites could be involved. Key words:breeding system evolution, environmental stress, gender dimorphism, gynodioecy, sex ratio variationCo-ordinating editor: J.F. Stuefer     

Selective nectar robbing in a gynodioecious plant (Glechoma longituba) enhances female advantage

Nectar robbing not only affects the reproductive fitness of the plant but it may also potentially affect the pollination dynamics of the associated coflowering individuals. In this study, we established that the nectar robber Xylocopa sinensis robs nectar only from the hermaphrodite ramets of the gynodioecious plant Glechoma longituba but not from the female ramets. In populations with high rates of nectar robbing, this results in hermaphrodite ramets having reduced seed set whereas the female ramets have a slightly increased seed set. We hypothesize that selective nectar robbing confers an advantage to female individuals and thus ensures their maintenance in gynodioecious populations. Results of controlled experiments indicated that the reduction in the amounts of nectar available occasioned by nectar robbing resulted in some legitimate pollinators switching to visiting flowers on female rather than hermaphrodite ramets. This resulted in lower pollination rates and seed set for hermaphrodites and higher pollination rates and seed set for females. This study presents a previously unreported mechanism causing female advantage in gynodioecious plants.     

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.     

The role of pollination level on the reproduction of females and hermaphrodites in the gynodioecious plant Gypsophila repens (Caryophyllaceae)

In gynodioecious plant species, females are expected to have more resources available for maturing seeds because pistillate flowers are smaller, do not produce pollen, and are thus less costly that perfect flowers. The potential female advantage arising from more abundant resources is, however, likely to vary depending on whether seed production is limited by resource or pollen availability. Here we experimentally investigated the influence of pollen and resource limitation on female advantage in a gynodioecious species using two levels of pollination. Total seed production of females was always greater than that of hermaphrodites: females produced more flowers and more fruits that contained similar numbers of seeds of similar mass. Under low pollination, female and hermaphrodite plants allocated resources to increased flower production rather than to increased seed size or quality. We did not detect any influence of pollen or resource limitation on female advantage, which remained similar under low (= abundant resources) and full pollination. Outcrossed fruits performed better than selfed fruits when the same plant received both selfed and outcrossed pollen on different flowers. These differences were not greater under high pollination, possibly because resources available for each fruit did not differ between our pollen intensity treatments.     

Consequences of inbreeding for offspring fitness and gender in Silene vulgaris,a gynodioecious plant

Abstract In gynodioecious plants, hermaphrodite and female plants co‐occur in the same population. In these systems gender typically depends on whether a maternally inherited cytoplasmic male sterility factor (CMS) is counteracted by nuclear restorer alleles. These restorer alleles are often genetically dominant. Although plants of the female morph are obligatorily outcrossing, hermaphrodites may self. This selfing increases homozygosity and may thus have two effects: (1) it may decrease fitness (i.e. result in inbreeding depression) and (ii) it may increase homozygosity of the nuclear restorer alleles and therefore increase the production of females. This, in turn, enhances outcrossing in the following generation. In order to test the latter hypothesis, experimental crosses were conducted using individuals derived from four natural populations of Silene vulgaris, a gynodioecious plant. Treatments included self‐fertilization of hermaphrodites, outcrossing of hermaphrodites and females using pollen derived from the same source population as the pollen recipients, and outcrossing hermaphrodites and females using pollen derived from different source populations. Offspring were scored for seed germination, survivorship to flowering and gender. The products of self‐fertilization had reduced survivorship at both life stages when compared with the offspring of outcrossed hermaphrodites or females. In one population the fitness of offspring produced by within‐population outcrossing of females was significantly less than the fitness of offspring produced by crossing females with hermaphrodites from other populations. Self‐fertilization of hermaphrodites produced a smaller proportion of hermaphroditic offspring than did outcrossing hermaphrodites. Outcrossing females within populations produced a smaller proportion of hermaphrodite offspring than did crossing females with hermaphrodites from other populations. These results are consistent with a cytonuclear system of sex determination with dominant nuclear restorers, and are discussed with regard to how the mating system and the genetics of sex determination interact to influence the evolution of inbreeding depression.     

An experimental test of the effects of resources and sex ratio on maternal fitness and phenotypic selection in gynodioecious Fragaria virginiana

Resources, sex ratio, and seed production by hermaphrodites covary among natural populations of many gynodioecious plant species, such that they are functionally "more dioecious" as resources become more limiting. Strong correlations among these three factors confound our understanding of their relative roles in maintaining polymorphic sexual systems. We manipulated resource availability and sex ratio and measured their effects on relative fertility and phenotypic selection through the maternal fitness of females and hermaphrodites of Fragaria virginiana. Two results were particularly surprising. First, hermaphrodites showed little variability in fecundity across resource treatments and showed strong positive and context-dependent selection for fruit set. This suggests that variation in hermaphrodite seed production along resource gradients in nature may result from adaptation rather than plasticity. Second, although females increased their fecundity with higher resources, their fertility was unaffected by sex ratio, which is predicted to mediate pollen limitation of females in natural populations where they are common. Selection on petal size of females was also weak, indicating a minimal effect of pollinator attraction on variation in the fertility of female plants. Hence, we found no mechanistic explanation for the complete absence of high-resource high female populations in nature. Despite strong selection for increased fruit set of hermaphrodites, both the strength of selection and its contribution to the maintenance of gynodioecy are severely reduced under conditions where females have high relative fecundity (i.e., low resources and high-female sex ratios). High relative fertility plus high female frequency means that the evolution of phenotypic traits in hermaphrodites (i.e., response to selection via seed function) should be manifested through females because most hermaphrodites will have female mothers. Fruit set was never under strong selection in females; hence, selection to increase fruit set hermaphrodites will be less effective in maintaining their fruiting ability in natural populations with low resources and high female frequency. In sum, both sex ratio and resource availability influence trait evolution indirectly-through their effects on relative fertility of the sexes and patterns of selection. Sex ratio did not impose strong pollen limitation on females but did directly moderate the outcome of natural selection by biasing the maternal sex of the next generation. This direct effect of sex ratio on the manifestation of natural selection is expected to have far greater impact on the evolution of traits, such as seed-producing ability in hermaphrodites and the maintenance of sexual polymorphisms in nature, compared to indirect effects of sex ratio on relative fertility of the sexes.     

POPULATION SEX STRUCTURE AND REPRODUCTIVE FITNESS IN GYNODIOECIOUS SIDALCEA MALVIFLORA MALVIFLORA (MALVACEAE)

The spatial distribution of females and hermaphrodites within gynodioecious populations is expected to exert considerable selective pressure on gender fitness through pollen limitation of seed set. If pollen flow is predominantly local, seed set in individual plants may be sensitive to the proximity of pollen donors; pollen limitation of seed set may occur if hermaphrodites are locally rare. Under such circumstances, female fitness will be negatively frequency dependent and hermaphrodite fitness will be positively frequency dependent. Given local seed dispersal, a nonrandom clumped distribution of the genders is expected in gynodioecious populations due to the heritability of gender in gynodioecious species. If gender fitness is frequency dependent, such structure should favor hermaphrodites and select against females. To test this hypothesis, I quantified the distribution of the genders in terms of nearest neighbors and neighborhood sex ratio in two populations of gynodioecious Sidalcea malviflora malviflora. I then measured the effect of neighborhood sex ratio on open-pollinated seed set and pollen limitation in both manipulated and unmanipulated neighborhoods. Results indicate that the genders have a patchy distribution and that both genders are pollen limited and show an increase in seed set with an increase in neighborhood hermaphrodite frequency. The observed population sex structure favors hermaphrodites and disadvantages females. These results highlight the importance that population-level traits can have in determining individual fitness and the evolution of sex ratios in gynodioecious species.     

GENDER VARIATION AND SEXUAL DIFFERENCES IN REPRODUCTIVE CHARACTERS AND SEED PRODUCTION IN GYNODIOECIOUS GERANIUM MACULATUM

Variation in sex expression, flowering pattern, and seed production was studied in the self-compatible perennial herb Geranium maculatum in Illinois and Indiana. In a survey of eight populations, female (male-sterile) plants were found in seven (frequencies ranging from 0.5% to 24.3% [median 4.2%]), and intermediate plants (with partly reduced male function) were found in all populations. Gender variation and sexual differences in reproductive characters were studied in detail in two populations. One population consisted of 5% female, 27% intermediate, and 68% hermaphrodite plants; the other consisted of 1% female, 20% intermediate, and 79% hermaphrodite plants. Females produced smaller flowers and began flowering earlier than hermaphrodites. Intermediates produced flowers of an intermediate size and began flowering as early as females. Females and hermaphrodites did not differ in flower number, vegetative size, flowering frequency, survival, or seed size. However, females produced 1.6 times more seeds than hermaphrodites. Intermediates produced 1.3–1.6 times more seeds than hermaphrodites. Some between-year variation in sex expression was observed. Hand-pollination with outcross pollen produced two to four times as many seeds as hand-pollination with self-pollen. A lower outcrossing rate in hermaphrodites than in females may at least partly explain the lower seed set in hermaphrodites. The higher seed production of females, and possibly the high fecundity of the intermediates, should contribute to the maintenance of this sexual polymorphism.     

When is it worth being a self-compatible hermaphrodite? Context-dependent effects of self-pollination on female advantage in gynodioecious Silene nutans

In gynodioecious plant species with nuclear‐cytoplasmic sex determination, females and hermaphrodites plants can coexist whenever female have higher seed fitness than hermaphrodites. Although the effect of self fertilization on seed fitness in hermaphrodites has been considered theoretically, this effect is far from intuitive, because it can either increase the relative seed fitness of the females (if it leads hermaphrodites to produce inbred, low quality offspring) or decrease it (if it provides reproductive assurance to hermaphrodites). Hence, empirical investigation is needed to document whether relative seed fitness varies with whether pollen is or is not limiting to seed production. In the current study, we measured fruit set and seed production in both females and hermaphrodites and the selfing rate in hermaphrodites in two experimental patches that differed in sex ratios in the gynodioecious plant Silene nutans. We found an impact of plant gender, patch, and their interaction, with females suffering from stronger pollen limitation when locally frequent. In the most pollen‐limited situation, the selfing rate of hermaphrodites increased and provided hermaphrodites with a type of reproductive assurance that is not available to females. By integrating both the beneficial (reproductive assurance) and costly effects (through inbreeding depression) of self‐pollination, we showed that whether females did or did not exhibit higher seed fitness depended on the degree of pollen limitation on seed production.     

RESOURCE COMPENSATION AND THE EVOLUTION OF GYNODIOECY IN PHACELIA LINEARIS (HYDROPHYLLACEAE)

Gynodioecy is a dimorphic breeding system in which hermaphrodite and female individuals coexist in populations. Theoretical models have shown that if nuclear genes control sex expression, then gynodioecy can evolve only when females have large advantages in one or more fitness components. These female advantages must be large enough that females' expected lifetime production of viable seeds is more than twice that of hermaphrodites. Previous studies have found that cytoplasmic inheritance and/or a large offspring-vigor advantage of females (caused by hermaphrodite self-pollination and inbreeding depression of selfed seeds) account for this breeding system's evolution. This paper reports studies of gynodioecy in Phacelia linearis, an insect-pollinated annual plant in which gender inheritance appears to be nuclear. Twenty-six P. linearis populations surveyed in northern Utah, USA, contain a majority of perfect-flowered hermaphrodites, but most (22) also contain male-sterile individuals (females), at frequencies of up to 0.16. The hermaphrodite selfing rate is low (0.00–0.20 in four populations). Maternal gender does not consistently affect components of offspring vigor, such as seed size, germination rate, seedling survivorship, and vegetative size. Plants of the two genders do not differ in number of seeds per fruit or mean seed mass. Females produce significantly more fruits and seeds than hermaphrodites in natural populations. The ratio of the mean lifetime seed production of females to the mean lifetime seed production of hermaphrodites ranged from 1.31 to 2.52 in six natural populations. Females have greater shoot biomass than hermaphrodites and produce more seeds at any given shoot biomass than hermaphrodites, suggesting that their seed-production advantage arises from gender-specific patterns of resource allocation to growth and reproduction. The gender difference in plant size varies across environments and across genetic backgrounds. In this species nuclear gynodioecy appears to be evolutionarily stable mainly because of resource compensation by females, without a large outcrossing advantage of females.     

Soil moisture and sex ratio in a plant with nuclear-cytoplasmic sex inheritance

I investigated whether soil moisture affects relative fitness of females and hermaphrodites and sex ratio in a gynodioecious plant with nuclear-cytoplasmic sex inheritance. I contrast these results with those from species with strictly nuclear sex inheritance. I performed a manipulative watering experiment on seed fitness of the two sexes, and field studies measuring seed fitness and sex ratio as a function of soil moisture. In the dry site, watered hermaphrodites produced approximately twice as many seeds as unwatered hermaphrodites, with little treatment effect on female seed production. Over a natural soil moisture gradient, the ratio of female to hermaphrodite seed production was higher in dry than in wet sites. These data show that the seed fitness advantage of females is a function of soil moisture. Despite this, regression of soil moisture on the sex ratio of 23 populations was not significant. These results indicate a sex-dependent effect of soil moisture on resource allocation to seeds that does not translate into a strong effect on sex ratio. This is consistent with theory based on genomic conflict in which sex ratios are predicted to be only partly determined by fitness differences of the sexes.     

Floral sex allocation and reproductive success within inflorescences of Hosta ventricosa,a pseudogamous apomict

Aims Within inflorescences of sexually reproducing hermaphrodites, the production of ovules, fruits and seeds commonly declines from basal (early-opening) to distal (late-opening) flowers, while pollen production remains constant or only changes slightly, with the result that distal (late-opening) flowers become functionally male. However, few empirical studies have specifically examined whether or not changes in allocation to pollen production actually lead to changes in the number of seeds sired, a more direct measure of male fitness. In pseudogamous apomicts, fitness depends on the number of seeds produced; thus, a contrasting pattern of variation in the pollen-to-ovule (P/O) ratio within inflorescences might be expected.Methods We investigated floral sex allocation and reproductive success within racemes of Hosta ventricosa, a pseudogamous apomictic hermaphrodite possessing flowers that open acropetally. We quantified variations in pollen number, ovule number, the P/O ratio and fruit and seed production, from 2007 to 2011, among flowers within racemes of four populations of H. ventricosa in southwest China. Ecological causes for fruit and seed production were evaluated by observing patterns of pollen deposition, flower removal and supplemental pollination.Important findings Pollen number, ovule number and the P/O ratio declined from basal-to-distal positions in all sampled populations (years). Fruit and seed production decreased distally in most populations (years). Low fruit and seed set of distal flowers was not due to pollen limitation because pollen deposition never declined distally and the low fruit and seed set of distal flowers remained even after supplementary pollination was provided. The flower-removal experiment indicated that inter-fruit competition for resources among flowers was common. The low P/O ratio of distal flowers in H. ventricosa might be favored because they were unable to obtain fitness by donating pollen and siring seeds on other plants. Our study may help to understand the adaptive significance of sex allocation among flowers within inflorescences of sexually reproducing hermaphrodites.     

Exploring the genetic basis and proximate causes of female fertility advantage in gynodioecious Thymus vulgaris

In many gynodioecous species, females produce more viable seeds than hermaphrodites. Knowledge of the relative contribution of inbreeding depression in hermaphrodites and maternal sex effects to the female fertility advantage and the genetic basis of variation in female fertility advantage is central to our understanding of the evolution of gender specialization. In this study we examine the relative contribution of inbreeding and maternal sex to the female fertility advantage in gynodioecious Thymus vulgaris and quantify whether there is genetically based variation in female fertility advantage for plants from four populations. Following controlled self and outcross (sib, within-population, and between-population) pollination, females had a more than twofold fertility advantage (based on the number of germinating seeds per fruit), regardless of the population of origin and the type of pollination. Inbreeding depression on viable seed production by hermaphrodites occurred in two populations, where inbreeding had been previously detected. Biparental inbreeding depression on viable seed production occurred in three of four populations for females, but in only one population for hermaphrodites. Whereas the maternal sex effect may consistently enhance female fertility advantage, inbreeding effects may be limited to particular population contexts where inbreeding may occur. A significant family x maternal sex interaction effect on viable seed production was observed, illustrating that the extent of female fertility advantage varies significantly among families. This result is due to greater variation in hermaphrodite (relative to female) seed fertility between families. Despite this genetic variation in female fertility advantage and the highly female biased sex ratios in populations of T. vulgaris, gynodioecy is a stable polymorphism, suggesting that strong genetic and/or ecological constraints influence the stability of this polymorphism.     

Sex allocation of females and hermaphrodites in the gynodioecious Geranium sylvaticum

Seed production and patterns of sex allocation were studied in female and hermaphroditic plants in two gynodioecious populations of Geranium sylvaticum (Geraniaceae). Females produced more flower buds and seeds than hermaphrodites in one of the two study populations. The other female traits measured (pistil biomass, seed number per fruit, individual seed mass) did not differ between the gender morphs. The relative seed fitness of hermaphrodites differed between the study populations, with hermaphrodites gaining less of their fitness through female function in the population with a high frequency of females. However, the amount and size of pollen produced by hermaphrodites did not differ between populations. The number of flower buds was positively correlated with seed production in females, whereas in hermaphrodites a positive correlation between number of buds and seed production was found in only one of the two study populations. These results suggest that fitness gain through female function is labile in hermaphrodites of this species, and is probably affected by environmental factors such as the sex ratio of the population.     

Seedling performance in a trioecious cactus,Pachycereus pringlei: Effects of maternity and paternity

We studied seed germination and the growth and survivorship of seedlings of females and hermaphrodites ofPachycereus pringlei (cardon), a Mexican columnar cactus whose geographically variable breeding system includes trioecy and gynodioecy. Results of a two-year field experiment conducted near Bahia Kino, Sonora, Mexico and a ten-month laboratory experiment were similar and did not support the hypothesis that seedlings of females outperform those of hermaphrodites. In the field, percent seed germination and 2-yr seedling survivorship averaged 66% and 95%, respectively and did not differ among six treatment classes. Seedlings of hermaphrodites generally were larger than those of females at the end of both experiments. Selfed seedlings of hermaphrodites did not grow more slowly than outcrossed seedlings of hermaphrodites or females. Hermaphrodite seedlings performed best when pollinated with hermaphrodite pollen; female seedlings performed best with male pollen. We conclude that superior seedling performance cannot explain why females are able to coexist with hermaphrodites in populations of this cactus. Instead, we postulate that greater annual seed production, which averaged 1.6 times higher in females than in hermaphrodites in two years, may be sufficient to allow females to co-occur with hermaphrodites in this large, longlived plant, especially if sex determination involves cytoplasmic-nuclear inheritance.