Maintenance Of Gynodioecy Research Articles

Insect Visitors of Sidalcea hickmanii ssp. petraea (Malvaceae) and Their Effect on Flower, Fruit, and Seed Production

This study sought to document potential insect pollinators of Neil Rock checkerbloom, Sidalcea hickmanii ssp. petraea (Malvaceae) and measure the effects of pollinator exclusion and plant type on flower, fruit, and seed production. Prior to this study, the pollination requirements of this gynodioecious plant were unknown and potentially complicated by its hermaphroditic and female-only plant types. Analyses showed that pollinator exclusion had no effect on mean number of flowers produced per raceme but significantly reduced the mean number of fruits produced per raceme and mean number of fruits produced per flower, as well as the mean number of seeds produced per raceme in both female-only and hermaphroditic plants. These results suggested that S. hickmanii ssp. petraea is pollinator dependent. Six orders (Hymenoptera, Coleoptera, Homoptera, Lepidoptera, Diptera, and Hemiptera) representing 29 taxa of insects (primarily Hymenoptera – notably Osmia and Hoplitis, and Coleoptera – notably Anthonomus and Trichodes) were collected from flowering S. hickmanii ssp. petraea plants. Adult Anthonomus weevils were observed selectively feeding on the developing fruits of hermaphroditic over female-only plants. This selective predation may have a significant impact on the maintenance of gynodioecy in this endemic, narrowly-isolated subspecies of Sidalcea hickmanii.

Patterns of Genome-Wide Nucleotide Diversity in the Gynodioecious Plant Thymus vulgaris Are Compatible with Recent Sweeps of Cytoplasmic Genes.

Gynodioecy is a sexual dimorphism where females coexist with hermaphrodite individuals. In most cases, this dimorphism involves the interaction of cytoplasmic male sterility (CMS) genes and nuclear restorer genes. Two scenarios can account for how these interactions maintain gynodioecy. Either CMS genes recurrently enter populations at low frequency via mutation or migration and go to fixation unimpeded (successive sweeps), or CMS genes maintain polymorphism over evolutionary time through interactions with a nuclear restorer allele (balanced polymorphism). To distinguish between these scenarios, we used transcriptome sequencing in gynodioecious Thymus vulgaris and surveyed genome-wide diversity in 18 naturally occurring individuals sampled from populations at a local geographic scale. We contrast the amount and patterns of nucleotide diversity in the nuclear and cytoplasmic genome, and find ample diversity at the nuclear level (π = 0.019 at synonymous sites) but reduced genetic diversity and an excess of rare polymorphisms in the cytoplasmic genome relative to the nuclear genome. Our finding is incompatible with the maintenance of gynodioecy via scenarios invoking long-term balancing selection, and instead suggests the recent fixation of CMS lineages in the populations studied.

HOW SELFING, INBREEDING DEPRESSION, AND POLLEN LIMITATION IMPACT NUCLEAR-CYTOPLASMIC GYNODIOECY: A MODEL

Gynodioecy, the co-occurrence of females and hermaphrodites, is often due to conflicting interactions between cytoplasmic male sterility genes and nuclear restorers. Although gynodioecy often occurs in self-compatible species, the effect of self-pollination, inbreeding depression, and pollen limitation acting differently on females and hermaphrodites remains poorly known in the case of nuclear-cytoplasmic gynodioecy (NCG). In this study, we model NCG in an infinite population and we study the effect of selfing rate, inbreeding depression, and pollen limitation on the maintenance of gynodioecy and on sex ratios at equilibrium. We found that selfing and inbreeding depression have a strong impact, which depends on whether restorer cost acts on male or female fitness. When cost affects male fitness, the strength of cost has no effect, whereas selfing and inbreeding depression only impact gynodioecy by modifying the value of the female advantage. When cost affects female fitness, selfing facilitates NCG and reduces the role of strength of the cost, even when no inbreeding depression occurs, whereas inbreeding depression globally restricts the maintenance of the polymorphism. Finally, we found that pollen limitation could additionally strongly modify the dynamic of gynodioecy. We discuss our findings in the light of empirical data available in gynodioecious species.

Maternal sex effects and inbreeding depression under varied environmental conditions in gynodioecious Fragaria vesca subsp. bracteata

Gynodioecy (coexistence of females and hermaphrodites) is a sexual system that occurs in numerous flowering plant lineages. Thus, understanding the features that affect its maintenance has wide importance. Models predict that females must have a seed fitness advantage over hermaphrodites, and this may be achieved via seed quality or quantity. Females in a population of Fragaria vesca subsp. bracteata, a long-lived gynodioecious perennial, do not demonstrate a seed quantity advantage, so this study explored whether females produced better quality seed via maternal sex effects or avoidance of inbreeding depression (IBD). Families of selfed and outcrossed seed were created using hermaphrodite mothers and families of outcrossed seed were created using female mothers. The effects of these pollination treatments were assessed under benign conditions early in life and under varied conditions later in life. To test for an effect of maternal sex, fitness components and traits associated with acclimation to variable environments of progeny of outbred hermaphrodites and females were compared. To test for expression of IBD, fitness parameters between inbred and outbred progeny of hermaphrodites were compared. Offspring of females were more likely to germinate in benign conditions and survive in harsh resource environments than outbred progeny of hermaphrodites. IBD was low across most life stages, and both the effect of maternal sex on progeny quality and the expression of IBD depended on both maternal family and resource condition of the progeny. The effect of maternal sex and IBD on progeny quality depended on resource conditions, maternal lineage and progeny life stage. In conjunction with known lack of differences in seed quantity, the quality advantages and IBD observed here are still unlikely to be sufficient for maintenance of gynodioecy under nuclear inheritance of male sterility.

Genetic determination of male sterility in gynodioecious Silene nutans.

Gynodioecy, the coexistence of female and hermaphrodite plants within a species, is often under nuclear-cytoplasmic sex determination, involving cytoplasmic male sterility (CMS) genes and nuclear restorers. A good knowledge of CMS and restorer polymorphism is essential for understanding the evolution and maintenance of gynodioecy, but reciprocal crossing studies remain scarce. Although mitochondrial diversity has been studied in a few gynodioecious species, the relationship between mitotype diversity and CMS status is poorly known. From a French sample of Silene nutans, a gynodioecious species whose sex determination remains unknown, we chose the four most divergent mitotypes that we had sampled at the cytochrome b gene and tested by reciprocal crosses whether they carry distinct CMS genes. We show that gynodioecy in S. nutans is under nuclear-cytoplasmic control, with at least two different CMSs and up to four restorers with epistatic interactions. Female occurrence and frequency were highly dependent on the mitotype, suggesting that the level of restoration varies greatly among CMSs. Two of the mitotypes, which have broad geographic distributions, represent different CMSs and are very unequally restored. We discuss the dynamics of gynodioecy at the large-scale meta-population level.

Inbreeding effect on male and female fertility and inheritance of male sterility in Nemophila menziesii (Hydrophyllaceae)

Models of the evolution of gynodioecy assume that inbreeding affects male and female fertility equally and ignore quantitative variation in sex expression. The objectives of this study were to assess inbreeding effects, genetic background, and plant maturity on male and female fertility and the mechanism of male sterility inheritance for Nemophila menziesii (Hydrophyllaceae). Frequency of male-sterile flowers, number of anthers and ovules, and percentage of viable pollen were measured on plants from different pedigrees and five inbreeding levels (F = 0, 0.0625, 0.25, 0.5, and 0.75). Quantitative variation in male sterility was evident. As inbreeding increased, anther and ovule number decreased; the effect on anther number was greater than on ovule number. Pedigrees varied in number of male-sterile flowers and inbreeding effects. Frequency of male-sterile flowers was greatest among first flowers. No trade-off between male and female fertility was detected. A model attributing male sterility to a cytoplasmic locus and restoration to male fertility to a nuclear locus accounted for the distribution of complete sterility and hermaphroditism over the pedigrees. This study suggests that models of the evolution and maintenance of gynodioecy should allow for quantitative variation in male and female fertility components due to inbreeding, pedigree, and plant maturity.

Reproductive characters in a gynodioecious species, Silene italica (Caryophyllaceae), with attention to the gynomonoecious phenotype

Gynodioecious populations (i.e. populations with female and hermaphrodite individuals) often contain a third phenotype with an intermediate sex expression. In Silene italica, this phenotype is characterized by a mixture of pistillate and perfect flowers and is thus gynomonoecious. To characterize sexual functions of these gynomonoecious individuals and their potential influence in the maintenance of gynodioecy, reproductive characters of the three sexual phenotypes were compared over 2 years in several families of S. italica produced by crossing. We found that gynomonoecious individuals were intermediate for flower production and female fertility characters, although they did not always significantly differ from female individuals. Perfect flowers of gynomonoecious and hermaphrodite plants were similar in size and pollen production. Gynomonoecious individuals were thus intermediate in female and in male functions. Family effects were found for most of the characters. The female advantage (i.e. the fertility of females compared to the female fertility of pollen producing plants) was not dramatically different when gynomonoecious plants were taken into account. © 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 87, 583–591.

Evidence of Gynodioecy inKallstroemia grandiflora(Zygophyllaceae): Microsporogenesis in Hermaphrodite and Female Plants and Lack of Reproductive Compensation

Understanding mechanisms involved in the maintenance of gynodioecy in natural populations requires evidence concerning the phenotypic expression and reproductive consequences of male sterility. We have recently discovered male sterility in populations of Kallstroemia grandiflora from northwestern Mexico. Here we describe the development of anther and pollen grains in hermaphrodite and female plants and explore whether females experience any compensatory advantage over hermaphrodites. The major difference in anther development between morphs was the early disintegration of tapetal cells in anthers of pistillate flowers. Abnormalities in developing pollen grains in pistillate flowers were seen in the microspore mother cells, microspore tetrads, and young and mature pollen grains. Biomass allocation to flowers, petals, and stamens were larger in hermaphrodites, while both sexes had the same number of ovules per flower. Hermaphrodite flowers were self-compatible. Pollination experiments revealed evidence of pollinator limitation for female plants but not for hermaphrodites. No evidence of reproductive compensation was detected, as flower and fruit production were similar for both sexes in two populations of K. grandiflora. We suggest alternative mechanisms that could maintain male sterility in natural populations of K. grandiflora.

Sex‐biased seed predation and the maintenance of females in a gynodioecious plant

We investigated genetic and ecological factors contributing to the maintenance of females in populations of the gynodioecious plant, Sidalcea hendersonii (Malvaceae). Our crossing experiments indicated that male sterility is controlled by a dominant nuclear allele. Nuclear determination of sex theoretically requires much higher female fitness to account for the high frequency of female plants often observed during surveys of S. hendersonii populations. Females were, in fact, shown to have higher fitness in an experimental population, producing more viable seed and surviving offspring than hermaphrodite plants. In natural populations, however, differences in viable seed production were not evident unless seed predation was considered. Sex-biased seed predation appears to play an important role in the maintenance of gynodioecy in S. hendersonii. In populations with high female frequencies, weevil larvae destroyed significantly more seeds from hermaphrodite plants than females, substantially reducing their seed production. To our knowledge, this study provides the first evidence that sex-biased predation may be responsible for high female frequencies in natural populations of a gynodioecious species.

The Maintenance of Gynodioecy and Androdioecy in a Metapopulation

The Maintenance of Gynodioecy and Androdioecy in a Metapopulation

Variation in a Mutualism: Phenology and the Maintenance of Gynodioecy in Two Indian Fig Species

11 studied phenological variation in the coevolved mutualism between gynodioecious figs (genus Ficus) and their species-specific pollinator wasps. The phenology of tropical gynodioecious figs is important to vertebrates relying on fig fruit as a resource, and to understanding the evolution of gynodioecy in Ficus. 2 Gynodioecious fig species have hermaphrodite trees with closed, urn-shaped inflorescences bearing male and female flowers, and female trees with inflorescences bearing female flowers. Pollinators entering receptive inflorescences on hermaphrodite trees pollinate, lay eggs in female flowers, and die; weeks later, offspring emerge, mate and carry pollen from hermaphrodite trees to other trees. Wasps entering inflorescences on female trees pollinate female flowers but cannot lay eggs, and die without leaving offspring. Hermaphrodite ('male') trees produce pollen and wasps, and no seeds; female trees produce only seeds. 3 During 1991 and 1992, I observed the phenology of two gynodioecious fig tree species, Ficus exasperata and F. hispida, in a dry and a wet site in Coorg District, south India. 4 Ficus exasperata trees displayed a synchronous phenology very similar to that predicted by one hypothesis relating the evolution of gynodioecy to phenology. Female trees of F. exasperata produced seeds synchronously during the monsoon season and 'male' trees produced pollinator wasps and pollen synchronously during the peak period of female receptivity. Crop production occurred more frequently in the dry than in the wet site. Female trees bore mature fruit for longer periods than 'male' trees. 5 In contrast, several phenological traits of F. hispida departed strongly from prediction. This species displayed an asynchronous phenology at the population level. Receptivity and wasp or seed production in F. hispida occurred year-round, female trees produced more crops than 'male' trees, and there was considerable overlap in timing of 'male' and female inflorescence production. Durations of phenological phases were longer on female than on 'male' trees at the wet site. 6 An asynchronous phenology appears to be more advantageous in aseasonal than in seasonal environments. If the two phenological types observed in this study are found to be widespread, then the possibility that functional dioecy in Ficus evolved via more than one pathway must be considered.

Spectrophotometric analysis of nectar production in Silene vulgaris (Caryophyllaceae)

Significant differences in nectar content were observed between hermaphrodite and female plants of the gynomonoecious‐gynodioecious taxon, Silene vulgaris, from populations in northern lower Michigan. These differences in nectar sugar content were observable with a carbohydrate digestion technique involving sulfuric acid, phenol, and measurement of the color change with a spectrophotometer. A hand‐held refractometer did not provide sufficient resolution to discern differences between the genders. Both genders were similar in the pattern of sugar content of nectar during floral development. A splitplot factorial design revealed significant differences both among individual plants and stages of floral phenology within each gender. The spectrophotometric technique and statistical analysis provided the needed resolution to discern differences between the genders that we relate to pollinator activity, levels of inbreeding depression, and the maintenance of gynodioecy in this taxon.

Floral sex ratio variation in hermaphrodites of gynodioeciousChionographis japonica var.kurohimensis Ajima et Satomi (Liliaceae)

Intrapopulation and interpopulation variations in floral sex ratio in hermaphrodites of gynodioeciousChionographis japonica var.kurohimensis (Liliaceae) were examined. The relative ratio of male flowers to total flowers (male and perfect flowers) decreased with plant size, suggesting size-dependent gender modification. The relative ratio of male flowers per population-basis is negatively correlated with the mean number of perfect flowers. Since the number of perfect flowers proportionally increased with plant size, populations showing low maleness consist of relatively bigger plants and are considered to be in high-quality environment. On the other hand, the relative ratio of male flowers per population basis is independent of female frequency in the population. Plasticity in gender expression probably plays an important role of maintenance of gynodioecy inC. japonica var.kurohimensis.

Female frequencies and fitness components between sex phenotypes among gynodioecious populations of the colonizing species Trifolium hirtum All. in California.

Male sterility has been recently discovered in Californian populations of rose clover (Trifolium hirtum). This study describes the frequency distribution of male sterility in Turkish and Californian populations, and compares fitness components of hermaphrodites and females. As male-steriles were found in Turkey, it is likely that they were introduced to California during the 1940's with the original material derived from Turkey. The spread of male-sterile genotypes in California has given rise to an asymmetrical frequency distribution of male sterility with positive skewness. The frequency of females has not exceeded fifty percent and it appears to be temporally stable in most of the Californian populations. The hypothesis that female frequencies and fitness differences between phenotypes are correlated was tested by comparing sex phenotypes in seven populations with contrasting levels of male sterility. The analysis of those populations showed no evidence for such a correlation as no significant differences were found between sex phenotypes for fecundity and seed germination. The hypothesis that females are maintained due to fitness differences in the progeny of hermaphrodites and females was experimentally tested in the population with maximum frequency of male-steriles. The results showed no significant differences in the demographic performance of the progenies of hermaphrodites and females. The present results are discussed in terms of the possible mechanism of maintenance of gynodioecy in rose clover.

The evolution and maintenance of gynodioecy in sexually and vegetatively reproducing plants

The evolution and maintenance of gynodioecy is explored theoretically at the ramet level in models that allow for differences between females and hermaphrodites in vegetative components of fitness as well as in sexual components. For nuclear control of male sterility, it is shown that females may be maintained by selection in an otherwise hermaphrodite population through advantages over hermaphrodites in vegetative fitness components, even if there is no sex difference in maternal fitness components. The advantage required depends on the importance of vegetative reproduction. If females produce more daughter ramets than ovule offspring, the advantage in vegetative fitness components required to maintain females is numerically smaller than the well-known requirement of a two-fold advantage in maternal fitness components. Three further findings in the nuclear models are that (a) with some parameter combinations, females attain frequencies of higher than 0·5, in which case their equilibrium frequency decreases rather than increases with increasing female advantage in seed fecundity; (b) the advantage in adult survivability required to maintain a given equilibrium frequency of females becomes smaller with increasing reliance on vegetative reproduction; and (c) the rate of approach to equilibrium is inversely proportional to the level of vegetative reproduction in the population as a whole. If male sterility is determined solely by cytoplasmic factors, females should be maintained if they have any advantage in vegetative reproduction over hermaphrodites, given that maternal fitness components are equal in the two sexes. For nuclear-cytoplasmic control, it is shown that the premise that a joint polymorphism for cytoplasmic male sterility and nuclear fertility restoration should not be maintained in the absence of differences in fitness between sex genotypes of the same sex phenotype (Charlesworth and Ganders, 1979) may be generalised to situations where sex differences in vegetative reproduction occur. The significance of vegetative reproduction in population genetic studies in general is briefly discussed.