Labile Sex Expression Research Articles

Labile sex expression in angiosperm species with sex chromosomes.

Here, we review the literature on sexual lability in dioecious angiosperm species with well-studied sex chromosomes. We distinguish three types of departures from strict dioecy, concerning either a minority of flowers in some individuals (leakiness) or the entire individual, which can constantly be bisexual or change sex. We found that for only four of the 22 species studied, reports of lability are lacking. The occurrence of lability is only weakly related to sex chromosome characteristics (number of sex-linked genes, age of the non-recombining region). These results contradict the naive idea that lability is an indication of the absence or the recent evolution of sex chromosomes, and thereby contribute to a growing consensus that sex chromosomes do not necessarily fix sex determination once and for all. We discuss some implications of these findings for the evolution of sex chromosomes, and suggest that more species with well-characterized lability should be studied with genomic data and tools. This article is part of the theme issue 'Sex determination and sex chromosome evolution in land plants'.

Probing the floral developmental stages, bisexuality and sex reversions in castor (Ricinus communis L.)

Castor (Ricinus communis L) is an ideal model species for sex mechanism studies in monoecious angiosperms, due to wide variations in sex expression. Sex reversion to monoecy in pistillate lines, along with labile sex expression, negatively influences hybrid seed purity. The study focuses on understanding the mechanisms of unisexual flower development, sex reversions and sex variations in castor, using various genotypes with distinct sex expression pattern. Male and female flowers had 8 and 12 developmental stages respectively, were morphologically similar till stage 4, with an intermediate bisexual state and were intermediate between type 1 and type 2 flowers. Pistil abortion was earlier than stamen inhibition. Sex alterations occurred at floral and inflorescence level. While sex-reversion was unidirectional towards maleness via bisexual stage, at high day temperatures (Tmax > 38 °C), femaleness was restored with subsequent drop in temperatures. Temperature existing for 2–3 weeks during floral meristem development, influences sexuality of the flower. We report for first time that unisexuality is preceded by bisexuality in castor flowers which alters with genotype and temperature, and sex reversions as well as high sexual polymorphisms in castor are due to alterations in floral developmental pathways. Differentially expressed (male-abundant or male-specific) genes Short chain dehydrogenase reductase 2a (SDR) and WUSCHEL are possibly involved in sex determination of castor.

Timing and Patterns of Size, Reproduction, and Seed Germination in Florida Endemic Euphorbia telephioides (Euphorbiaceae): Management and Conservation Implications

To protect and manage species listed under the US Endangered Species Act requires knowledge of the species' biology. Biological information was lacking for Euphorbia telephioides, a threatened species endemic to pine flatwoods in the Florida Panhandle. Decline of this species is due largely to habitat loss and degradation. To understand the conservation requirements for the recovery of E. telephioides, we established three permanent plots, marked 150 plants, and investigated size and reproduction, response to fire, and in situ seed germination and seedling survival from 2010 to 2014. Plants are long-lived and survived fire by resprouting. Populations are composed of vegetatives, males, females, and monoecious individuals with labile sex expression, including fire-induced sex change. Both adults and seedlings exhibited obligate winter dormancy and facultative non-synchronized summer dormancy, and some adults had prolonged (>1 y) vegetative dormancy, which minimize exposure to stressful conditions. Reproductive plants tended to be larger than vegetatives, but did not differ significantly in most size parameters. Seeds possess a deep physiological dormancy, tolerate fire, and persist in the field less than 1 y; thus, soil seed bank is unlikely to maintain populations in the face of environmental stochasticity. Once established, seedlings resprout after fire, which likely contributes to population persistence. Overall, E. telephioides displays life history traits that are adaptive in the fire-prone habitats where this species occurs. For specific management recommendations in the field, knowledge of gender expression and lability, seed ecology, and the effects of disturbances such as fire on plants and habitat are imperative.

Floral development and the formation of functionally unisexual flowers in Xanthoceras sorbifolium (Sapindaceae), a morphologically andromonoecious tree endemic to northern China

KEY MESSAGE: Xanthoceras sorbifolium is apparently andromonoecious but exhibits a cryptically monoecious breeding system. Sexual differentiation in male and functional female flowers occurs 2 weeks before flowering. Individual trees of Xanthoceras sorbifolium bear male and morphologically bisexual flowers but functionally female flowers, and show labile sex expression. Investigations of the floral development are of significant value for understanding the breeding system and elucidating the systematic relationships. We studied floral development of male and bisexual flowers using scanning electron and light microscopy. The early stages of floral development were essentially the same, and all floral organ primordia were initiated in the two types of flowers of X. sorbifolium. Later, the stamens in bisexual flowers and the gynoecium in male flowers were aborted. We divided floral development into nine stages. Morphological differences between male and bisexual flowers appeared first at stage 8, when the style elongated obviously and the stigma papillae began to expand in the bisexual flowers but not in the male flowers. Ovule development was arrested shortly after formation of megaspore mother cells or during meiosis in the male flowers, whereas anther development was aberrant in the bisexual flowers. Morphologically bisexual flowers of X. sorbifolium do not have male function and are functionally female. Comparison of floral developmental characters did not support the separation of the Chinese monotypic genus Xanthoceras from the family Sapindaceae.

On merging Acer sections Rubra and Hyptiocarpa: Molecular and morphological evidence.

In this study, we expanded Acer sect. Rubra Pax to include A. sect. Hyptiocarpa Fang. Traditionally, section Rubra comprises two iconic species, Acer rubrum Linnaeus (red maple) and A. saccharinum Linnaeus (silver maple), of eastern North American forests as well as the rare Japanese montane species, A. pycnanthum K. Koch. Section Hyptiocarpa consists of A. laurinum Hasskarl and A. pinnatinervium Merrill, which occur in subtropical and tropical regions of southwestern China to southeast Asia. Here, we confirm prior phylogenetic results showing the close relationship between sects. Rubra and Hyptiocarpa, and we use scanning electron microscopy to demonstrate that leaves of species within these sections have similar arrangements of cuticular waxes, which account for the silvery color of their abaxial surfaces. We describe that the sections also share labile sex expression; inflorescences that range from compound racemose thyrses, to racemes or umbels and that may have undergone evolutionary reduction; and several features of their fruits, such as seed locules without keels, basal portion of wings straight, acute attachment angle between mericarps, and production of some mericarps that are seedless and partially developed at maturity. Our expansion of sect. Rubra to include sect. Hyptiocarpa better elucidates the biogeographic and evolutionary history of these species. Additionally, we show that A. laurinum and A. pinnatinervium have intergrading morphology and are probably synonymous, but we note that further studies are required to conclude their taxonomic status.

Absolute and relative content of carbon and nitrogen differ by sex inCeratopteris richardiigametophytes

When habitats are heterogeneous regarding key abiotic factors, and individual organisms have no control over the environment in which they develop, labile sex expression can allow individuals to adjust their sex based on local environmental conditions, resulting in increased individual fitness. Sexual lability is found extensively in homosporous ferns, where sex expression is often regulated via the pheromone antheridiogen. Nutrient availability may provide additional signals for sex determination in fern gametophytes, particularly if nutrient demands required for sexual development differ by sex. The model fern Ceratopteris richardii Brongn. has a well-characterized antheridiogen response and short time to sexual maturity. Although tests for nutrient effects on sex determination have been conducted in this fern, tests for differences in nutrient demands by sex have not. Elemental analysis demonstrated that 14-day-old ameristic male and meristic female or hermaphrodite gametophytes of C. richardii differ significantly in their relative carbon and nitrogen masses, resulting in significantly dissimilar C:N ratios between the sexes. Average gametophyte dry mass in ameristic males was approximately half that of meristic plants of the same age, and contained less N than meristic gametophytes in both relative and absolute terms. Those characteristic differences in elemental composition imply that variation in nutrient availability could potentially influence sex expression in C. richardii gametophyte populations, rather than regulation of sex determination by the antheridiogen system alone.

Effects of variation in carbon, nitrogen, and phosphorus molarity and stoichiometry on sex determination in the fernCeratopteris richardii

Carbon (C), nitrogen (N), and phosphorous (P) are needed by all organisms for basic biological processes. When an individual macronutrient is not accessible, nutrient limitation occurs. The stochiometric balance between multiple nutrients and individual concentrations are both vital for normal growth and development. Labile sex expression in plants is a phenotypic trait predicted to be sensitive to local nutrient conditions because males and females differ in their nutritional demands. We applied concepts from ecological stoichiometry to assess the effects of variation in individual nutrient concentration and multiple macronutrient stoichiometry on sexual development in the fern Ceratopteris richardii Brongn. Manipulation of N, P, and organic and inorganic C was expected to yield variation in the ratio of males to females, consistent with environmental sex-determination theory. Our results suggest nutrient stoichiometry, not strictly concentration, influences sex determination at ambient CO2. However, an early response to population density preempted nutrient effects in elevated CO2environments with exogenous glucose, in which C. richardii gametophytes presumably grow naturally. Although sex determination is not nutrient-dependent in the latter environment, C:N in the dry mass of meristic gametophytes is influenced by the external nutrient context, suggesting sex determination takes place before abiotic environmental factors subsequently influence plant nutrient uptake.

Duodichogamy and sex lability in Sapindaceae: the case of Paullinia weinmanniifolia

Paullinia weinmanniifolia (Sapindaceae) is an endemic Brazilian climber found in the Atlantic Forest. The flowers are arranged in synflorescences with approximately 34 thyrses. In the studied material, each thyrse produced 85.8 male flowers and 15.8 female flowers. The small, diclinous and zygomorphic flowers present a sophisticated morphology, described here in detail. They are visited by many insects, with bees being the main pollinators. Sex expression was investigated by monitoring one population of restinga in Marica Environmental Protection Area, Rio de Janeiro State, Brazil, during 2–4 years. Experiments were conducted taking into account thyrse, synflorescence, plant and population. Most individuals showed a duodichogamic sequence of flowering (male–female–male). However, the population overall had a more complex flowering pattern: some individuals were protogynous, others protandrous; a few individuals produced flowers of only one sex, and some individuals changed sex expression in the second year of the study, either from male to female or from female to male. This was the first ever labile sex expression recorded for the tribe Paullinieae. Anthetic female and male flowers were never found simultaneously in the same thyrse or synflorescence. Nevertheless, the two flower morphs overlapped, though rarely, within the same individual. The pattern of flowering observed in this species maximizes the level of outcrossing, since the temporal separation of male and female flowers on the same plant is precise enough for the species to be regarded as (obligatorily) xenogamous.

Labile Sex Expression and the Evolution of Dioecy in Ophryotrocha Polychaete Worms

Labile sex expression is considered to play a key role in the evolution of breeding systems and in the transition from hermaphroditism to dioecy, according to the evolutionary models proposed for plants. While in hermaphrodites sex allocation within the individual can be plastically adjusted in response to social environment, in dioecious species it is predicted to be fixed. However, labile sex expression in the form of gender plasticity can still be present in dioecious species of animals with environmental sex determination. It is still unclear how gender plasticity is involved in the evolution of breeding systems and what its role is in the transition from hermaphroditism to dioecy. We assessed the degree of plasticity in gender expression in three dioecious species of polychaete worms of the genus Ophryotrocha. We found sexual polymorphism and plasticity in sex expression during the juvenile phase to be a response to social environment. The majority of juveniles reared with an adult female or male expressed the gender opposite of that of the partner, so as to form heterosexual pairs. On the basis of these findings we outline a possible evolutionary pathway of the transition from hermaphroditism to dioecy in the genus Ophryotrocha.

Development and characterization of a novel set of microsatellite markers for Arisaema serratum (Araceae)

We developed novel microsatellite markers in Arisaema serratum, a perennial herb that possesses pitfall flowers and exhibits labile sex expression, to facilitate research on parentage and pollination biology in this species. By using procedures for enrichment of desired microsatellite-containing fragments and PCR-based isolation of microsatellite arrays, we detected 18 novel microsatellite loci. Thirteen were highly polymorphic: the number of alleles per locus ranged from six to 46, the observed heterozygosities ranged from 0.320 to 0.940, and the expected heterozygosities ranged from 0.440 to 0.976. Nine of the 13 markers successfully amplified regions in congeneric species. These highly polymorphic markers will facilitate further studies on the mode of pollination and other aspects of reproductive biology in A. serratum.

Generation of expressed sequence tags from carob (Ceratonia siliqua L.) flowers for gene identification and marker development

Carob (Ceratonia siliqua L.) is a caesalpinoid legume tree showing labile sex expression. With the main aims of identifying flower-expressed genes and of developing specific markers, 1,056 clones from a complementary DNA library of carob flowers were bidirectionally sequenced. A total of 1,377 high-quality expressed sequence tags were clustered into 1,096 unigenes. Basic Local Alignment Search Tool and Gene Ontology functional annotation allowed to identify several agronomically important genes, such as those involved in flower development and sexual reproduction, response to stress, galactomannan synthesis, and hormone pathways. Genes involved in the ethylene biosynthesis and response were quantified in developing flowers of three sex genotypes (male, female, and hermaphrodite) using quantitative reverse transcription polymerase chain reaction. The transcript levels of 1-aminocyclopropane-1-carboxylic acid oxidase, acting downstream in ethylene pathway, and Ethylene Insensitive 3 (EIN3)-like, a transcription factor involved in ethylene signaling, were directly correlated with maleness, indicating a possible role of ethylene in carob sex expression. Furthermore, the first set of carob genic microsatellites was developed, which might be useful for genotyping and genetic diversity analysis.

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.

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

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

Sex expression of an immobile coral-inhabiting snail, Quoyula monodonta

To test the hypotheses explaining the sex expression of the immobile snail Quoyula monodonta, which inhabits the surfaces of the branching coral, Pocillopora eydouxi, the size, sex, gonad development, penis length and the composition of neighboring individuals were investigated between November 1994 and August 1995 in southern Taiwan. Although the snails often aggregated and formed patches, more than 50% were solitary. Females were larger than males both within a snail patch and in the whole population, but the overlap in size range was wide. The males were generally accompanied by females, whereas most females were solitary. Females were rarely (6%) found in the same patch with another female, but 35% of the males had male neighbors. Most juveniles found were also solitary. The composition pattern within a patch cannot be explained by random sampling. Gonad development of an individual was dependent on the presence and the sex of its neighbors within the same patch; the penis length of males also depended on the presence of neighbors. These phenomena suggest that an individual is sensitive to its neighbors. No individuals in the process of sex change were ever found from histological studies of the gonads. Neither the hypothesis that the sex of recruits determines their habitats, nor the hypothesis that there is strict protandric sex-change is supported. The results, however, are all clearly compatible with the hypothesis that the snail has labile sex expression. In the presence of existing females in a patch, recruits are more likely to develop into males, whereas recruits starting a new patch grow to a larger size before developing into females directly. The labile sex expression of Q. monodonta is the only such report in neogastropods.

A Rare Occurrence of Seed Formation on Male Branches of the Dioecious Tree, Populus deltoides

Abstract We observed formation of female flowers and seedpods, subsequent to the production of male flowers and pollen, on branch cuttings from a male Populus deltoides var. wislizenii tree. Labile sex expression is rare in the genus Populus, and this is the only recorded instance for this variety of P. deltoides. Mature trees exhibited the same phenomenon in the field and some released copious amounts of seed during 1997. These observations may explain apparent sexual lability within four populations of P. deltoides along the Rio Grande. If protandrous hermaphrodites exist in this species, observations of sexual lability in these field populations could be explained by year to year variation in the timing of census observations; i.e., earlier season observations would score these individuals as males. We conclude that P. deltoides var. wislizenii is a subdioecious species with occasional bisexual individual plants.

The Influence of Fruit on the Regulation of Internal Ethylene Concentrations and Sex Expression inCucurbita texana

Plants with labile sex expression often regulate the production of pistillate and staminate flowers on the basis of developmental and environmental conditions. In many monoecious plant species, developing fruits inhibit pistillate flower production and promote staminate flower production. Because the phytohormone ethylene promotes pistillate flower production in a variety of wild and cultivated plant species, we examined the influence of fruit development on internal ethylene production and their combined effects on sex expression in field‐grown Cucurbita texana (Cucurbitaceae). We compared the sex expression of plants with fruit and without fruit, and we measured internal ethylene concentrations within the hollow internodes of their branches. Plants without fruit had more than twice as many pistillate flowers than plants with fruit. Ethylene was greatest within internodes just below the tips of branches compared with more basal internodes (2–21 internodes from the tip) in both fruiting and fruitless treatments. Ethylene concentrations within branches with fruit were highest 18 d after pollination, just as fruits reached their maximum volume. Branches with two or more developing fruits had the lowest ethylene concentrations, whereas ethylene levels were significantly higher on fruitless branches and one‐fruited branches. Our results indicate that young developing fruits may send a signal that inhibits ethylene production, leading to the promotion of staminate flowers, and that, when fruits are no longer strong resource sinks, ethylene concentrations increase and promote pistillate flower production.

Labile sex expression in plants

ABSTRACTThe range of environmental sex determination and sex changes throughout plant taxa from bryophytes and pteridophytes to spermatophytes is reviewed. Lability in sex expression occurs in many plant taxa but only in homosporous pteridophytes is labile sex the rule. Among angiosperms, labile sex appears to be more common among dioecious and monoecious plants than among hermaphrodites. However, hermaphrodites can control allocation to male and female functions by varying the relative emphasis on pollen and ovules. A majority of plants with labile sex expression are perennials, which indicates that flexibility in sex is more important for species with long life cycles. Environmental stress, caused by less‐than‐optimal light, nutrition, weather or water conditions, often favours maleness. The extreme lability in the sex expression of homosporous pteridophytes is suggested to be related primarily to the mating systems.

Floral herbivore effect on the sex expression of an andromonoecious plant, Isomeris arborea (Capparaceae)

Flower-feeding insects may influence the reproductive behavior of their host plant. In plants with labile sex expression, the ratio of maternal to paternal investment may change in response to damage, an effect that goes beyond the direct reduction of plant gametes. We examined the effects of floral herbivory by the beetle Meligethes rufimanus (Nitidulidae) on the ratio of hermaphroditic flowers to male flowers in an andromonoecious shrub, Isomeris arborea (Capparaceae) in southern California. Plants exposed to herbivory had a greater rate of flower bud abortion than those protected from herbivory. Exposed plants produced a greater proportion of hermaphroditic flowers to male flowers, although damaged inflorescences still produced fewer fruit. An additional manipulative experiment showed that the removal of pistils on inflorescences led to an increase in the proportion of hermaphroditic flowers. This suggests that the presence of fruit may lead to pistil suppression in developing flowers. Adaptive responses to herbivory which favor andromonoecy thus include the continued production of hermaphroditic flowers when floral damage is high (and hence low fruit set), and a switch to male flower production when floral damage is low (and fruit production increases). The consequences of an altered six ratio induced by insect herbivores may lead to indirect effects on both the male and female reproductive success of this plant.

Gender variation and the evolution of dioecy in Thymelaea hirsuta (Thymelaeaceae)

Phenotypic gender in the evergreen shrub Thymelaea hirsuta was studied at regular intervals over 3–6 years in five natural populations in the western desert of Egypt. Quantitative estimates of gender were calculated for each plant, each year over the entire study period. Plants were also classified using a typological framework, allowing discrimination between plants that followed different flowering phenologies (e.g., dichogamy) but that may have had the same quantitative values of phenotypic gender. Two contrasting patterns of gender were revealed. Approximately one-third of all plants were stable in their gender expression (i.e., they produced the same floral pattern and quantitative gender on every occasion); the remainder had labile gender phenotypes, showing varying degrees and patterns of gender lability. The relative frequency of gender phenotypes differed significantly between sites. Stable unisexual forms were most prevalent at the depression sites, where the water table is closer to the soil surface. Patterns of gender variation in T. hirsuta can be interpreted in terms of a complex evolutionary pathway to dioecy, represented by several intermediate stages, including dichogamous, monoecious, and subdioecious individuals. Alternatively, there may be no directionality to the array; gender phenotypes may reflect localized selection that confers differential fitness on the phenotypes, to the extent that such phenotypes may be heritable. Keywords: dioecy, evolution, Thymelaea hirsuta, labile sex expression, gender variation.

ECOLOGICAL ASPECTS OF SEX EXPRESSION IN SUBDIOECIOUS SCHIEDEA GLOBOSA (CARYOPHYLLACEAE)

The importance of ecological factors such as sex lability, spatial segregation, and resource allocation in the evolution of dioecy were examined in Schiedea globosa. S. globosa is a subdioecious species with equal numbers of plants possessing strictly male or female function and a small proportion of hermaphrodites. The propensity for labile sex expression was under both environmental and genetic control; some plants with male function became hermaphroditic (by producing female flowers) under better growing conditions in the field and in the greenhouse. There was some spatial segregation of the sexes. Because of sex lability, more hermaphrodites than males occurred on moister slopes. Although there were not measurable sex‐related differences in mortality within or between two flowering seasons, more females than males and hermaphrodites occurred at the bottom of slopes. Males and females produced the same number of ramets and inflorescences, but females had a greater number of flowers per inflorescence. Males and females had the same number of ovules (vestigial in males), but females had larger ovules and longer stigmas. Hermaphrodites and males had the same amount of pollen per flower despite the production of fruit by the hermaphrodites. In hermaphrodites, there was no apparent tradeoff within flowers between pollen production and ovule production. These results indicate that spatial segregation, sex lability, and environmental conditions influence allocation patterns of S. globosa, and in combination with high inbreeding depression and selling rates, may promote the further evolution of dioecy in S. globosa.