Floral development and vasculature in Eriocaulon (Eriocaulaceae) provide insights into the evolution of Poales

Background and AimsFloral developmental studies are crucial for understanding the evolution of floral structures and sexual systems in angiosperms. Within the monocot order Poales, both subfamilies of Eriocaulaceae have unisexual flowers bearing unusual nectaries. Few previous studies have investigated floral development in subfamily Eriocauloideae, which includes the large, diverse and widespread genus Eriocaulon. To understand floral variation and the evolution of the androecium, gynoecium and floral nectaries of Eriocaulaceae, we analysed floral development and vasculature in Eriocaulon and compared it with that of subfamily Paepalanthoideae and the related family Xyridaceae in a phylogenetic context.MethodsThirteen species of Eriocaulon were studied. Developmental analysis was carried out using scanning electron microscopy, and vasculature analysis was carried out using light microscopy. Fresh material was also analysed using scanning electron microscopy with a cryo function. Character evolution was reconstructed over well-resolved phylogenies.Key ResultsPerianth reductions can occur due to delayed development that can also result in loss of the vascular bundles of the median sepals. Nectariferous petal glands cease development and remain vestigial in some species. In staminate flowers, the inner stamens can emerge before the outer ones, and carpels are transformed into nectariferous carpellodes. In pistillate flowers, stamens are reduced to staminodes and the gynoecium has dorsal stigmas.ConclusionsFloral morphology is highly diverse in Eriocaulon, as a result of fusion, reduction or loss of perianth parts. The nectariferous carpellodes of staminate flowers originated first in the ancestor of Eriocaulaceae; petal glands and nectariferous branches of pistillate flowers originated independently in Eriocaulaceae through transfer of function. We present a hypothesis of floral evolution for the family, illustrating a shift from bisexuality to unisexuality and the evolution of nectaries in a complex monocot family, which can contribute to future studies on reproductive biology and floral evolution in other groups.     

Flower structure and potential bisexuality in Freycinetia reineckei (Pandanaceae), a species of the Samoa Islands

In Freycinetia reineckei the staminate flower (on the staminate spikes) comprises 3 or 4 (sometimes 2) stamens and a pistillode with 2 (sometimes 4) carpellodes, and the pistillate flower (on the pistillate spikes) is formed of a pistil with 2 (sometimes 4) carpels and of 3 or 4 (sometimes 2) staminodes. This perfect floral homology, also observed in all the other species that were studied with both pistillate and staminate material, strongly suggests that the flower of Freycinetia is basically and potentially bisexual, and may explain the occasional sexual lability and bisexuality of that flower (occurrence of both pistillate and staminate inflorescences, and/or of bisexual inflorescences with bisexual flowers and/or unisexual flowers, on the same individuals) in some species, and also the frequent occurrence of bisexual spikes in this species. These may be partitioned into pistillate, staminate, mixed and sterile zones. In the pistillate zones the flowers have the same aspect and structure as the pistillate flowers. In the staminate zones the flowers generally comprise 3 or 4 (sometimes 2) stamens and a ‘semi-pistil’ some have both stamens and staminodes. The semi-pistils are intermediate between pistils and pistillodes in length, aspect and structure, but always have placentas and ovules. In the mixed zones the flowers are generally formed of a pistil and 3 or 4 (sometimes 2) stamens, and are therefore true hermaphrodite flowers; some have both stamens and staminodes. In the sterile zones the flowers comprise a semi-pistil and 3 or 4 (sometimes 2) staminodes. The staminodes are anatomically very similar to the stamens, especially in the staminate, mixed, and sterile zones, in which they exhibit a wide range of variation in length, aspect and structure. The perfect floral homology as generic character on one hand, and the occasional bisexuality both with and without bisexual flowers and other aspects of sex expression (e.g. occurrence of both pistillate and staminate shoots on the same individuals) in some species on the other hand, seem to indicate that Freycinetia is a basically monoecious, sex changing genus.     

Morphology, development and homologies of the perianth and floral nectaries in Croton and Astraea (Euphorbiaceae-Malpighiales)

New observations are presented on the ontogeny, vasculature and morphology of both staminate and pistillate flowers of Croton and Astraea. These data support earlier hypotheses that the filamentous structures in pistillate flowers represent reduced and transformed petals. Staminate flowers of both genera possess five free nectaries, which are vascularised by divergences of the sepal traces in Croton and unvascularised in Astraea. In pistillate flowers, there are five separate non-vascularised nectaries in Astraea, but in Croton there is a single nectariferous disk that is vascularised by divergences of the sepal traces. The nectaries are initiated late in floral development, but their location indicates that they could represent the outer stamen whorl transformed into secretory staminodes. Other glandular structures occur in pistillate flowers of most Croton species, resulting in flowers with two secretory organ whorls. In these cases, the inner whorl is formed by modified staminodes. Our observations support the recent segregation of Astraea species from the larger genus Croton. Despite strong similarities between the two genera, there are clear structural differences, including the presence of colleters in Astraea (absent in Croton), moniliform trichomes on petals (rather than simple trichomes in Croton), non-vascularised nectaries (vascularised in Croton) and reduced, non-secretory filamentous structures (well developed and secretory in Croton).     

Floral ontogeny and vasculature in Xyridaceae,with particular reference to staminodes and stylar appendages

We provide a detailed comparative study of floral ontogeny and vasculature in Xyridaceae, including Xyris, Abolboda and Orectanthe. We evaluate these data in the context of a recent well-resolved phylogenetic analysis of Poales to compare floral structures within the xyrid clade (Xyridaceae and Eriocaulaceae). Xyrids are relatively diverse in both flower structure and anatomy; many species incorporate diverse and unusual floral structures such as staminodes and stylar appendages. Xyridaceae possess three generally epipetalous stamens in a single whorl; the “missing” stamen whorl is either entirely absent or transformed into staminodes. Fertile stamens each receive a single vascular bundle diverged from the median petal bundle. In Xyris, the stamen bundle diverges at the flower base, but it diverges at upper flower levels in both Abolboda and Orectanthe. In species of Abolboda that possess staminodes, staminode vasculature is closely associated with the lateral vasculature of each petal. Despite the likely sister-group relationship between Eriocaulaceae and Xyridaceae, our character optimization indicates that the stylar appendages that characterize some Xyridaceae (except Xyris and Achlyphila) are non-homologous with those of some Eriocaulaceae. On the other hand, it remains equivocal whether the loss of a fertile outer androecial whorl occurred more than once during the evolutionary history of the xyrid clade; this transition occurred either once followed by a reversal to fertile stamens in Eriocauloideae and staminodes in some Xyridaceae, or twice independently within both Xyridaceae and Eriocaulaceae.     

单性木兰（木兰科）花的形态发生

报道了单性木兰(Kmeria septentrionalis Dandy)花的形态发生过程。发现过去一直被认为是雌花条状披针形的“内轮花被片”,实际为退化雄蕊,它形态发生的时间与位置均与雄花的雄蕊相同,在成熟结构中仍可见药室残迹,说明单性木兰的雌性花是由两性花退化而来。通过与K. duperreana(Pierre) Dandy和Magnolia thailandica Noot. &; Chalermglin雌花的比较,发现它们雌花的形态相同,从而得知人们长期以来对此3种植物雌花的认识有误,原一直认为的“内轮花被片”实为退化雄蕊。     

INFLORESCENCE AND FLOWER STRUCTURE IN NYPA FRUTICANS (PALMAE)

Details of organogenesis, anatomy, and some aspects of histogenesis are described for the inflorescence units and flowers of the mangrove palm, Nypa fruticans. The genus is of special interest in evolutionary studies because of its disjunct morphology and substantial fossil record. The inflorescence is an erect monopodial axis bearing 7–9 lateral branches and ending in a pistillate head. The lowest of the lateral branches bears up to six orders of branches, the next ones progressively fewer, and the uppermost is usually unbranched. Lateral branches of all orders end in thick spicate, staminate rachillae. The rachillae and the pistillate head consist of spirally inserted sessile flowers, each borne in the axil of a bract. Staminate and pistillate flowers are similar in structure. Both have three separate sepals and three separate petals, which are loosely closed in bud. Staminate flowers have no pistillodes; nor are there any staminodes in the pistillate flower. The androecium consists of a stalk bearing three anthers distally and is shown to represent three stamens with filaments congenitally fused and anthers connate by the ventral faces of the connectives. The pistillate flower has three separate carpels, which expand rapidly so that by anthesis they much exceed the perianth. Each carpel is cupulate in shape, with a two-crested distal opening, and receives ca. 150 vascular bundles, many of which may branch dichotomously. No dorsal or ventral bundles can be definitely distinguished, but a ventrally open ring of 10–12 bundles surrounding the locule matures first. Allometric growth clearly accounts for much of the morphological disjunction in the reproductive organs of Nypa contrasted with those of other palms. Resemblances to coryphoid, ceroxyloid, arecoid, and cocosoid palms are indicated by these studies. Different combinations of characters and several distinctive features justify a separate major taxonomic category for this genus within the Palmae.     

Flower morphology and biology of Myrsine laetevirens, structural and evolutionary implications of anemophily in Myrsinaceae

This study deals with the phenology, pollination biology and floral morphology of Myrsine laetevirens , a neotropical dioecious tree. In Punta Lara (Argentina), its flowering period occurs during January-February. Both pistillate and staminate flowers are small, with a yellowish-green perianth and produce neither nectar nor odour. Staminate flowers have five stamens and a vestigial gynoecium while pistillate flowers, have non-functional anthers and a conspicuous stigma. The floral characteristics of staminate and pistillate plants are related to the syndrome of anemophily. Fruit set in inflorescences covered with mesh bags and observations prove that animals are not involved in the pollination process. A provisional cladistic analysis of Myrsinaceae shows that dioecy evolved as one of the most recent apomorphies of Myrsine and is part of the anemophilous syndrome.     

Reproductive structures of an extinct platanoid from the early Cretaceous (latest Albian) of eastern North America

Two new species of platanoid reproductive structure are described from the Bull Mountain locality in the Patapsco Formation (Potomac Group) of northeastern Maryland, USA. Pistillate inflorescences and infructescences (Platanocarpus elkneckensis sp. nov.) consist of flowers and fruits in sessile globose heads that are borne on an elongate axis. Individual pistillate flowers consist of five free carpels surrounded by prominent tepals. Staminate inflorescences, flowers and isolated stamens are assigned to Hamatia elkneckensis gen. et sp. nov. Staminate flowers are borne in a globose head with a small number of stamens (five?) per flower. Stamens consist of very short filaments, long anthers with strongly valvate dehiscence and an apically expanded connective. The connective expansion is frequently very well-developed, hook-like and extends down the ventral surface of the stamen. Anthers contain small, tricolporate, reticulate pollen. Association evidence, similarity of inflorescence structure and the occurrence of Hamatia-type pollen on flowers, carpels and fruits of Platanocarpus elkneckensis suggests that the staminate and pistillate material was produced by a single species of plant. The “Hamatia-plant” provides further evidence of pentamerous floral structure in mid-Cretaceous platanoids and documents the occurrence of unequivocal tricolporate pollen in the platanoid complex.     

Reproductive biology of Echinodorus longipetalus (Alismataceae): Sexual morphs,breeding system and pollinators

The floral biology, pollinators and breeding system of Echinodorus longipetalus Micheli were studied in a marshy area of the district of Taquaritinga (State of São Paulo), southeastern Brazil. E. longipetalus is gynodioecious and as far as is known, this is the first record of unisexual flowers, besides perfect flowers, in Echinodorus. Proportion of female individuals in the studied population is 50% and produces 31% more flowers than hermaphrodites. Perfect and pistillate flowers of E. longipetalus are similar in appearance and are pollinated by several species of Hymenoptera (mainly by Xylocopa (Neoxylocopa) suspecta Moure & Camargo). Perfect flowers offer pollen as a reward. Pistillate flowers attract floral visitors by deceit with their staminodes that resemble the stamens of the perfect flowers. Visits to pistillate flowers are quick (1–2 s), while visits to perfect flowers last up to 120 s. The perfect flowers are self-compatible and produce fruits through spontaneous self-pollination (control flowers), whereas the pistillate ones only set fruits through cross-pollinations. Perfect and pistillate flowers set more fruits under natural conditions than in manual treatments, respectively. Although the pistillate and perfect flowers bear a strong similarity, the selective pollinator behavior seems to be responsible for the increase of fruit set in perfect flowers.     

Floral Morphology and Relationships of Clusia gundlachii with a Discussion of Floral Organ Identity and Diversity in the Genus Clusia

The genus Clusia L. is highly variable in many floral features. Several Clusia species have floral organs of mixed or uncertain identity, such as organs that are transitional between bracteoles and sepals, petaloid sepals, and partly petaloid stamen rings. Unique in Clusia is the "corona" of Clusia gundlachii Stahl, a thick, urn-shaped structure that is initiated as a ring primordium. In male flowers it surrounds a synandrium, and in female flowers it surrounds the ovary and a row of staminodes. The corona combines features typical of both petals and stamens of other Clusia species. It is hypothesized that this corona may be the result of the altered expression patterns of the genes that determine floral organ identity. Clusia gundlachii has many floral features in common with two small genera that are sometimes included in Clusia: Havetiopsis and Oedematopus. These genera have four thick connivent petals. Their apparent close relationship makes it seem likely that the corona of C. gundlachii evolved via congenital fusion of such petals. The corona is also somewhat similar to the staminodial rings present in many Clusia species, but taxa in which such organs occur show little similarity to C. gundlachii in terms of other floral characters.     

Study of homeosis in the flower of Philodendron (araceae): a qualitative and quantitative approach

This study deals specifically with floral organogenesis and the development of the inflorescence of Philodendron squamiferum and P. pedatum. Pistillate flowers are initiated on the lower portion of the inflorescence and staminate flowers are initiated on the distal portion. An intermediate zone consisting of sterile male flowers and atypical bisexual flowers with fused or free carpels and staminodes is also present. This zone is located between the sterile male and female floral zones. In general, the portion of bisexual flowers facing the male zone forms staminodes, and the portion facing the female zone develops an incomplete gynoecium with few carpels. The incomplete separation of some staminodes from the gynoecial portion of the whorl shows that they belong to the same whorl as the carpels. There are two levels of aberrant floral structures in Philodendron: The first one is represented by the presence of atypical bisexual flowers, which are intermediates between typical female flowers and typical sterile male flowers. The second one is the presence of intermediate structures between typical carpels and typical staminodes on a single atypical bisexual flower. The atypical bisexual flowers of P. squamiferum and P. pedatum are believed to be a case of homeosis where carpels have been replaced by sterile stamens on the same whorl. A quantitative analysis indicates that in both species, on average, one staminode replaces one carpel.     

Reproductive biology of Echinodorus longipetalus (Alismataceae): Sexual morphs,breeding system and pollinators

The floral biology, pollinators and breeding system of Echinodorus longipetalus Micheli were studied in a marshy area of the district of Taquaritinga (State of São Paulo), southeastern Brazil. E. longipetalus is gynodioecious and as far as is known, this is the first record of unisexual flowers, besides perfect flowers, in Echinodorus. Proportion of female individuals in the studied population is 50% and produces 31% more flowers than hermaphrodites. Perfect and pistillate flowers of E. longipetalus are similar in appearance and are pollinated by several species of Hymenoptera (mainly by Xylocopa (Neoxylocopa) suspecta Moure & Camargo). Perfect flowers offer pollen as a reward. Pistillate flowers attract floral visitors by deceit with their staminodes that resemble the stamens of the perfect flowers. Visits to pistillate flowers are quick (1–2 s), while visits to perfect flowers last up to 120 s. The perfect flowers are self-compatible and produce fruits through spontaneous self-pollination (control flowers), whereas the pistillate ones only set fruits through cross-pollinations. Perfect and pistillate flowers set more fruits under natural conditions than in manual treatments, respectively. Although the pistillate and perfect flowers bear a strong similarity, the selective pollinator behavior seems to be responsible for the increase of fruit set in perfect flowers.     

CENTRIFUGAL STAMEN INITIATION IN PHYTELEPHANTOID PALMS

The phytelephantoid group, considered very highly specialized among the 15 major groups of palms, includes only three dioecious genera which are distinguished by multipartite flowers. Staminate flowers of these genera have from 120 to over 900 stamens, the largest number known in palms. Developmental material shows centrifugal inception of stamens in Palandra and Phytelephas, and the course of the trunk bundles indicates centrifugal initiation of stamens in Ammandra. Stamens of all three genera are supplied by large trunk bundles that develop acropetally following the different centrifugal expansion of the floral apex in each genus. Branches of the trunk bundles form later to supply stamen primordia as they develop. Polyandric androecia occur in ten of the major groups of palms. Other multistaminate genera show expansion and change in shape of the floral apex before stamen initiation. Centrifugal development appears to represent a different method of expansion of the floral apex to accommodate increase in stamen number in this group. Centrifugal inception of stamens in monocotyledons has previously been established only for two genera of Butomaceae.     

Scent emissions and floral nutrients of Carludovicoideae (Cyclanthaceae) and their importance for associated beetles

To better understand the complex pollination biology of Carludovicoideae (Cyclanthaceae), four species from French Guiana were investigated in both the field and laboratory. The pistillate flowers of all species of the subfamily have long staminodes up to 10 cm long or more, which emit scent and apparently attract beetles during anthesis. Scent was collected by standard headspace methods and analyzed in the laboratory by GC/MS. The histology of staminodes, measurements of inflorescence temperatures, and analyses of the floral nutrients were performed. The staminodes have two ducts with a mucilage-like liquid containing sugar, which provides nourishment for beetle visitors. In Evodianthus funifer, four of the six beetle morphospecies (Curculionidae: Acalyptini) were pollinators and oviposited in staminate flowers. The remaining pair of morphospecies were non-pollinators, and avoided entering the inflorescence, while only cutting the staminodes for possible oviposition on the ground. Staminate flowers and staminodes have a high energy content, providing for larval development of the beetles. Our findings revealed that the staminodes released aromatic components, miscellaneous cyclic components, and terpenoids. Some of the major scent compounds of E. funifer and Ludovia lancifolia, i.e., (E,E)-α-farnesene-2(3),9(10)-diepoxid and 3-methylen-2-(pent-2(Z)-enyl)-cyclopentanol, are new to science. Also, Carludovicoideae are a subfamily of plants that attract beetle pollinators through highly specific scent compounds, making them comparable to species of Araceae, Magnoliaceae, and Annonaceae.     

The occurrence and structure of apparently bisexual flowers in the date palm, Phoenix dactylifera L. (Arecaceae)

Individuals of Phoenix dactylifera L. have expanded pistillodes or pseudocarpels in staminate flowers. These pseudocarpels are located in the centre of the male flowers and are surrounded by stamens. The gynoecium has the characteristic three carpellate arrangement commonly found in female date palm flowers. Pseudocarpels from male flower buds can expand into parthenocarpic fruit. Histology of the expanded pistillodes or pseudotarpels is similar to that of normal carpels from pistillate plants. These pseudocarpels lack ovules. Nutrient medium containing 10 mg 1^-1 of 2,4-dichlorophenoxyacetic acid or p-chlorophenylacetic acid and 0.3% activated neutralized charcoal enhanced the development and outgrowth of the pseudocarpels of cultured male flowers.     

Fossil floral structures of a basal angiosperm with monocolpate,reticulate-acolumellate pollen from the Early Cretaceous of Portugal

Distinctive monocolpate and reticulate-acolumellate pollen grains with a coarse, loosely attached reticulum have long been known as a conspicuous element of many palynological assemblages from the Early and mid-Cretaceous. These grains are now described in situ in staminate structures and on the surface of pistillate organs from two Early Cretaceous (Barremian or Aptian) mesofloras from Portugal (Vale de Agua and Buarcos). Staminate organs include a staminate axis with spirally arranged stamens and many isolated stamens. Stamens consist of a short filament, a dithecate, tetrasporangiate anther, and a short apical extension of the connective. Anther dehiscence is extrorse by longitudinal slits and in situ pollen is monocolpate, semi-tectate with a coarse, loosely attached reticulum composed of narrow muri with a spiny ornamentation. The infratectal layer of the pollen wall is thin, granular, and lacking columellae; and the foot layer is distinct. The endexine is thin, except under the aperture where it is thick. The pistillate organs are minute consisting of a simple unilocular ovary containing a single thin-walled seed. Associated with staminate and pistillate structures are many coprolites consisting almost exclusively of pollen grains of this distinctive type. The staminate and pistillate organs are not found in organic connection, and two new genera are established to accommodate the new floral structures: Pennistemon comprising the staminate structures and Pennicarpus comprising the pistillate structures. A new genus, Pennipollis, is also established for the dispersed grains, based on the type species Peromonolites peroreticulatus Brenner, since no appropriate genus has yet been described for these acolumellate grains. Features of the pollen grains strongly indicate affinity with members of the Alismatales and characters of the mesofossils also support this assignment. This is the first record of putative monocots in the early Cretaceous based on combined pollen and floral features.     

Influence of plant domestication on plant-pollinator interactions: Floral attributes and floral visitor communities in wild and cultivated squash plants

Premise

Domestication of plant species results in phenotypic modifications and changes in biotic interactions. Most studies have compared antagonistic plant-herbivore interactions of domesticated plants and their wild relatives, but little attention has been given to how domestication influences plant-pollinator interactions. Floral attributes and interactions of floral visitors were compared between sister taxa of the genus Cucurbita (Cucurbitaceae), the domesticated C. moschata, C. argyrosperma ssp. argyrosperma and its wild progenitor C. argyrosperma ssp. sororia in the place of origin.

Methods

We conducted univariate and multivariate analyses to compare floral morphological traits and analyzed floral reward (nectar and pollen) quantity and quality between flowers of wild and domesticated Cucurbita taxa. Staminate and pistillate flowers of all three taxa were video recorded, and visitation and behavior of floral visitors were registered and analyzed.

Results

Most floral morphological characteristics of flowers of domesticated taxa were larger in both staminate and pistillate flowers. Staminate and pistillate flowers presented distinct correlations between floral traits and integration indices between domesticated and wild species. Additionally, pollen quantity and protein to lipid ratio were greater in domesticated species. Cucurbit pollen specialists, Eucera spp., had the highest probability of visit for all Cucurbita taxa.

Conclusions

We provide evidence that floral traits of domesticated and wild Cucurbita species experienced different selection pressures. Domesticated Cucurbita species may have more resources invested towards floral traits, thereby increasing attractiveness to pollinators and potentially plant reproductive success. Wild ancestor plant populations should be conserved in their centers of origin to preserve plant-pollinator interactions.     

Functional Monoecy Due to Delayed Anther Dehiscence: A Novel Mechanism in Pseuduvaria mulgraveana (Annonaceae)

Unlike most genera in the early-divergent angiosperm family Annonaceae, Pseuduvaria exhibits a diversity of floral sex expression. Most species are structurally andromonoecious (or possibly androdioecious), although the hermaphroditic flowers have been inferred to be functionally pistillate, with sterile staminodes. Pseuduvaria presents an ideal model for investigating the evolution of floral sex in early-divergent angiosperms, although detailed empirical studies are currently lacking. The phenology and pollination ecology of the Australian endemic species Pseuduvaria mulgraveana are studied in detail, including evaluations of floral scent chemistry, pollen viability, and floral visitors. Results showed that the flowers are pollinated by small diurnal nitidulid beetles and are protogynous. Pollen from both hermaphroditic and staminate flowers are shown to be equally viable. The structurally hermaphroditic flowers are nevertheless functionally pistillate as anther dehiscence is delayed until after petal abscission and hence after the departure of pollinators. This mechanism to achieve functional unisexuality of flowers has not previously been reported in angiosperms. It is known that protogyny is widespread amongst early-divergent angiosperms, including the Annonaceae, and is effective in preventing autogamy. Delayed anther dehiscence represents a further elaboration of this, and is effective in preventing geitonogamy since very few sexually mature flowers occur simultaneously in an individual. We highlight the necessity for field-based empirical interpretations of functional floral sex expression prior to evaluations of evolutionary processes.     

The evolution of staminodes in angiosperms: patterns of stamen reduction, loss, and functional re-invention

Stamens that have lost their primary function of pollen production, or staminodes, occur uncommonly within angiosperms, but frequently fulfill important secondary floral functions. The phylogenetic distribution of staminodes suggests that they typically arise during evolutionary reduction of the androecium. Differences in the genetic control and patterns of stamen loss between actinomorphic and zygomorphic flowers shape staminode development. In clades with actinomorphic flowers, staminodes generally replace an entire stamen whorl and staminode loss seems irreversible. In contrast, in clades with zygomorphic flowers staminodes evolve from a subset of the stamens in a whorl and staminodes can reappear in a lineage after being lost (e.g., Cheloneae, Scrophulariaceae). If staminodes do not adopt new functions during androecium reduction they are lost quickly, so that nonfunctional staminodes appear only in recently derived taxa. Alternatively, when staminodes assume new floral roles, either directly or indirectly after a nonfunctional period, they can become integral floral components which perpetuate within clades (e.g., Orchidaceae). Indirect evolution of staminode function allows greater flexibility of function by allowing staminodes to take over roles not performed by stamens, such as involvement in mechanisms to prevent self-pollination and mechanisms of explosive pollination. Multifunctional staminodes characterize lineages with universal or widespread staminodes.     

Floral development of dioecious species and trends of floral evolution in Piper sensu lato

The initiation of the floral parts (mainly stamens and carpels) is described for the four dioecious species of Piper: Piper polysyphorum C. DC, P. bavinum C. DC., P. pedicellatum C. DC., P. pubicatulum C. DC. The initiation order resembles that in the perfect flowers of some species, such as P. amalago. The carpels are initiated simultaneously, in most cases, as three primordia. In P. polysyphorum , carpel tips split into two lobes, so that finally a four- or five-lobed stigma will be formed when the ovary is fully developed. The staminodes (exactly, staminodial primordia) in the female flowers are initiated in the same order as the stamens in the male flowers and remain until the ovaries are enclosed. The unisexual flowers have stamens reduced to three or two. The reduction of stamen or staminode (staminodial primordium) number is accompanied by the change of their positions from opposite the carpels to alternate. After the initiation of the staminodes, or, exactly staminodial primordia, in the female flowers, the central part of the floral apex forms a ring meristem which is triangular. The carpel primordia (often three) are initiated on the three points of the ring meristem. The evolutionary trends of the flowers of Piper sensu lato are discussed.