Flower Morphs Research Articles

Chloroplast phylogeography of threatened aquatic Oxalis (Oxalidaceae): significant inter-population structure, divergent haplotypes and conservation implications

The aquatic lineage consisting of the sister taxa Oxalis dines and O. disticha is confined to a few small vernal pools in the semi-arid Greater Cape Floristic Region of South Africa. All known populations are at risk of extinction due to anthropogenically induced disturbance. To identify priority sites for focused conservation management, the chloroplast intergenic spacer regions psbA-trnH and trnS-trnG were used to determine population structure and genetic diversity in this lineage across its distribution range. Population viability was assessed using flower morph ratios as surrogate for sexual health. Fourteen and four haplotypes were identified from O. disticha and O. dines populations, respectively. Analyses of Molecular Variance indicated an extremely high level of interpopulation differentiation across the entire aquatic lineage as well as within O. disticha and O. dines. Fifty percent of the eighteen haplotypes were confined to single pools, and 84% of populations contained only a single haplotype, even though pool interspacing distance for O. disticha was often less than 5 km. Almost half of O. disticha haplotype diversity was restricted to very small populations. Two O. dines haplotypes were restricted to small populations, with one of these presenting a divergent haplotype sister to the remainder of the aquatic lineage. Flower morph frequency ratio analyses suggested that most populations were reproductively healthy. Low haplotypic diversity within local populations and differentiation between populations are consistent with very low seed-level gene flow and sporadic founder effects. Conservation efforts should be focussed on preserving as many pools as possible with small, genetically distinct populations representing a main concern.

Unusual heterostyly: style dimorphism and self-incompatibility are not tightly associated in Lithodora and Glandora (Boraginaceae).

Heterostyly is a floral polymorphism characterized by the reciprocal position of stamens and stigmas in different flower morphs in a population. This reciprocal herkogamy is usually associated with an incompatibility system that prevents selfing and intra-morph fertilization, termed a heteromorphic incompatibility system. In different evolutionary models explaining heterostyly, it has been alternately argued that heteromorphic incompatibility either preceded or followed the evolution of reciprocal herkogamy. In some models, reciprocal herkogamy and incompatibility have been hypothesized to be linked together during the evolution of the heterostylous system. We examine the incompatibility systems in species with different stylar polymorphisms from the genera Lithodora and Glandora (Boraginaceae). We then test whether evolution towards reciprocal herkogamy is associated with the acquisition of incompatibility. To this end, a phylogeny of these genera and related species is reconstructed and the morphological and reproductive changes that occurred during the course of evolution are assessed. Both self-compatibility and self-incompatibility are found within the studied genera, along with different degrees of intra-morph compatibility. We report for the first time extensive variability among members of the genus Glandora and related species in terms of the presence or absence of intraspecies polymorphism and heteromorphic incompatibility. Overall, our results do not support a tight link between floral polymorphism and incompatibility systems. The independent evolution of stylar polymorphism and incompatibility appears to have occurred in this group of plants. This refutes the canonical view that there is strong linkage between these reproductive traits.

Difference in Floral Traits, Pollination, and Reproductive Success between White and Blue Flowers of Gentiana leucomelaena (Gentianaceae) in an Alpine Meadow

The blue-white gentian, Gentiana leucomelaena (Gentianaceae), bears two colors of flowers (blue and white) within populations and on individual plants. We tested the hypothesis that these flower morphs have different mating systems associated with differences in pollinator species and visitation rates. This hypothesis was driven by the fact that colorful flowers are often more likely to be pollinated by diverse animal pollinators, and by the observation that white G. leucomelaena flowers always blossom earlier than blue ones in early spring, when few pollinators are available. This hypothesis was investigated by determining the pollination success, daily duration of flower opening, flower life span, the number of pollen grains and ovules per flower, pollinator visitation rates, and seed output for both color morphs during the flowering season of 2009. Hand-pollination and pollinator-exclusion experiments were also conducted to determine whether the two color morphs differed in their ability to self-pollinate. In general, blue flowers were found to have a trait combination that favors a significantly higher degree of pollinator specificity and cross fertilization, whereas white flowers were characterized as pollinator generalists and self-fertilizing. We speculate that the difference in the floral structure and function between blue and white flowers and their coexistence are likely adaptive in unpredictable and often pollinator-limited environments such as those found in the alpine meadows of the Qinghai-Tibet Plateau.

Flower Development and the Evolution of Self-fertilization in Amsinckia: The Role of Heterochrony

We studied the development of 26 flower traits under natural conditions in three clades of the genus Amsinckia (Boraginaceae). Each clade contained both a derived highly self-fertilizing taxon and an ancestral more highly outcrossing taxon. The more outcrossing taxa contained two flower morphs—pins and thrums—with opposite positioning of the sex organs (heterostyly). The highly selfing taxa had smaller flowers with sex organs in close proximity (homostyly). Growth trajectories were quantified over the entire or nearly the entire period from primordium initiation to flower opening. These trajectories were compared in the heterochronic framework and, in contrast with previous studies, character size was tracked over time rather than relative to another character. We focused on three hypotheses: (1) The distinct developmental trajectories leading to pins and thrums should be similar in all clades, while the trajectories leading to homostylous flowers might differ among clades. This was supported. Specifically, contrasting growth rates of stamen and pistil heights in heterostylous flowers caused pin and thrum flowers to have the reciprocal arrangement of anther and stigma heights. From the viewpoint of heterochrony, the decreased size (paedomorphosis) of the homostylous morph, compared to pins and thrums, resulted from decreased growth rate (neoteny) and earlier offset (progenesis) in all clades. Nevertheless, multiple heterochronic processes were involved in the mosaic development and evolution of homostylous flowers. (2) We tested the hypothesis that small, self-fertilizing flowers have reduced development times, one of the proposed selective advantages of increased self-fertilization rates. We found in contrast that developmental duration of homostylous flowers was either the same (two clades) or longer (one clade) compared to duration of pins and thrums. (3) Finally, we tested von Baer’s Law, which proposes that developmental differences among closely related taxa should arise later in development than differences among more distantly related taxa. Von Baer’s Law was supported strongly among homostyles, moderately among thrums and weakly among pins.

Floral formulae updated for routine inclusion in formal taxonomic descriptions

AbstractBuilding on two centuries of history, we advocate an expanded and maximally informative format for floral formulae to describe angiosperm flowers in formal taxonomic descriptions. Using standard typeface and Unicode character codes, the format can summarise a wide range of features, including: acropetal sequence of organ initiation, number and symmetry of each whorl of floral organs (bracts, sepals, petals [or tepals], androecium, gynoecium, ovules), position of the organs relative to each other, partial and/or complete fusion of organs, resupination, organ loss and suppression, and deviations from standard bisexuality. We use several complex flowers to demonstrate our view that all known flower morphs can be accurately represented by the updated format, and show how use of floral formulae can outline some unanswered questions regarding the floral organisation of the model organism Arabidopsis. Possible uses of floral formulae extend beyond static description of mature morphology into the comparative realm. When combined with phylogenies, they help to elucidate generalised groundplans, plesiomorphic architecture, and the location and polarity of particular character‐state transitions. They can usefully be applied within as well as between species, to compare wildtype versus mutant morphs and different ontogenetic stages. Perhaps their greatest strengths are that they (1) require only a universally available typescript, and (2) bring a comprehensive uniformity to the description of flowers, acting as a checklist of features to be examined. We recommend that floral formulae become a routine component of diagnoses in protologues and other formal taxonomic (re)descriptions, functioning as a logical phenotypic counterpart to the DNA barcode.

A search of Brassica SI-involved orthologs in buckwheat leads to novel buckwheat sequence identification: MLPK possibly involved in SI response

Self-incompatibility (SI) systems, gamethophytic (GSI) and sporophytic (SSI), prevent self-pollination in angiosperms. Buckwheat displays heteromorphic SSI, with pollination allowed only between different flower morphs - thrum and pin. The physiology of thrum and pin morph SI responses are entirely different, resembling homomorphic Brassica SSI and Prunus GSI responses, respectively. Considering angiosperm species may share ancestral SI genes, we examined the presence of Brassica and Prunus SI-involved gene orthologs in the buckwheat genome. We did not find evidence of SRK, SLG and SP11 Brassica or S-RNase and SFB Prunus orthologs in the buckwheat genome, but we found a Brassica MLPK ortholog. We report the partial nucleotide sequence of the buckwheat MLPK and discuss the possible implications of this finding.

Microsporogenesis and microgametogenesis of Cardiospermum grandiflorum and Urvillea chacoensis (Sapindaceae, Paullinieae)

Microsporogenesis and microgametogenesis of two species, Cardiospermum grandiflorum Sw. and Urvillea chacoensis Hunz. (Sapindaceae, Paullinieae), were studied using light and transmission electron microscopy. Both species are monoecious, with staminate and hermaphrodite, although functionally pistillate, flowers. A comparative pollen-development study of these two floral morphs is reported. For the present study, five stages of pollen ontogeny were identified. The development of the anther wall is of basic type. Its wall consists of epidermis, endothecium, two middle layers and a uninucleate secretory tapetum. The microspore tetrads are tetrahedral. The mature anther in staminate flowers presents the endothecium with well developed fibrillar thickenings, remains of tapetal cells, a single locule formed in the theca by dissolution of the septum before anther dehiscence and two-celled pollen grains when shed. In functionally pistillate flowers, the mature anthers present remnants of the middle layers, tapetal cells without signs of degradation, the theca with two locules and pollen grains uni- or bicellular, some of them with the cytoplasm collapsed. These anthers are not dehiscent. It can be concluded that male sterility is characterised by failure to produce functional pollen grains, an event that would be associated with the persistence of tapetal cells. Ultrastructural analysis clearly shows the difference in tapetal cells between the two flower morphs.

Origin of the disjunct distribution of flower colour polymorphism within Limonium wrightii (Plumbaginaceae) in the Ryukyu Archipelago

The sea lavender, Limonium wrightii, has six morphs of flower colour variation. The geographical distribution of flower colour morphs is disjunct; the distribution of the pink flower morph is divided into two subregions, and that of the yellow flower morph intervenes between them. The present study aimed to examine the origin of this apparent distribution pattern of flower colour in L. wrightii. Two main hypotheses (i.e. past dispersal events and phenotypic changes by natural selection and/or stochastic processes) have been proposed to account for the origin of leapfrog distribution patterns. To determine which hypothesis was applicable, we conducted a molecular phylogenetic analysis using sequence variation in chloroplast DNA (three regions of intergenic spacers, trnG-trnfM, trnV-trnM, and psbA-trnH). We sequenced 58 accessions of L. wrightii frin 28 islands in the Ryukyu Archipelago and the Izu-Ogasawara Islands, located south of the Japanese mainland, and 12 accessions of four congeneric species. Within L. wrightii, we obtained four lineages of ten haplotypes. These lineages and haplotypes did not correlate with the different flower colours. These results indicate that the formation processes of populations are complex. The haplotypes of the pink flower morph did not show a sister relationship between the two disjunct subregions, indicating that the disjunct populations of the pink flower morphs are unlikely to share the pink flower colour as a result of common ancestry. We conclude that the observed leapfrog distribution pattern is caused by natural selection and/or stochastic processes. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 97, 709–717.

Contribution of small insects to pollination of common buckwheat, a distylous crop

AbstractCrop pollination by animals is an essential ecosystem service. Among animal‐pollinated crops, distylous plants strongly depend on animal pollination. In distylous pollination systems, pollinator species are usually limited, although flowers of some distylous plants are visited by diverse animals. We studied the pollination biology of common buckwheat (Fagopyrum esculentum), a distylous crop mainly pollinated by honeybees and visited by many insect species, to evaluate the effects of non‐honeybee species on pollination services. We focused on insects smaller than honeybees to determine their contribution to pollination. We applied pollination treatments with bags of coarse mesh to exclude flower visits by honeybees and larger insects and compared the seed set of bagged plants with that of untreated plants for pin and thrum flower morphs. We found a great reduction of seed set only in bagged pin flowers. We also confirmed that small insects, including ants, bees, wasps and flies, carried pin‐morph pollen. These small insects transfer pollen from the short anthers of pin flowers to the short styles of thrum flowers, leading to sufficient seed set in thrum flowers. Consequently, small, non‐honeybee insects have the potential to maintain at least half of the yield of this honeybee‐dependent distylous crop.

An Examination of the Function of Male Flowers in an Andromonoecious Shrub Capparis spinosa

The pollen donor and pollinator attractor hypotheses are explanations for the functions of the male flowers of andromonoecious plants. We tested these two hypotheses in the andromonoecious shrub Capparis spinosa L. (Capparaceae) and confirmed that pollen production and cumulative volume and sugar concentration of nectar do not differ between male and perfect flowers. However, male flowers produced larger anthers, larger pollen grains and smaller ovaries than perfect flowers. Observations on pollinators indicated that two major pollinators (Xylocopa valga Gerst and Proxylocopa sinensis Wu) did not discriminate between flower morphs and that they transferred pollen grains a similar distance. However, there were more seeds per fruit following hand pollination with pollen from male flowers than from perfect flowers. Individuals of C. spinosa with a larger floral display (i.e. bearing more flowers) received more pollen grains on the stigma of perfect flowers. Female reproductive success probably is not limited by pollen. These results indicate that male flowers of C. spinosa save resources for female function and that they primarily serve to attract pollinators as pollen donors.

Comparative reproductive biology of Primula merrilliana Schltr. and P. cicutariifolia Pax

The reproductive biology of Primula merrilliana Schltr. and P. cicutariifolia Pax that are sister taxa and the only two members of Primula sect. Ranunculoides were studied. The results showed that P. merrilliana is typically a distylous species not only in morphology but also in function; it has an incompatibility system that restricts the legitimate pollination to that between pin and thrum flower morphs, but self-fertilization may occur under certain conditions. P. cicutariifolia is self-compatible. The pin morph of P. merrilliana has longer stigma papillae and smaller pollen than the thrum morph. The results stated above support the view that P. filchnerae should be moved from sect. Pinnatae to sect. Auganthus.

The structure of the stigma and the style of Oxalis spp. (Oxalidaceae)1

The anatomy of the stigma and style of three species of Oxalis (O. articulata, O. hispidula, and O. paludosa), belonging to different sections (Articulatae, Ionoxalis, and Corniculatae) was studied using light, scanning, and transmission electron microscopy. The stigma morphology of each of the different flower morphs of the three species (longistylous, medistylous, and brevistylous flowers) was compared in this work. The stigma is dry and has multicellular and multiseriate papillae. The morphology of the papillae does not differ between flower morphs. According to the Ca2+ concentration in pre-anthesis, anthesis, and post-anthesis, we hypothesize that the stigmas of the different morphs are equally receptive. Oxalis style is solid type. The cytoplasm of the transmitting tissue cells is dense with few vacuoles and abundant organelles. The transmitting tissue cells have large amounts of intercellular substance, mainly at the corners. This substance has moderate electron density in the species O. articulata and O. hispidula and shows some laxer areas in O. paludosa. The transmitting cell wall of the two first species has wall ingrowths like fingers with low electron density that protrude into the cytoplasm. The ultrastructural characteristics of the transmitting cells allow to characterize three of the sections of the genus.

The Biology of Invasive Alien Plants in Canada. 10. Nymphoides peltata (S. G. Gmel.) Kuntze

The freshwater aquatic species Nymphoides peltata has been introduced to Canada as an ornamental plant and has been found at sites in Newfoundland, Nova Scotia, Quebec, Ontario and British Columbia. It is currently available through the aquatic nursery trade in Canada and the United States. It may be considered as adventive in Canada since populations readily expand beyond the site of planting, but there is no evidence as yet that it is fully naturalized. In the United States it has naturalized in still or slow-moving waters at widely scattered locations where it replaces native plant communities, changes ecological processes and interferes with human navigation and recreational activities. The short rhizomes over-winter under Canadian conditions, even when complete water drainage results in freezing of the substratum. In its native range, the species has two floral morphs (i.e., is distylous) with a weak incompatibility system, but North American populations usually consist of a single flower morph. A population at Ottawa, ON, has monomorphic flowers with characteristics overlapping between the two Eurasian morphs and has been observed to produce large numbers of viable seeds. Seeds germinate in the spring either on the substratum in shallow water or at the water surface. Seedlings germinating at the water surface may float for several weeks prior to sinking and establishing on the substratum in shallow water. Vigorous stolon production promotes rapid colonization, and vegetative dispersal is readily accomplished through fragmentation of stolons and stems. Key words: Nymphoides peltata, yellow floating-heart, Menyanthaceae, faux nénuphar, NYPPE, weed biology

Odour and colour polymorphism in the food-deceptive orchid Dactylorhiza romana

The food deceptive orchid, Dactylorhiza romana (Sebastiani) Soo exhibits a colour polymorphism with yellow, red, and intermediate orange morphs. In this study we tested if floral odour differed among the three distinct colour morphs. We identified 23 odour compounds in D. romana, and all of them occurred in the three colour morphs. Monoterpenes dominated the floral scent. On the basis of Euclidean distances of relative amounts of compounds, yellow morphs were closer to each other than to orange or red morphs. Differentiation of the morphs was mainly due to linalool and benzaldehyde. Linalool occurred in low relative amounts in the yellow morphs, but in high amounts in some of the red individuals, whereas benzaldehyde occurred in higher relative amounts in yellow morphs. Linalool and benzaldehyde are known to be important signal-substances in plant-insect communication, however, it remains to be shown whether insects can discriminate between flower morphs on the basis of the here shown odour differences.

Distribution of Flower Morphs, Ploidy Level and Sexual Reproduction of the Invasive Weed Oxalis pes-caprae in the Western Area of the Mediterranean Region

Oxalis pes-caprae is a widespread invasive weed in regions with a Mediterranean climate. In its native habitat (southern Africa) this species has been reported as heterostylous with trimorphic flowers and a self- and morph-incompatible reproductive system. In most of the areas invaded, only a pentaploid short-styled morphotype that reproduces mainly asexually by bulbils is reported, but this has only been confirmed empirically. This study aims to analyse the floral morph proportions in a wide distribution area, test the sexual female success, and explain the causes of low sexual reproduction of this species in the western area of the Mediterranean Basin. Fifty-five populations of O. pes-caprae were sampled in the Iberian Peninsula and Morocco to evaluate the floral morph ratio and individual fruit set. In plants from a dimorphic population, hand-pollination experiments were performed to evaluate the effect of the pollen source on pollen tube growth through the style. The ploidy level and genome size of individuals of each floral morph were analysed using flow cytometry. From the populations studied 89.1 % were monomorphic, with most of them containing the short-styled (SS) floral morph, and 10.9 % were dimorphic containing long-styled (LS) and SS morphs. In some of these, isoplethy was verified but no fruit production was observed in any population. A sterile form was also recorded in several populations. Hand-pollination experiments revealed that pollen grains germinated over recipient stigmas. In intermorph crossings, pollen tubes were able to develop and fruit initiation was observed in some cases, while in intramorph pollinations, pollen tube development was sporadic and no fruit initiation was observed. All individuals within each floral form presented the same DNA ploidy level: SS plants were pentaploid and LS and the sterile form were tetraploid. The low or null sexual reproduction success of this species in the area of invasion studied seems related with the high frequency of monomorphic populations, the unequal proportion of floral morphs in dimorphic populations and the presence of different ploidy levels between SS and LS morphs. The discovery of the occurrence of an LS floral morph and a sterile form, whose invading capacity in these areas is as yet unknown, will be valuable information for management programmes.

Intraspecific variation of flower colour and its distribution within a sea lavender, Limonium wrightii (Plumbaginaceae), in the northwestern Pacific Islands

Differentiation of flower colour is thought to be one of the most important factors promoting plant speciation. We describe the intraspecific variation of flower colour and its distribution in Limonium wrightii. We conducted a survey on 36 islands in the northwestern Pacific and discriminated six morphs of flower colour variation. Two flower colour morphs, pink and yellow, were most frequently observed, and their geographical distributions were basically allopatric. These two morphs were in contact in a narrow zone on Okinoerabu Island, located in the middle region of the Ryukyu Archipelago. In addition, orange, white, and ivory flower morphs were also found in this zone. The geographical distribution of pink and yellow morphs showed a "leapfrog" pattern; the distribution of pink flowers was divided into two areas, intercalated by the distribution of the yellow flower morph. The orange morph may have resulted from hybridization between the pink and yellow flower morphs.

Comparative Study on the Aerial and Subterranean Flower Development in Amphicarpaea edgeworthii Benth. (Leguminosae: Papilionoideae), an Amphicarpic Species

Amphicarpy is a rare phenomenon in angiosperms. There are few studies on the floral development of aerial and especially subterranean flowers of the amphicarpic species. In this study, we examine the floral ontogeny of Amphicarpaea edgeworthii, an amphicarpic legume, using SEM. Three types of flowers can be produced in the same individual of the species: the subterranean flowers, solitary without subtending leaves; the aerial cleistogamous flowers, generally solitary in leaf axils; and the aerial chasmogamous flowers, one or two subtended by a bract. There is little difference in terms of the organ initiation among the three flower morphs. The order of initiation among whorls is sepals, petals, carpel, outer‐whorl stamens, and inner‐whorl stamens. Within each whorl, no obvious unidirectional order is found among the floral organ components. The development of petals, two‐whorl stamens, and a carpel in the aerial and subterranean flowers diverges at the mid‐ to late‐development stage. The mature aerial cha...

Floral plasticity and flower evolution in Atriplex halimus L. (Amaranthaceae)

Atriplex halimus, a monoecious species, produces flowers displaying two basic structures. A first structural pattern is made of pentamerous male flowers with perianth parts and stamens. The second structural pattern is represented by female flowers, limited to a single pistil enclosed in two opposite bracteoles. In both structures, however, unisexual flowers of the unexpected sex and hermaphroditic flowers have been detected. In the present work, new flowers, never found before in A. halimus, are described. Their structural pattern includes bracteoles and perianth segments, and they are either hermaphroditic or unixesual. These findings revealing the huge floral plasticity, suggest that the two flower structures normally occurring in A. halimus have derived from the same original flower morph through two pathways, implicating selective suppressions of flower parts.

A morphological, karyological and chemical study of the Apteranthes (Caralluma) europaea complex

The Apteranthes europaea complex (Apocynaceae–Asclepiadoideae–Ceropegieae–Stapeliinae) distributed from Morocco/southern Spain along the North African coast of the Mediterranean Sea up to Sinai, Negev and southern Jordan is studied with emphasis on stem and flower morphology by SEM, chromosome sizes and flavonoid compounds. Apteranthes europaea was found to be rich in rather uncommon flavone glycosides. Of these, luteolin 4′-neohesperidoside represents the major flavonoid of all samples; luteolin-3′-O-(6′-O-sinapoylglucoside)-4′-O-neohesperidoside and luteolin-3′-O-(6′-O-feruloylglucoside)-4′-O-neohesperidoside are reported here for the first time. Flavonol glycosides also occur, but in much smaller quantities. The different flower morphs, variation in stem and corolla epidermal structures, slight variations in the length of the 2n = 22 chromosomes and in quantitative flavonoid composition are taxonomically best reflected by subdividing the complex into a western var. europaea (Europe and Africa) and an eastern var. judaica (Sinai, Arabia). © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 419–432.

Variação no número de glândulas e produção de óleo em flores de Stigmaphyllon paralias A. Juss. (Malpighiaceae)

Foi estudada uma população de Stigmaphyllon paralias (Malpighiaceae) em Feira de Santana, Bahia, Brasil, visando analisar a variação do número de glândulas e sua produção de óleo nas flores. Dos indivíduos analisados, 76% não variaram o número de glândulas entre suas flores, ocorrendo 41% de indivíduos com flores que possuem 10 glândulas, 31% com oito glândulas e 4% com nove glândulas. Nas flores dos morfos que apresentam oito e nove glândulas, as glândulas ausentes são sempre as da sépala inferior. Centris leprieuri e Epicharis sp. (Apidae: Centridini) foram as únicas espécies que visitaram S. paralias, coletando óleo como recompensa. A sépala inferior localiza-se sob o abdome do polinizador quando pousado na flor, tornando-se inacessível à coleta de óleo. Sugerimos que a incapacidade de utilização de algumas glândulas pelos polinizadores possa ter possibilitado o aparecimento de morfos nas populações que não apresentam estas glândulas como caráter adaptativo por gerar economia de recursos na produção de recompensa não utilizada pelo polinizador. Todas as glândulas de todos os morfos são funcionais. As flores dos dois morfos principais com oito e 10 glândulas, produzem a mesma quantidade total de óleo. As glândulas das flores com oito glândulas aumentam a produção em cerca de 20%, compensando a produção total de óleo por flor.