Evolutionary Trends in the Flowers of Asteridae: Is Polyandry an Alternative to Zygomorphy?

Background and Aims

Floral symmetry presents two main states in angiosperms, actinomorphy (polysymmetry or radial symmetry) and zygomorphy (monosymmetry or bilateral symmetry). Transitions from actinomorphy to zygomorphy have occurred repeatedly among flowering plants, possibly in coadaptation with specialized pollinators. In this paper, the rules controlling the evolution of floral symmetry were investigated to determine in which architectural context zygomorphy can evolve.

Methods

Floral traits potentially associated with perianth symmetry shifts in Asteridae, one of the major clades of the core eudicots, were selected: namely the perianth merism, the presence and number of spurs, and the androecium organ number. The evolution of these characters was optimized on a composite tree. Correlations between symmetry and the other morphological traits were then examined using a phylogenetic comparative method.

Key Results

The analyses reveal that the evolution of floral symmetry in Asteridae is conditioned by both androecium organ number and perianth merism and that zygomorphy is a prerequisite to the emergence of spurs.

Conclusions

The statistically significant correlation between perianth zygomorphy and oligandry suggests that the evolution of floral symmetry could be canalized by developmental or spatial constraint. Interestingly, the evolution of polyandry in an actinomorphic context appears as an alternative evolutionary pathway to zygomorphy in Asteridae. These results may be interpreted either in terms of plant–pollinator adaptation or in terms of developmental or physical constraints. The results are discussed in relation to current knowledge about the molecular bases underlying floral symmetry.Key words: Floral symmetry, architectural constraints, Asteridae, comparative analysis, composite tree, correlated evolution, evolutionary scenario     

Establishment of zygomorphy on an ontogenic spiral and evolution of perianth in the tribe Delphinieae (Ranunculaceae)

Background and Aims

Ranunculaceae presents both ancestral and derived floral traits for eudicots, and as such is of potential interest to understand key steps involved in the evolution of zygomorphy in eudicots. Zygomorphy evolved once in Ranunculaceae, in the speciose and derived tribe Delphinieae. This tribe consists of two genera (Aconitum and Delphinium s.l.) comprising more than one-quarter of the species of the family. In this paper, the establishment of zygomorphy during development was investigated to cast light on the origin and evolution of this morphological novelty.

Methods

The floral developmental sequence of six species of Ranunculaceae, three actinomorphic (Nigella damascena, Aquilegia alpina and Clematis recta) and three zygomorphic (Aconitum napellus, Delphinium staphisagria and D. grandiflorum), was compared. A developmental model was elaborated to break down the successive acquisitions of floral organ identities on the ontogenic spiral (all the species studied except Aquilegia have a spiral phyllotaxis), giving clues to understanding this complex morphogenesis from an evo-devo point of view. In addition, the evolution of symmetry in Ranunculaceae was examined in conjunction with other traits of flowers and with ecological factors.

Key Results

In the species studied, zygomorphy is established after organogenesis is completed, and is late, compared with other zygomorphic eudicot species. Zygomorphy occurs in flowers characterized by a fixed merism and a partially reduced and transformed corolla.

Conclusions

It is suggested that shifts in expression of genes controlling the merism, as well as floral symmetry and organ identity, have played a critical role in the evolution of zygomorphy in Delphinieae, while the presence of pollinators able to exploit the peculiar morphology of the flower has been a key factor for the maintenance and diversification of this trait.Key words: Delphinieae, development, evolution, evo-devo, nectar spurs, ontogenic spiral, Ranunculaceae, zygomorphy     

The influence of floral symmetry,dependence on pollinators and pollination generalization on flower size variation

Background and Aims

The pollinator-mediated stabilizing selection hypothesis suggests that the specialized pollination system of zygomorphic flowers might cause stabilizing selection, reducing their flower size variation compared with actinomorphic flowers. However, the degree of ecological generalization and of dependence on pollinators varies greatly among species of both flower symmetry types and this may also affect flower size variation.

Methods

Data on 43 species from two contrasting communities (one alpine and one lowland community) were used to test the relationships and interactions between flower size phenotypic variation, floral symmetry, ecological pollination generalization and species'' dependence on pollinators.

Key Results

Contrary to what was expected, higher flower size variation was found in zygomorphic than in actinomorphic species in the lowland community, and no difference in flower size variation was found between symmetry types in the alpine community. The relationship between floral symmetry and flower size variation depended on ecological generalization and species'' dependence on pollinators, although the influence of ecological generalization was only detected in the alpine community. Zygomorphic species that were highly dependent on pollinators and that were ecologically specialized were less variable in flower size than ecologically generalist and selfing zygomorphic species, supporting the pollinator-mediated stabilizing selection hypothesis. However, these relationships were not found in actinomorphic species, probably because they are not dependent on any particular pollinator for efficient pollination and therefore their flower size always shows moderate levels of variation.

Conclusions

The study suggests that the relationship between flower size variation and floral symmetry may be influenced by population-dependent factors, such as ecological generalization and species'' dependence on pollinators.     

Ontogenetic origins of floral bilateral symmetry in Moringaceae (Brassicales)

Floral morphology of the 13 species of Moringa ranges from actinomorphic flowers with little hypanthium to highly zygomorphic flowers with well-developed hypanthia. Scanning electron and light microscopy were used to identify ontogenetic differences among two actinomorphic and eight zygomorphic species. All species show traces of zygomorphy between petal organogenesis and anther differentiation. At late organogenesis, zygomorphy is manifest by one petal being larger than the others, slight unidirectional maturation of the anthers, and in many species, some staminodes may be missing. At organ differentiation and beyond, the actinomorphic species show a trend toward increasing actinomorphy, whereas the zygomorphic features of early ontogeny are progressively accentuated throughout the ontogeny of the zygomorphic species. Because of the early traces of zygomorphy throughout the family, ontogeny in Moringa does not resemble that known from the sister taxon Caricaceae, which has flowers that are actinomorphic throughout ontogeny. Great intraspecific variation was found in floral plan in the actinomorphic-flowered species in contrast to the zygomorphic species. Each of the main clades in the family is distinguished by at least one feature of floral ontogeny. In general, ontogenetic differences that are congruent with deeper phylogenetic splits tend to occur earlier in ontogeny than those congruent with more recent divergences.     

The need to re-investigate the nature of homoplastic characters: an ontogenetic case study of the 'bracteoles' in Atripliceae (Chenopodiaceae)

Background and Aims

Within Chenopodioideae, Atripliceae have been distinguished by two bracteoles enveloping the female flowers/fruits, whereas in other tribes flowers are described as ebracteolate with persistent perianth. Molecular phylogenetic hypotheses suggest ‘bracteoles’ to be homoplastic. The origin of the bracteoles was explained by successive inflorescence reductions. Flower reduction was used to explain sex determination. Therefore, floral ontogeny was studied to evaluate the nature of the bracteoles and sex determination in Atripliceae.

Methods

Inflorescences of species of Atriplex, Chenopodium, Dysphania and Spinacia oleracea were investigated using light microscopy and scanning electron microscopy.

Key Results

The main axis of the inflorescence is indeterminate with elementary dichasia as lateral units. Flowers develop centripetally, with first the formation of a perianth primordium either from a ring primordium or from five individual tepal primordia fusing post-genitally. Subsequently, five stamen primordia originate, followed by the formation of an annular ovary primordium surrounding a central single ovule. Flowers are either initially hermaphroditic remaining bisexual and/or becoming functionally unisexual at later stages, or initially unisexual. In the studied species of Atriplex, female flowers are strictly female, except in A. hortensis. In Spinacia, female and male flowers are unisexual at all developmental stages. Female flowers of Atriplex and Spinacia are protected by two accrescent fused tepal lobes, whereas the other perianth members are absent.

Conclusions

In Atriplex and Spinacia modified structures around female flowers are not bracteoles, but two opposite accrescent tepal lobes, parts of a perianth persistent on the fruit. Flowers can achieve sexuality through many different combinations; they are initially hermaphroditic, subsequently developing into bisexual or functionally unisexual flowers, with the exception of Spinacia and strictly female flowers in Atriplex, which are unisexual from the earliest developmental stages. There may be a relationship between the formation of an annular perianth primordium and flexibility in floral sex determination.     

Floral structure of Emmotum (Icacinaceae sensu stricto or Emmotaceae), a phylogenetically isolated genus of lamiids with a unique pseudotrimerous gynoecium,bitegmic ovules and monosporangiate thecae

Background and Aims

Icacinaceae sensu stricto consist of a group of early branching lineages of lamiids whose relationships are not yet resolved and whose detailed floral morphology is poorly known. The most bizarre flowers occur in Emmotum: the gynoecium has three locules on one side and none on the other. It has been interpreted as consisting of three fertile and two sterile carpels or of one fertile carpel with two longitudinal septa and two sterile carpels. This study focused primarily on the outer and inner morphology of the gynoecium to resolve its disputed structure, and ovule structure was also studied. In addition, the perianth and androecium were investigated.

Methods

Flowers and floral buds of two Emmotum species, E. harleyi and E. nitens, were collected and fixed in the field, and then studied by scanning electron microscopy. Microtome section series were used to reconstruct their morphology.

Key Results

The gynoecium in Emmotum was confirmed as pentamerous, consisting of three fertile and two sterile carpels. Each of the three locules behaves as the single locule in other Icacinaceae, with the placenta of the two ovules being identical, which shows that three fertile carpels are present. In addition, it was found that the ovules are bitegmic, which is almost unique in lamiids, and that the stamens have monosporangiate thecae, which also occurs in the closely related family Oncothecaceae, but is not known from any other Icacinaceae sensu lato so far.

Conclusions

The flowers of Emmotum have unique characters at different evolutionary levels: the pseudotrimerous gynoecium at angiosperm level, the bitegmic ovules at lamiid level and the monosporangiate thecae at family or family group level. However, in general, the floral morphology of Emmotum fits well in Icacinaceae. More comparative research on flower structure is necessary in Icacinaceae and other early branching lineages of lamiids to better understand the initial evolution of this large lineage of asterids.     

On the roles of colour and scent in a specialized floral mimicry system

Background and Aims

Sexually deceptive orchids achieve cross-pollination by mimicking the mating signals of female insects, generally hymenopterans. This pollination mechanism is often highly specific as it is based primarily on the mimicry of mating signals, especially the female sex pheromones of the targeted pollinator. Like many deceptive orchids, the Mediterranean species Ophrys arachnitiformis shows high levels of floral trait variation, especially in the colour of the perianth, which is either green or white/pinkinsh within populations. The adaptive significance of perianth colour polymorphism and its influence on pollinator visitation rates in sexually deceptive orchids remain obscure.

Methods

The relative importance of floral scent versus perianth colour in pollinator attraction in this orchid pollinator mimicry system was evaluated by performing floral scent analyses by gas chromatography-mass spectrometry (GC-MS) and behavioural bioassays with the pollinators under natural conditions were performed.

Key Results

The relative and absolute amounts of behaviourally active compounds are identical in the two colour morphs of O. arachnitiformis. Neither presence/absence nor the colour of the perianth (green versus white) influence attractiveness of the flowers to Colletes cunicularius males, the main pollinator of O. arachnitiformis.

Conclusion

Chemical signals alone can mediate the interactions in highly specialized mimicry systems. Floral colour polymorphism in O. arachnitiformis is not subjected to selection imposed by C. cunicularius males, and an interplay between different non-adaptive processes may be responsible for the maintenance of floral colour polymorphism both within and among populations.     

Floral development of Hydrocera and Impatiens reveals evolutionary trends in the most early diverged lineages of the Balsaminaceae

Background and Aims

Balsaminaceae consist of two genera, the monospecific Hydrocera and its species-rich sister Impatiens. Although both genera are seemingly rather similar in overall appearance, they differ in ecology, distribution range, habitat preference and morphology. Because morphological support for the current molecular phylogenetic hypothesis of Impatiens is low, a developmental study is necessary in order to obtain better insights into the evolutionary history of the family. Therefore, the floral development of H. triflora and I. omeiana was investigated, representing the most early-diverged lineage of Impatiens, and the observations were compared with the literature.

Methods

Flowers at all developmental stages were examined using scanning electron microscopy and light microscopy.

Key results

In Hydrocera, two whorls of five free perianth primordia develop into a less zygomorphic perianth compared with its sister genus. The androecial cap originates from five individual stamen primordia. Post-genital fusion of the upper parts of the filaments result in a filament ring below the anthers. The anthers fuse forming connivent anther-like units. The gynoecium of Hydrocera is pentamerous; it is largely synascidiate in early development. Only then is a symplicate zone formed resulting in style and stigmas. In I. omeiana, the perianth is formed as in Hydrocera. Five individual stamen primordia develop into five stamens, of which the upper part of the filaments converge with each other. The gynoecium of I. omeiana is tetramerous; it appears annular in early development.

Conclusions

Comparison of the present results with developmental data from the literature confirms the perianth morphocline hypothesis in which a congenital fusion of the parts of the perianth results in a shift from pentasepalous to trisepalous flowers. In addition, the development of the androecial cap and the gynoecium follows several distinct ontogenetic sequences within the family.     

Specific Duplication and Dorsoventrally Asymmetric Expression Patterns of Cycloidea-Like Genes in Zygomorphic Species of Ranunculaceae

Floral bilateral symmetry (zygomorphy) has evolved several times independently in angiosperms from radially symmetrical (actinomorphic) ancestral states. Homologs of the Antirrhinum majus Cycloidea gene (Cyc) have been shown to control floral symmetry in diverse groups in core eudicots. In the basal eudicot family Ranunculaceae, there is a single evolutionary transition from actinomorphy to zygomorphy in the stem lineage of the tribe Delphinieae. We characterized Cyc homologs in 18 genera of Ranunculaceae, including the four genera of Delphinieae, in a sampling that represents the floral morphological diversity of this tribe, and reconstructed the evolutionary history of this gene family in Ranunculaceae. Within each of the two RanaCyL (Ranunculaceae Cycloidea-like) lineages previously identified, an additional duplication possibly predating the emergence of the Delphinieae was found, resulting in up to four gene copies in zygomorphic species. Expression analyses indicate that the RanaCyL paralogs are expressed early in floral buds and that the duration of their expression varies between species and paralog class. At most one RanaCyL paralog was expressed during the late stages of floral development in the actinomorphic species studied whereas all paralogs from the zygomorphic species were expressed, composing a species-specific identity code for perianth organs. The contrasted asymmetric patterns of expression observed in the two zygomorphic species is discussed in relation to their distinct perianth architecture.     

Floral ontogeny of Annonaceae: evidence for high variability in floral form

Background and Aims

Annonaceae are one of the largest families of Magnoliales. This study investigates the comparative floral development of 15 species to understand the basis for evolutionary changes in the perianth, androecium and carpels and to provide additional characters for phylogenetic investigation.

Methods

Floral ontogeny of 15 species from 12 genera is examined and described using scanning electron microscopy.

Key Results

Initiation of the three perianth whorls is either helical or unidirectional. Merism is mostly trimerous, occasionally tetramerous and the members of the inner perianth whorl may be missing or are in double position. The androecium and the gynoecium were found to be variable in organ numbers (from highly polymerous to a fixed number, six in the androecium and one or two in the gynoecium). Initiation of the androecium starts invariably with three pairs of stamen primordia along the sides of the hexagonal floral apex. Although inner staminodes were not observed, they were reported in other genera and other families of Magnoliales, except Magnoliaceae and Myristicaceae. Initiation of further organs is centripetal. Androecia with relatively low stamen numbers have a whorled phyllotaxis throughout, while phyllotaxis becomes irregular with higher stamen numbers. The limits between stamens and carpels are unstable and carpels continue the sequence of stamens with a similar variability.

Conclusions

It was found that merism of flowers is often variable in some species with fluctuations between trimery and tetramery. Doubling of inner perianth parts is caused by (unequal) splitting of primordia, contrary to the androecium, and is independent of changes of merism. Derived features, such as a variable merism, absence of the inner perianth and inner staminodes, fixed numbers of stamen and carpels, and capitate or elongate styles are distributed in different clades and evolved independently. The evolution of the androecium is discussed in the context of basal angiosperms: paired outer stamens are the consequence of the transition between the larger perianth parts and much smaller stamens, and not the result of splitting. An increase in stamen number is correlated with their smaller size at initiation, while limits between stamens and carpels are unclear with easy transitions of one organ type into another in some genera, or the complete replacement of carpels by stamens in unisexual flowers.     

Natural selection on Erysimum mediohispanicum flower shape: insights into the evolution of zygomorphy

Paleontological and phylogenetic studies have shown that floral zygomorphy (bilateral symmetry) has evolved independently in several plant groups from actinomorphic (radially symmetric) ancestors as a consequence of strong selection exerted by specialized pollinators. Most studies focused on unraveling the developmental genetics of flower symmetry, but little is known about the adaptive significance of intraspecific flower shape variation under natural conditions. We provide the first evidence for natural selection favoring zygomorphy in a wild population of Erysimum mediohispanicum (Brassicaceae), a plant showing extensive continuous variation in flower shape, ranging from actinomorphic to zygomorphic flowers. By using geometric morphometric tools to describe flower shape, we demonstrate that plants bearing zygomorphic flowers received more pollinator visits and had the highest fitness, measured not only by the number of seeds produced per plant but also by the number of seeds surviving to the juvenile stage. This study provides strong evidence for the existence of significant fitness differences associated with floral shape variation in E. mediohispanicum, thus illuminating a pathway for the evolution of zygomorphy in natural populations.     

Ontogeny and structure of the acervulate partial inflorescence in Hyophorbe lagenicaulis (Arecaceae; Arecoideae)

Background and Aims

The palm tribe Chamaedoreeae displays flowers arranged in a complex partial inflorescence called an acervulus. This type of partial inflorescence has so far not been reported elsewhere in the largest palm subfamily Arecoideae, which is traditionally characterized by flowers predominantly arranged in triads of one central female and two lateral male flowers. The ontogenetic basis of the acervulus is as yet unknown and its structural diversity throughout the genera of the Chamaedoreeae poorly recorded. This study aims to provide critical information on these aspects.

Methods

Developmental series and mature inflorescences were sampled from plants cultivated in international botanical gardens and wild populations. The main techniques employed included scanning electronic microscopy and serial anatomical sectioning of resin-embedded fragments of rachillae.

Key Results

Inflorescence ontogeny in Hyophorbe lagenicaulis demonstrates that the acervulus and the inflorescence rachilla form a condensed and cymose branching system resembling a coenosome. Syndesmy results from a combined process of rapid development and adnation, without or with reduced axis elongation. Acervulus diversity in the ten taxa of the Chamaedoreeae studied is displayed at the level of their positioning within the inflorescence, their arrangement, the number of floral buds and their sexual expression.

Conclusions

The results show that a more general definition of the type of partial inflorescence observed within the large subfamily Arecoideae would correspond to a cyme rather than to a floral triad. In spite of their common cymose architecture, the floral triad and the acervulus present differences with respect to the number and arrangement of floral buds, the superficial pattern of development and sexual expression.     

Floral ontogeny and gene protein localization rules out euanthial interpretation of reproductive units in Lepironia (Cyperaceae,Mapanioideae, Chrysitricheae)

Background and Aims

In the sedge subfamily Mapanioideae there are considerable discrepancies between the standard trimerous monocot floral architecture expected and the complex floral and inflorescence morphologies seen. Decades of debate about whether the basic reproductive units are single flowers or pseudanthia have not resolved the question. This paper evaluates current knowledge about Mapaniid reproductive structures and presents an ontogenetic study of the Mapaniid genus Lepironia with the first floral protein expression maps for the family, localizing the products of the APETALA1/FRUITFULL-like (AP1/FUL) MADS-box genes with the aim of shedding light on this conundrum.

Methods

A range of reproductive developmental stages, from spikelet primordia through to infructescence material, were processed for anatomical and immunohistochemical analyses.

Key Results

The basic reproductive unit is subtended by a bract and possesses two prophyll-like structures, the first organs to be initiated on the primordium, which grow rapidly, enclosing two whorls of initiating leaf-like structures with intervening stamens and a central gynoecium, formed from an annular primordium. The subtending bract and prophyll-like structures possess very different morphologies from that of the internal leaf-like structures and do not show AP1/FUL-like protein localization, which is otherwise strongly localized in the internal leaf-like structures, stamens and gynoecia.

Conclusions

Results support the synanthial hypothesis as the evolutionary origin of the reproductive unit. Thus, the basic reproductive unit in Lepironia is an extremely condensed pseudanthium, of staminate flowers surrounding a central terminal pistillate female flower. Early in development the reproductive unit becomes enclosed by a split-prophyll, with the whole structure subtended by a bract.     

A double-flowered variety of lesser periwinkle (Vinca minor fl. pl.) that has persisted in the wild for more than 160 years

Background and Aims

Homeotic transitions are usually dismissed by population geneticists as credible modes of evolution due to their assumed negative impact on fitness. However, several lines of evidence suggest that such changes in organ identity have played an important role during the origin and subsequent evolution of the angiosperm flower. Better understanding of the performance of wild populations of floral homeotic varieties should help to clarify the evolutionary potential of homeotic mutants. Wild populations of plants with changes in floral symmetry, or with reproductive organs replacing perianth organs or sepals replacing petals have already been documented. However, although double-flowered varieties are quite popular as ornamental and garden plants, they are rarely found in the wild and, if they are, usually occur only as rare mutant individuals, probably because of their low fitness relative to the wild-type. We therefore investigated a double-flowered variety of lesser periwinkle, Vinca minor flore pleno (fl. pl.), that is reported to have existed in the wild for at least 160 years. To assess the merits of this plant as a new model system for investigations on the evolutionary potential of double-flowered varieties we explored the morphological details and distribution of the mutant phenotype.

Methods

The floral morphology of the double-flowered variety and of a nearby population of wild-type plants was investigated by means of visual inspection and light microscopy of flowers, the latter involving dissected or sectioned floral organs.

Key Results

The double-flowered variety was found in several patches covering dozens of square metres in a forest within the city limits of Jena (Germany). It appears to produce fewer flowers than the wild-type, and its flowers are purple rather than blue. Most sepals in the first floral whorl resemble those in the wild-type, although occasionally one sepal is broadened and twisted. The structure of second-whorl petals is very similar to that of the wild-type, but their number per flower is more variable. The double-flowered character is due to partial or complete transformation of stamens in the third whorl into petaloid organs. Occasionally, ‘flowers within flowers’ also develop on elongated pedicels in the double-flowered variety.

Conclusions

The flowers of V. minor fl. pl. show meristic as well as homeotic changes, and occasionally other developmental abnormalities such as mis-shaped sepals or loss of floral determinacy. V. minor fl. pl. thus adds to a growing list of natural floral homeotic varieties that have established persistent populations in the wild. Our case study documents that even mutant varieties that have reproductive organs partially transformed into perianth organs can persist in the wild for centuries. This finding makes it at least conceivable that even double-flowered varieties have the potential to establish new evolutionary lineages, and hence may contribute to macroevolutionary transitions and cladogenesis.     

An assessment of morphogenetic fluctuation during reproductive phase change in Arabidopsis

Background and Aims

Reproductive phase change in Arabidopsis thaliana is characterized by two transitions in phytomer identity, the differentiation of the first elongate internode (bolting transition) and of the first flower (floral transition). An evaluation of the dynamics of these transitions was sought by examining the precision of the corresponding phytomer identity changes.

Methods

The length of the first elongate internode and the frequency of chimeric inflorescence structures, e.g. paraclades not subtended by a leaf (no-leaf/paraclades) and flowers subtended by a bract (bract/flowers), were measured in the Wassilewskija (Ws) accession and 47 early flowering mutants under a wide range of photoperiods. The impact of photoperiodic perturbations applied to Ws plants at different times of development was also evaluated.

Key Results

In Ws, both types of characters were remarkably constant across photoperiods in spite of a high degree of interindividual variability. Bract/flowers were not normally produced in Ws, but they were observed in conditions that suggest enhanced light signalling, e.g. in response to continuous light perturbations and in mutants with reduced hypocotyl elongation. In contrast, no-leaf/paraclades were normally present in approx. 20 % of Ws plants, and their frequency was increased in conditions that suggest reduced light signalling, e.g. in mutants with altered specification of long-day responses. The length of the first elongate internode was unrelated to the rate of stem elongation and to the regulation of reproductive phase change.

Conclusions

Bract/flowers and no-leaf/paraclades corresponded to opposite effects on the floral transition that reflected different dynamics of progression to flowering. In contrast, the length of the first elongate internode was only indirectly related to the regulation of reproductive phase change and was mainly dependent on global morphogenetic constraints. This paper proposes that morphogenetic variability could be used to identify critical phases of development and characterize the canalization of developmental patterns.     

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 zygomorphy, the recurring evolution of a successful trait

The flowers of the primitive angiosperm plants were radially symmetrical (actinomorphic). Flowers with bilateral symmetry (zygomorphic) evolved in several clades independently as an adaptation to specialized methods of pollination and played an important role in the diversification of flowering plants. In the model species Antirrhinum majus (snapdragon), the related genes CYCLOIDEA (CYC) and DICHOTOMA (DICH) are key in the development of this trait. This raises the question of whether they played a role in the evolution of floral bilateral symmetry. To address this, the evolution of CYC in relation to the evolution of zygomorphy is being investigated. Phylogenetic and functional analyses of CYC-like genes are being carried out in groups either closely related to Antirhinum or in families where zygomorphy evolved as an independent event. In addition, the origin of zygomorphy is being studied by comparing the function of CYC-like genes in species with zygomorphic flowers with their function in species with radially symmetrical flowers.