Evolution Of Distyly Research Articles

Comprehensive transcriptomic profiling reveals complex molecular mechanisms in the regulation of style-length dimorphism in Guettarda speciosa (Rubiaceae), a species with "anomalous" distyly.

The evolution of heterostyly, a genetically controlled floral polymorphism, has been a hotspot of research since the 19th century. In recent years, studies on the molecular mechanism of distyly (the most common form of heterostyly) revealed an evolutionary convergence in genes for brassinosteroids (BR) degradation in different angiosperm groups. This floral polymorphism often exhibits considerable variability that some taxa have significant stylar dimorphism, but anther height differs less. This phenomenon has been termed "anomalous" distyly, which is usually regarded as a transitional stage in evolution. Compared to "typical" distyly, the genetic regulation of "anomalous" distyly is almost unknown, leaving a big gap in our understanding of this special floral adaptation strategy. Here we performed the first molecular-level study focusing on this floral polymorphism in Guettarda speciosa (Rubiaceae), a tropical tree with "anomalous" distyly. Comprehensive transcriptomic profiling was conducted to examine which genes and metabolic pathways were involved in the genetic control of style dimorphism and if they exhibit similar convergence with "typical" distylous species. "Brassinosteroid homeostasis" and "plant hormone signal transduction" was the most significantly enriched GO term and KEGG pathway in the comparisons between L- and S-morph styles, respectively. Interestingly, homologs of all the reported S-locus genes either showed very similar expressions between L- and S-morph styles or no hits were found in G. speciosa. BKI1, a negative regulator of brassinosteroid signaling directly repressing BRI1 signal transduction, was identified as a potential gene regulating style length, which significantly up-regulated in the styles of S-morph. These findings supported the hypothesis that style length in G. speciosa was regulated through a BR-related signaling network in which BKI1 may be one key gene. Our data suggested, in species with "anomalous" distyly, style length was regulated by gene differential expressions, instead of the "hemizygous" S-locus genes in "typical" distylous flowers such as Primula and Gelsemium, representing an "intermediate" stage in the evolution of distyly. Genome-level analysis and functional studies in more species with "typical" and "anomalous" distyly would further decipher this "most complex marriage arrangement" in angiosperms and improve our knowledge of floral evolution.

Flower, seed, and fruit development in three Tunisian species of Polygonum: Implications for their taxonomy and evolution ofdistylyin Polygonaceae.

Polygonum is the largest genus of Polygonaceae and 5 species are reported in Tunisia. In order to characterized flower, seed, and fruit development in Polygonum, flower and fruit of Polygonium equisetiforme (var. graecum and peyerinhoffi), P. aviculare and P. maritimum, collected from Tunisia, were examined. Flowers are composed of five oblong tepals. P. equisetiforme and P. aviculare have whitish-pink distylous flowers with dimorphism of style, filament and anther height, pollen diameter and stigma size. In contrast, P. maritimum shows white homostylous flowers. The floral vasculature showed that the tepals are inserted in one whorl and their traces arise independently in 3+2 manner. The eight stamens are arranged in a 5+3 manner and the staminal bundles arise independently in the two whorls. The epidermis and endothecium cells width were higher in P. maritimum and the lowest endothecium width was observed in P. aviculare. Polygonum aviculare and P. equisetiforme showed circular pollen with shallow colpi and trilobite pollen shape with deep colpi, while P. maritimum rarely showed shallow colpi. The ovule is anatropous with basal placentation in P. equisetiforme and P. aviculare and apical placentation in P. maritimum. The young seed coat was formed by an endotesta with thick-walled cells, a mesotesta and exotesta with thin-walled cells and a tegmen composed of radially elongated cells. The fruits of the studied species are trigonous with ovate-lanceolate shape. In P. aviculare, the exocarp is thicker compared to the two other species, in P. equisetiforme, the mature exocarp consists of smaller rectangular cells with narrow cavities, and in P. maritimum showed a thinner exocarpIn conclusion, P. equisetiforme and P. aviculare are a typically distylous species from the morphological point of view and we discussed the significance of heterostyly in Polygonaceae. From this first morpho-anatomical study of Polygonum species in North Africa, we can conclude mainly that there is no significant difference between P. equisetiforme var. graecum and var. peyerinhoffi supporting a taxonomic grouping of these two varieties.

Floral biology of the velvetseed Guettarda platypoda DC. (Rubiaceae): Atypical distyly or style dimorphism?

Distylous species have flowers with short styles and long stamens (thrums), and flowers with the inverse condition (pins) in different individuals. Studies suggested that style dimorphism (floral morphs that differ only in style height) is an intermediate stage in the evolution of distyly. We found populations of Guettarda platypoda DC. with apparent morphological variations of distyly and our objective was to assess stylar condition and other reproductive characteristics of G. platypoda. We analyzed the anthesis period, scent glands, nectar features, pollen number and viability, and measured lengths of corolla, anther and stigmatic lobes, heights of stigma and anther, and proportion of individuals of the floral morphs within the population. We characterized the species’ reproductive system and investigated the behavior and frequency of its flower visitors. Two flower morphs were observed, one with a short style (thrum) and the other with a long style (pin); the anthers have similar height. Anthesis occurred between 1700h and 1100h. The volume of nectar, number of pollen grains and pollen viability did not differ between morphs, but the thrum showed more concentrated nectar. Both morphs had scent glands. The lengths of anthers and stigmas were similar among morphs, but the corolla was longer in the thrums. The influence of the corolla was the same on the different whorls in the pins, but stronger on stamen height than on stigma position in the thrums. The population is isoplethic and formed fruits in all treatments, with a partial incompatibility system for the thrums. Its visitors were three moth species, including two sphingids. The style dimorphism found in this sphingophilous species may indicate that G. platypoda represents an intermediate stage in the evolution towards distyly.

Pollen and stigma size changes during the transition from tristyly to distyly in Oxalis alpina (Oxalidaceae).

Pollen and stigma size have the potential to influence male fitness of hermaphroditic plants, particularly in species presenting floral polymorphisms characterised by marked differences in these traits among floral morphs. In this study, we take advantage of the evolutionary transition from tristyly to distyly experienced by Oxalis alpina (Oxalidaceae), and examined whether modifications in the ancillary traits (pollen and stigma size) respond to allometric changes in other floral traits. Also, we tested whether these modifications are in accordance with what would be expected under the hypothesis that novel competitive scenarios (as in distylous-derived reproductive system) exert morph- and whorl-specific selective pressures to match the available stigmas. We measure pollen and stigma size in five populations of O. alpina representing the tristyly-distyly transition. A general reduction in pollen and stigma size occurred along the tristyly-distyly transition, and pollen size from the two anther levels within each morph converged to a similar size that was characterised by whorl-specific changes (increases or decreases) in pollen size of different anthers in each floral type. Overall, results from this study show that the evolution of distyly in this species is characterised not only by changes in sexual organ position and flower size, but also by morph-specific changes in pollen and stigma size. This evidence supports the importance of selection on pollen and stigma size, which increase fitness of remaining morphs following the evolution of distyly, and raises questions to explore on the functional value of pollen size in heterostylous systems under pollen competition.

Developmental variation and the evolution of distyly in Hedyotis caerulea (Rubiaceae).

The development of distyly is thought to arise from differential growth patterns in the pin and thrum morphs. However, few detailed studies exist on the early floral development of distylous flowers, and fewer still look at variation in these traits among populations. Buds at multiple stages of development were collected from five populations of Hedyotis caerulea to quantify how pins and thrums diverge with respect to the initiation, rate, and termination of growth between the stamens and stigmas. The growth rate of anthers varied little spatially across five populations and temporally in both pins and thrums, although thrum anthers grew faster than pin anthers. Dimorphy in stigma height was more complex. Pin stigmas first grew at a faster rate than those of thrums, and late in bud development, growth of thrum styles slowed. These rate changes varied among populations, and they differed from the congeneric H. salzmanii. Similar differences between morphs are known in other heterostylous species, and such variation in growth pattern among related species has been used to infer independent evolution of distylous systems.

Female and Male Mediation of Incompatibility Modifications during the Tristyly-Distyly Transition in Oxalis alpina

Transitions between breeding systems offer an opportunity to understand the selective forces underlying these changes. In the evolutionary transition from tristyly to distyly, changes in tristylous self-incompatibility (SI) may be associated with modifications of female function, male function, or both. To test the hypothesis that modifications of pollen incompatibility reactions are associated with these changes, we used reciprocal factorial crosses in two Oxalis alpina populations that differed in their incompatibility relationships. Contrary to predictions, the population exhibiting stronger tristylous SI showed significant variation in both female and male components of incompatibility. The population with more highly modified tristylous SI at a putatively later stage in the evolution of distyly had less variation in both paternal and maternal control of incompatibility. The more highly modified population also showed evidence of correlations between the changes in maternal and paternal components of tristylous SI and between incompatibility and changes in floral morphology. Comparisons of these populations indicate that modifications of both female and male components of tristylous SI may occur before changes in floral morphology during the transition from tristyly to distyly in O. alpina.

The role of historical factors and natural selection in the evolution of breeding systems of Oxalis alpina in the Sonoran desert ‘Sky Islands’

Pleistocene climatic oscillations are known to influence the patterns of genetic diversity and the distribution of traits that are the target of selection. Here, we combine phylogeographical and ecological niche modelling (ENM) approaches to explore the influence of historical factors (Pleistocene climatic shifts) and natural selection on the evolution of distyly (two floral morphs) from tristyly (three floral morphs) of Oxalis alpina in the Sky Islands of the Sonoran Desert. Molecular data and ENM indicate that historical factors have had a strong influence on the genetic structure and the geographical distribution of reproductive systems of O.alpina. Moreover, genetic results suggest the possibility that distylous populations do not represent a monophyletic group. We propose that the combined effects of natural selection and genetic drift have influenced the tristyly-distyly transition.

Nectar robbers pollinate flowers with sexual organs hidden within corollas in distylous Primula secundiflora (Primulaceae)

Nectar robbers are thought rarely to pollinate flowers, especially those with sexual organs hidden within corollas. In this study, we examined whether robbers pollinate flowers of distylous Primula secundiflora. Distylous plants have two floral morphs. Pin flowers have long styles and short stamens, and thrum flowers have short styles and long stamens. Flowers of P. secundiflora were commonly robbed by bumble-bees, and robbing holes were always situated between high and low sexual organs for both floral morphs. We observed that pollen grains of pin flowers were removed while thrum flowers received fresh pollen grains immediately after flowers were robbed. We manipulated flowers so that only nectar robbers could visit them. This resulted in 98 per cent of thrum flowers and 6 per cent of pin flowers setting fruit, and seed number per thrum fruit was also significantly higher than per pin fruit. Our findings suggest that nectar robbers transfer pollen from pin flowers to thrum flowers effectively, and consequently increase male fitness of the pin morph and female fitness of the thrum morph. Such asymmetrical pollen flow caused by nectar robbers may act as an important selective agent in floral fitness and evolution of distyly.

Evolutionary transitions of style polymorphisms in Lithodora (Boraginaceae)

Floral polymorphisms provide suitable model systems to test hypotheses concerning the evolution of outbreeding in plants. Although heterostyly has evolved in more than 28 angiosperm families, the evolutionary pathways involving related floral conditions have not yet been fully resolved. In this study, the reconstruction of ancestral states of style polymorphism, with both parsimony and maximum likelihood methods, was carried out for Boraginaceae species in the tribe Lithospermeae, particularly in the genus Lithodora sensu lato, where species present a wide variety of stylar conditions. Detailed floral morphometric analysis confirm different types of style polymorphism within Lithodora. They also reveal a novel style polymorphism (relaxed style dimorphism) in which anther height is variable within a flower (each anther being at a different height), which contrasts to regular distyly (constant anther height within flowers). Style monomorphism is likely to be the ancestral condition in Lithospermeae where the evolution of distyly has occurred several times. Style dimorphism is probably ancestral to distyly, as predicted by certain evolutionary models proposed for heterostyly. However, a reversion from distyly to style dimorphism also appears to occur in this tribe. This is the first documented occurrence of such a transition. This secondary style dimorphism is of the relaxed type and demonstrates the labile nature of floral polymorphisms, which are not necessarily a transition towards heterostyly. We discuss the selective forces involved in the evolution, maintainance and loss of style polymorphisms.

The evolution of distyly from tristyly in populations of Oxalis alpina (Oxalidaceae) in the Sky Islands of the Sonoran Desert

The evolution of distyly from tristyly was investigated in populations of Oxalis alpina at high elevations throughout the Sky Islands of the Sonoran Desert. Incompatibility systems in tristylous populations, where self-incompatible short-, mid-, and long-styled morphs occur in populations, vary from those typical of tristylous species in which each morph is equally capable of fertilizing ovules of the other two morphs, to breeding systems in which incompatibility relationships are asymmetric. In these populations, selection against the allele controlling expression of the mid-styled morph is likely. The degree of modification of incompatibility in the short- and long-styled morphs in 10 populations was strongly associated with fewer mid-styled morphs, supporting models predicting the effect of these modifications of incompatibility on frequency of the mid-styled morph. Self-compatibility of the mid-styled morph may be important for maintaining the frequency of this morph, depending on the level of self-pollination, self-fertilization, and the extent of inbreeding depression. Modifications of incompatibility in tristylous populations and the distribution of distylous populations of O. alpina in the Sky Island region have similar geographic components, indicating the potential importance of historical factors in the evolution of distyly from tristyly.

Evolutionary consequences of extensive morph loss in tristylous decodon verticillatus (Lythraceae): a shift from tristyly to distyly?

The evolution of distyly from tristyly has occurred repeatedly, especially in the Lythraceae. However, the evolutionary forces involved remain unclear since species exhibiting transitional stages between tristyly and distyly have rarely been studied. The self‐compatible, wetland perennial Decodon verticillatus (Lythraceae) may provide this transitional variation since populations commonly lack style morphs, particularly the mid‐styled (M) morph. In dimorphic populations lacking the M morph, anthers positioned at the mid level in both the long‐ (L) and short‐styled (S) morphs have lost their target stigma, setting the stage for either evolutionary repositioning of mid‐level anthers to increase pollen export to L and S stigmas, or increased variability in mid‐level anther position resulting from relaxed selection. We examined these two hypotheses by comparing floral morphology in eight dimorphic and ten trimorphic populations from throughout the species’ range. We found no evidence that loss of the M morph has led to evolutionary modification of mid‐level stamens. While mid‐level stamens of the S morph were 11.0 ± 4.0% (mean ± 1 SE) longer than those of the L morph in dimorphic populations, divergence in stamen length between morphs occurred to the same extent (10.4 ± 2.0%) in trimorphic populations and cannot be attributed to the absence of the M morph. Analyses of variability using median ratio tests revealed no difference in the variability of mid‐level stamen length between dimorphic and trimorphic populations. Mid‐level stamens were not more variable than long‐ and short‐level stamens within dimorphic populations. The consistent divergence in mid‐level stamens between the L and S morphs may reflect morph‐specific differences in the optimal position of mid‐level anthers for maximizing cross‐pollination and avoiding self‐fertilization.

The Evolution of Distyly: Pollen Transfer in Artificial Flowers

The Evolution of Distyly: Pollen Transfer in Artificial Flowers

Primary homostyly in Primula L. subgenus Sphondylia (Duby) Rupr. and the evolution of distyly in Primula.

We have studied eight species classified within Primula L. subgenus Sphondylia (Duby) Rupr. Two have monomorphic flowers and four have typically distylous flowers. P. floribunda Wall, includes both monomorphic and distylous races, while P. boveana Decres. has an incompletely discontinuous dimorphism for style length and pollen size, but is monomorphic for anther position. All the species have been tested and they are fully self-fertile. Evidence suggests that dimorphisms for style length (G/g), pollen size (P/p) and anther position (A/a) are each under independent genetic control. In the monomorphic P. verticillata, variations in stigma papilla length and style cell length appear to result from developmental correlates with style-length variation. Both the monomorphic species show some continuous variation for herkogamy. Several of the species studied show an incomplete development of the full distylous syndrome typical of most Primula species. If it is assumed that these represent evolutionary stages in the development of the full syndrome, and if it is assumed that diallelic incompatibility evolved after the evolution of distyly, then it would appear that the components of the distyly linkage group are likely to have evolved from a non-herkogamous ancestor in the following order: (i) short style mutant G; (ii) small pollen mutant p; (iii) low anther position mutant a.

The incompatibility relationships of tristylous species of Oxalis section Ionoxalis of southern Mexico

Ancestral incompatibility relationships occur in populations of tristylous species of Oxalis section Ionoxalis in southern Mexico. Legitimate pollinations lead to substantial seed production; illegitimate pollinations result in complete failure of seed production in most cases. Modifications of trimorphic incompatibility which have led to the evolution of distyly in northern populations of O. alpina were not detected in populations of the southern Mexican species. Rapid genomic changes which have occurred during the northward migration of Oxalis species apparently have been accompanied by the spread of incompatibility modifiers favoring the evolution of distyly.

The evolutionary genetics of sexual systems in flowering plants.

Population genetic studies of the evolution of breeding systems in flowering plants are reviewed. The selective advantage of a gene's increasing the selfing rate is stressed. In the evolution of outbreeding mechanisms, some strong disadvantage to selfing must therefore be acting; it is suggested that this disadvantage is inbreeding depression. Populations with no absolute barrier to selfing, and with intermediate levels of self-fertilization, appear to be the most likely starting state for the evolution of outbreeding mechanisms. There is some evidence for inbreeding depression in such populations. The evolution of distyly and dioecy are considered in some detail. An explanation for the existence of supergenes controlling these systems is proposed. The breakdown of distyly and tristyly are also considered. The evolution of recombination rates in selfing and outcrossing species is examined briefly.

Variation in Heterostylous Reproductive Systems Among Populations of Oxalis alpina in Southeastern Arizona

Numerous stages in the evolution of distyly from tristyly may be ob- served among populations of Oxalis alpina in southeastern Arizona. At one extreme, the mid form is common in populations and features of floral morphology are similar to those of typical trimorphic species. At the other extreme, the mid form is absent and few of the morphological features of tristyly have been retained. A spectrum of populations with intermediate mid frequencies and floral morphology connects these extremes. Modifications of style form representation and floral mor- phology are consistent with those expected in populations where modified incom- patibility has resulted in selection against the mid form. Disjunction of populations and variation in evolutionary rates have probably resulted in the diversity of inter- mediate reproductive systems occurring in this region.

Dispersal Patterns and the Evolution of Distyly in Oxalis alpina

Individuals from distylous and ti-istylous populations of Oxalis clpiina (Rose) Knuth (section Ionoxalis) from southeastern Arizona were crossed and the fitness of the resultant F1 hybrids analyzed to provide estimates of genetic divergence among populations. Crossability was highest when tristylous individuals were used as seed parents. Ci-osses among distylous populations resulted in the lowest seed set. Proportions of flowering F1 progeny were highest for crosses with ti-istylous individuals as seed parents, and lowest for distylous x distylous crosses. Pollen fer-tility of F1 progeny was higher in the tristylous x tristylous crosses than in distylous x distylous crosses. Results consistently indicated a higher degree of genetic relationship among tristylous populations than among distylous populations. A likely explanation for the present distribution of tristylous and distylous populations in Arizona is the initial migration of a tristylous race into this region, followed by disjunction into isolated populations due to Pleistocene drying. Following isolation, variation in evolutionary rate has apparently resulted in i-etention of tristyly in some populationis, and the independent evolution of distyly in those populations Which have diverged at the greatest r-ates. Crossability data and analysis of F1 fitness thus suggest a likely dispersal pattern for 0. alpina in southeaster-n Arizona as well as the evolutionar-y relationship between tristylous and distylous reproductive systems in this species. In southeastern Arizona, adjacent New Mexico and the Mexican states of Sonora and Chihuahua, populations of Oxalis alpina (Rose) Knuth (section Ionoxalis) occurring at forested higher elevations possess either tristylous or distylous reproductive systems. In distylous populations approximately half the individuals in the population produce flowers with long styles and short stamens, while the remaining individuals produce flowers with short styles and long stamens. Pollinations leading to fertilization and seed set are those occurring between the two forms. Selfpollinations and pollinations among individuals with identical floral form fail to result in seed set. The incompatibility relationships of distylous populations of 0. alpina are similar to those found in many distylous species occurring in other plant families. Three floral forms are found in the tristylous populations. Although the morphological features of the floral forms are similar to those found in many tristylous species, the incompatibility relationships are unusual, resembling those found in distylous populations. On the basis of these unusual incompatibility relationships, I have suggested that distyly has evolved from tristyly in this region (Weller, 1976a). Cytogeographic evidence supports the same general trend in the remaining species of section Ionoxalis (Weller and Denton, 1976). Tristylous and distylous populations of Oxalis alpina in southeastern Biological Sciences, University of Illinois. Chicago IL. 60680.

CYTOGEOGRAPHIC EVIDENCE FOR THE EVOLUTION OF DISTYLY FROM TRISTYLY IN THE NORTH AMERICAN SPECIES OF OXALIS SECTION IONOXALIS

A survey of haploid chromosome numbers of 18 North American taxa of Oxalis section Ionoxalis was initiated to determine the relationship between ploidal level, geographic distribution, and the occurrence of tristyly and distyly. Although chromosome numbers in the section are variable, the majority of tristylous populations are diploid. Among the distylous taxa a greater diversity of ploidal levels exists, with the higher chromosome numbers predominating. In section Ionoxalis the majority of the tristylous taxa are geographically restricted endemics of southern Mexico, while the distylous taxa have more extensive distributions ranging to the north. The association of diploidy and geographic endemism in the majority of the tristylous taxa suggests that these species are relictual. A few widespread tristylous taxa are polyploid, and often somewhat weedy. The probable derivation of widespread polyploid species from the restricted diploid endemics of southern Mexico appears to have been accompanied by the evolution of distyly from tristyly. The frequent association of polyploidy and distyly in section Ionoxalis has apparently resulted from the concurrence of two evolutionary trends: increase in ploidal level and the derivation of distyly from tristyly.

Cytogeographic Evidence for the Evolution of Distyly from Tristyly in the North American Species of Oxalis Section Ionoxalis

Cytogeographic Evidence for the Evolution of Distyly from Tristyly in the North American Species of Oxalis Section Ionoxalis