Heterostylous Species Research Articles

Biologia reprodutiva de Psychotria poeppigiana Mull. Arg. (Rubiaceae) em mata de galeria

Psychotria L. (Rubiaceae) é o gênero com mais espécies heterostílicas dentre as Angiospermas. O objetivo deste trabalho é descrever a biologia floral, fenologia, o sistema reprodutivo e os polinizadores de Psychotria poeppigiana Müll. Arg. As inflorescências são capitadas terminais, com brácteas vermelhas e flores amarelas apresentando dois morfos distintos: brevistiladas e longistiladas, caracterizadas por flores hermafroditas com diferentes comprimentos de estiletes e posicionamento oposto das anteras (hercogamia recíproca). Encontrou-se diferenças no tamanho das anteras, dos grãos de pólen e da superfície estigmática entre os morfotipos. Polinizações controladas mostraram que os morfotipos apresentam auto-incompatibilidade e intramorfo-incompatibilidade ao nível do estigma e do estilete. Os visitantes são pequenas vespas, abelhas, borboletas e beija-flores, que visitam as flores com maior freqüência no início da manhã. De acordo com a freqüência e eficiência no comportamento de transportar os grãos de pólen entre os morfos florais, o principal polinizador foi o beija-flor Thalurania furcata. O néctar é produzido em pequena quantidade (máximo de 8µl) e durante a abertura das flores, que ocorre entre 5 e 7h. A espécie forma agrupamentos devido à existência de reprodução vegetativa.

Convergent evolution of flower polymorphism in Narcissus (Amaryllidaceae)

Summary • We present new results on morphological variation for style polymorphism and perianth features in the seven species of Narcissus sect. Apodanthi and in N. pallidulus (sect. Cyclaminei), which exhibits a wide array of flower conditions: heterostyly, style dimorphism of variable reciprocity, and style monomorphism. • There is a significant association between perianth morphology and style polymorphism in the studied species. Among significant flower features, the two heterostylous species show pendulous flowers. Most style-dimorphic species have patent flowers, whereas monomorphic and one style-dimorphic species display erect flowers. • Interpretation of a chloroplast ( trn L- trn F) phylogeny of species representing most sections in the genus leads us to conclude that the two heterostylous species have independent origins, supporting previous hypothesis of convergence of heterostyly in Narcissus . Remarkable resemblance of flower features between both species indicates that pollinator activity might have driven flower convergence. •A second chloroplast ( trn T- trn L) phylogeny in sect. Apodanthi helps elucidate some evolutionary transitions in moulding heterostyly. Stylar dimorphism appears to precede distyly and style monomorphism. Population studies on style dimorphic and monomorphic species of Narcissus are congruent with a pollinator-mediated process also involved in a shift to monomorphism.

Pollen transfer patterns in a distylous plant with overlapping pollen‐size distributions

In this study we quantify the relative rates and amounts of between‐morph (legitimate) cross‐pollination, within‐morph (illegitimate) cross‐pollination and self‐pollination in a natural population of distylous Gaertnera vaginata (Rubiaceae) endemic to the oceanic island of La Réunion in the Indian Ocean. Since pollen size distributions of each morph overlap we develop a method, based on chi‐squared comparisons of observed to expected pollen size distributions, to quantify pollen transfer proficiencies. This method, unlike previous methods, does not assume an equal chance of pollen transfer for pollen grains in the region of overlap. The probability that a single pollen grain from a short‐styled plant undergoes legitimate pollen transfer to long‐styled flowers (4.19×10−2) was more than twice that for illegitimate transfer to other short‐styled plants (1.56×10−2). In contrast, the probability that a single pollen grain from a long‐styled flower undergoes legitimate pollen transfer to short‐styled flowers (1.65×10−2) was no greater than that of illegitimate pollen transfer to other long‐styled plants (2.15×10−2). The transfer proficiencies of individual pollen grains are thus highly asymmetric. However, because long‐styled flowers produce significantly more pollen, the ratio of legitimate to illegitimate pollen on the stigmas of short‐styled flowers (1.85) markedly exceeded that for long‐styled flowers (1.11). Short‐styled flowers incurred significantly higher levels of self‐pollination than long‐styled plants, emphasizing the importance for self‐pollination to be removed before comparing stigmatic pollen loads. The method we propose could be applied to other distylous species with pollen size overlap between morphs and thus allow for a more widespread study of the pollination ecology of heterostylous species.

Variation in Pollen Tube Inhibition Sites Within and Among Three Heterostylous Species of Rubiaceae

Pollen tube growth was examined following self, intramorph, and intermorph pollinations in three distylous species of Rubiaceae, the angiosperm family containing the greatest number of distylous taxa. Hand pollinations of Psychotria poeppigiana Muell. Arg., Psychotria chiapensis Standl., and Bouvardia ternifolia (Cav.) Schlecht. were followed by observation of pollen tube growth using fluorescence microscopy. Patterns of pollen tube growth were compared between conspecific floral morphologies, among type of illegitimate pollination, and among taxa. Short‐styled flowers of both Psychotria L. species had a majority of illegitimate pollen tube growth arrested within the stigma. In long‐styled Psychotria L. flowers, illegitimate pollen tube growth was inhibited either within the stigma or at various locations within the style. In the more distantly related B. ternifolia (Cav.) Schlecht., variable inhibition sites ranged from the stigma surface to the base of the style, among both short‐ and long‐styled flower...

Quantitative evaluation of pollen polymorphism in a tristylous weed,Lythrum salicaria(Lythraceae)

Tristylous breeding system consists of three different forms of flowers that differ reciprocally in the heights of stigmas and anthers within flowers. Apart from the style and stamen lengths, heterostylous species also demonstrate pollen and stigma polymorphisms. Tristylous Lythrum salicaria L. bears trimorphic, striate, tricolporate pollen with three true colpi and three pseudocolpi. Using a scanning electron microscope, we quantified pollen polymorphism in L. salicaria by measuring the length and diameter of pollen, and the length of colpi and pseudocolpi. Pollen grains from the long stamens are significantly larger than those from the mid stamens, followed by those from the short stamens. Despite significant differences in pollen size among long, mid, and short stamens, pollen morphometric traits demonstrate overlap among morphs. Pollen diameter also differed significantly between source populations. A discriminant function analysis separated long-level pollen from mid- and short-level pollen based on the canonical scores of measurements of pollen structure. The polymorphism of pollen in conjunction with that of the stigma may play a functional role in self-incompatibility mechanisms.Key words: Lythrum salicaria, purple loosestrife, Lythraceae, heterostyly, incompatibility, pollen polymorphism.

Ontogenetic differences in heterostylous plants and implications for development from a herkogamous ancestor.

Alternative ontogenetic pathways among heterostylous species of Rubiaceae may reflect differences in their evolutionary histories. In this study, measurements were taken at different developmental stages on a series of long-styled (LS) and short-styled (SS) buds of the heterostylous taxa Psychotria chiapensis, P. poeppigiana, and Bouvardia ternifolia (all Rubiaceae). Results indicated that modifications in growth rates of stamens relative to corollas in all three species led to differences in anther heights between LS and SS flowers. Distinct style heights for LS and SS flowers of P. chiapensis and P. poeppigiana originate in the earlier stages of bud development and are maintained as styles elongate at equal rates. This contrasts with B. ternifolia, which has differences in style heights resulting from unequal relative growth rates between floral morphs. The "approach herkogamous" floral morphology, defined by having stigmas positioned above anthers, has been proposed as a potential evolutionary precursor for heterostylous taxa. To examine this hypothesis, floral development of two species with approach herkogamous morphologies, Psychotria pittieri and P. brachiata, was compared to that of the three heterostylous taxa. Differences in the relative rates of style elongation for flowers of approach herkogamous versus heterostylous species predict additional steps in the original model for the evolution of heterostyly from an approach herkogamous ancestor. The diversity of heterostylous ontogenies found within Rubiaceae provides insight into potential evolutionary pathways for this sexual system in other angiosperm families.

ONTOGENETIC DIFFERENCES IN HETEROSTYLOUS PLANTS AND IMPLICATIONS FOR DEVELOPMENT FROM A HERKOGAMOUS ANCESTOR

Alternative ontogenetic pathways among heterostylous species of Rubiaceae may reflect differences in their evolutionary histories. In this study, measurements were taken at different developmental stages on a series of long-styled (LS) and short-styled (SS) buds of the heterostylous taxa Psychotria chiapensis, P. poeppigiana, and Bouvardia ternifolia (all Rubiaceae). Results indicated that modifications in growth rates of stamens relative to corollas in all three species led to differences in anther heights between LS and SS flowers. Distinct style heights for LS and SS flowers of P. chiapensis and P. poeppigiana originate in the earlier stages of bud development and are maintained as styles elongate at equal rates. This contrasts with B. ternifolia, which has differences in style heights resulting from unequal relative growth rates between floral morphs. The “approach herkogamous” floral morphology, defined by having stigmas positioned above anthers, has been proposed as a potential evolutionary precursor for heterostylous taxa. To examine this hypothesis, floral development of two species with approach herkogamous morphologies, Psychotria pittieri and P. brachiata, was compared to that of the three heterostylous taxa. Differences in the relative rates of style elongation for flowers of approach herkogamous versus heterostylous species predict additional steps in the original model for the evolution of heterostyly from an approach herkogamous ancestor. The diversity of heterostylous ontogenies found within Rubiaceae provides insight into potential evolutionary pathways for this sexual system in other angiosperm families.Corresponding Editor: K. Holsinger

Quantitative evaluation of pollen polymorphism in a tristylous weed, <i>Lythrum salicaria</i> (Lythraceae)

Tristylous breeding system consists of three different forms of flowers that differ reciprocally in the heights of stigmas and anthers within flowers. Apart from the style and stamen lengths, heterostylous species also demonstrate pollen and stigma polymorphisms. Tristylous Lythrum salicaria L. bears trimorphic, striate, tricolporate pollen with three true colpi and three pseudocolpi. Using a scanning electron microscope, we quantified pollen polymorphism in L. salicaria by measuring the length and diameter of pollen, and the length of colpi and pseudocolpi. Pollen grains from the long stamens are significantly larger than those from the mid stamens, followed by those from the short stamens. Despite significant differences in pollen size among long, mid, and short stamens, pollen morphometric traits demonstrate overlap among morphs. Pollen diameter also differed significantly between source populations. A discriminant function analysis separated long-level pollen from mid- and short-level pollen based on ...

Heterostyly in the Lamiaceae: The case ofSalvia brandegeei

Heterostyly rarely occurs in families with strongly zygomorphic flowers. For this reason Darwin (1877) doubted whether heterostyly would occur in the Lamiaceae and recent reviews have not reported the floral polymorphism in this family. Here we describe distyly in a rare species ofSalvia restricted to bluffs and seaward canyons on Santa Rosa Island (Santa Barbara Co., California) and northwestern Baja California (Mexico).Salvia brandegeei is morphologically distylous with populations composed of equal frequencies of long-and short-styled morphs differing reciprocally in stigma and anther position. Controlled hand pollinations demonstrated no significant differences in the seed set of self, intramorph or intermorph pollinations. Unlike most heterostylous species investigated,S. brandegeei does not possess diallelic incompatibility or ancillary polymorphisms of pollen and stigmas. We propose that the evolution of distyly inS. brandegeei may have been associated with an ecological shift to a new environment in which protandry failed to prevent increased levels of geitonogamy. Heterostyly was then selected because it increased the proficiency of cross-pollination. The origin of distyly in self-compatibleS. brandegeei is consistent with Lloyd and Webb's theoretical model for the evolution of distyly.

Quantitative evaluation of stigma polymorphism in a tristylous weed, Lythrum salicaria (Lythraceae)

Tristyly involves three different forms of flowers that differ reciprocally in the heights of stigmas and anthers within flowers. Apart from the style and stamen lengths, heterostylous species also demonstrate pollen and stigma polymorphisms. We quantified stigma polymorphism in tristylous Lythrum salicaria by measuring the stigma diameters, structure of papillae, and density and distribution of papillae on the stigma from flower samples of 201 individuals belonging to three morphs. The diameter of the stigma and the distribution of papillae were quantified using a scanning electron microscope, and the structure of papillae was determined using a light microscope. The stigma diameter in the long morph was significantly greater than in the mid and short morphs. While the density of stigmatic papillae was significantly greater in the mid and short morphs than in the long morph, the total number of papillae per stigma did not differ across morphs. The length and diameter of papillae at the apex, neck, and base were significantly greater in the long morph followed by the mid and short morphs. A discriminant function analysis separated the long morph from the mid and short morphs based on the canonical scores of measurements of papillae structure. The stigma polymorphism coupled with those of pollen may play a functional role in self-incompatibility mechanisms.

Pollen Dimorphism in Heterostylous Species of Oxygonum (Polygonaceae, Polygoneae)

The pollen dimorphism of eight African heterostylous species of Oxygonum Burch. ex Campd. is described for the first time using light and scanning electron microscopy. The pollen grains are mostly 3-colporate, subprolate to prolate with semitectate-reticulate exine. The pollen grains from short-styled (thrum) flowers are larger than those from long-styled (pin) flowers, with the ratios of thrum/pin pollen size varying from 1.01 to 1.35 in polar axis, and 1.07-1.62 in equatorial diameter. 0. sinuatum shows the most pronounced pollen dimorphism with respect to size and exine ornamentation. In other taxa, such as 0. dregeanum, 0. fruticosum and 0. stuhlmannii, the pollen dimorphism is weak. In the thrum flowers the exine lumina are slightly larger than in the pin flowers. There is, however, no significant difference in shape and in the number of apertures. Pollen polymorphism as a significant component of heterostyly and its functional significance and evolution are briefly discussed. More- over, heterostyly is reported here in four additional species of Oxygonum, i.e., 0. alatum, 0. frutico- sum, 0. pachybasis and 0. tenerum.

A collapsed tribe revisited: pollen morphology of the Isertieae (Cinchonoideae–Rubiaceae)

The pollen morphology of 41 species belonging to 19 genera of the tribe Isertieae sensu lato was investigated with LM and SEM. The problematic tribal delimitation and classification is reflected in the wide variation in many pollen morphological characters within the study group. This paper focuses on the recognition of distinct characters and states to describe this morphological variation. Nineteen pollen characters were retained for cladistic analysis. Coding problems for heterostylous species with pollen dimorphism are discussed. The palynological observations are confronted with existing hypotheses on phylogenetic relationships based on morphological and rbcL data. The tribes Mussaendeae (truncate ectocolpus ends, endocolpi with diverging ends) and Isertieae (relatively large pollen, endexine reduced to granular `islands', endocolpi with thickened lateral margins) in their new circumscription are supported palynologically. The Sabiceeae show more heterogenous pollen and do not appear as a well defined group in our analyses.

Predicted Genetic Consequences of Strong Fertility Selection Due to Pollinator Loss in an Isolated Population of Primula sieboldii

Previous studies demonstrated strong fertility selection for a self‐fertile, homostyle morph due to pollinator loss in an isolated population of Primula sieboldii, an endangered heterostylous species. To predict genetic consequences of the selection we developed a deterministic genetic model based on a classical “supergene” model, and we studied the effects of pollinator availability and inbreeding depression on temporal changes of morph frequencies through model simulation. Because of the severe pollinator limitation experienced by the population, fast, irreversible loss of the thrum morph from the population was predicted, even if high inbreeding depression was assumed. To prevent the breakdown of the normal breeding system of the species, morph frequency monitoring for timely active management should be implemented. Active management should include hand pollinations and pollinator therapy—reintroduction and reestablishment of suitable pollinator populations. The method we adopted in this study to parametrize pollinator availability can be used widely in conservation modeling for a range of plant species that have multiple mating types with different degrees of self‐incompatibility.

Reproductive Biology of Oxalis corniculata (Oxalidaceae): Style Length Polymorphisms and Breeding Systems of Japanese Populations

Abstract Style length polymorphisms and breeding systems of Oxalis corniculata populations in Japan were investigated. In Japan this species is composed of two floral morphs, a homostyled morph in which the level of the stigma and the anther of longer stamens are more or less the same, and a long‐styled morph in which the stigmas conspicuously protrude from the level of anthers of the longer stamens. Homostyled plants are common in artificially disturbed urban and ruderal habitats, whereas long‐styled plants occur mainly in less disturbed habitats of maritime Pinus thunbergii forests. Each of five populations examined in this study was exclusively composed of one or the other of the two floral morphs, with no mixed populations observed. Measurements of floral traits and reproductive parameters indicated that plants of homostyled populations exhibited characteristics of a typical autogamous breeding system, whereas those of long‐styled populations exhibited characteristics of predominant outcrossing. Crossing experiments revealed that the length of the stigmas and anthers of longer stamens, which characterizes the two floral morphs, is quantitatively inherited. The results obtained suggest that disassortative pollination among different floral morphs, which is commonly observed in some other heterostylous species, does not occur in O. corniculata populations in Japan. The origin of homostyled and long‐styled morphs in O. corniculata is also discussed.

Tristyly, self-compatibility and floral variation in Decodon verticillatus (Lythraceae)

Abstract Heterostyly typically involves reciprocal polymorphism in stamen and style lengths, physiological self- and intramorph-incompatibility, and a set of associated polymorphisms of pollen and stigma characters. This study examined floral morphology and compatibility relationships in the monotypic, herbaceous perennial Decodon verticillatus (Lythraceae). There have been conflicting reports on the occurrence of tristyly in the species, probably because of frequent loss of style morphs from populations in parts of the species' range. Floral morphology was examined using material collected from natural populations throughout the range. Detailed floral measurements revealed discrete trimorphism in style length and anther positioning in three populations. Data from two dimorphic populations showed similar patterns of floral polymorphism, except that both were missing the mid-styled morph. In one dimorphic population, there was evidence for modification in the length of mid-level stamens. Measurements in three populations indicated pronounced floral variability, including high frequencies of modified phenotypes with reduced stigma anther separation. Pollen size was only weakly differentiated among anther levels, and there were no differences in pollen production among anther levels or morphs. In contrast, stigma size and papilla length showed a strong negative correlation with style length; a pattern opposite to most heterostylous species. Experimental crosses performed under glasshouse conditions on plants from two populations showed a high degree of both self- and intramorph-compatibility. A comparative analysis of floral morphology showed that D. verticillatus is not unusual in terms of the precision and reciprocity of organ positioning compared with 13 other tristylous species.

Tristyly, self-compatibility and floral variation in Decodon verticillatus (Lythraceae)

Heterostyly typically involves reciprocal polymorphism in stamen and style lengths, physiological self- and intramorph-incompatibility, and a set of associated polymorphisms of pollen and stigma characters. This study examined floral morphology and compatibility relationships in the monotypic, herbaceous perennial Decodon verticillatus (Lythraceae). There have been conflicting reports on the occurrence of tristyly in the species, probably because of frequent loss of style morphs from populations in parts of the species' range. Floral morphology was examined using material collected from natural populations throughout the range. Detailed floral measurements revealed discrete trimorphism in style length and anther positioning in three populations. Data from two dimorphic populations showed similar patterns of floral polymorphism, except that both were missing the mid-styled morph. In one dimorphic population, there was evidence for modification in the length of mid-level stamens. Measurements in three populations indicated pronounced floral variability, including high frequencies of modified phenotypes with reduced stigma anther separation. Pollen size was only weakly differentiated among anther levels, and there were no differences in pollen production among anther levels or morphs. In contrast, stigma size and papilla length showed a strong negative correlation with style length; a pattern opposite to most heterostylous species. Experimental crosses performed under glasshouse conditions on plants from two populations showed a high degree of both self- and intramorph-compatibility. A comparative analysis of floral morphology showed that D. verticillatus is not unusual in terms of the precision and reciprocity of organ positioning compared with 13 other tristylous species.

Patterns of Female Fertility in Heterostylous Primula Sieboldii under Severe Pollinator Limitation

1 In order to identify the mode and intensity of fertility selection in a heterostylous population under severe pollinator limitation, morph composition and intraand intermorph pollen loads, fruit and seed set were investigated in an isolated population of the endangered, heterostylous species Primula sieboldii. 2 Seventy-six genets were classified as either of the pin or thrum morph on the basis of measurements of stigma-anther separation and relative anther height, except for one genet that exhibited a short homostylous phenotype. There was a 1:1 ratio of pin and thrum plants in the population. 3 Measurements of stigmatic pollen load indicated that legitimate pollination (i.e. by the opposite morph) was extremely limited. Female fertility was generally low but varied significantly among style morphs and among genets within morphs. The pin morph showed significantly higher fertility than the thrum morph. High fruit and seed set was recorded for the short homostyle. 4 Legitimate pollination by hand resulted in a significant increase in fruit and seed set except for the homostyle where high spontaneous seed set already occurred. Intragenet pollination or illegitimate (i.e. intramorph) pollination resulted in no seed set. 5 It was concluded that pollen limitation is largely responsible for the low female fertility of plants in the population. Under severe pollinator limitation, it is possible that the self-fertile homostyle will have a selective advantage and will spread in the population.

The biology of Canadian weeds. 100. Lythrum salicaria

Lythrum salicaria is a serious weed of wetlands in Canada, particularly in Ontario and Quebec. Indeed some assessments suggest that this exotic is now responsible for the conversion of more wetland habitat than is current human development pressure¡ Lythrum is a heterostylous species and clones by means of root buds. Despite its tristylous breeding system, Lythrum is a successful colonizer, and can produce prodigious numbers of seeds. It is likely that control can be achieved by hand-pulling in low-density populations, but once the species is established it generally becomes abundant and often approaches a monoculture. This species is particularly difficult to control because of its strong competitive ability, the extreme sensitivity of wetland habitats, and the likelihood of serious repercussions for wetland wildlife and fisheries if herbicides are used to control it. We see better possibilities for control through cultural techniques (e.g., manipulation of water levels to favour native species), enhancement of North American herbivores, and, possibly, the introduction of biological control agents from Europe and Asia.Key words: Purple loosestrife, Lythrum salicaria, wetlands, introduced weed

Palynological variation in primula L. subgenus Sphondylia (Duby) Rupr., and the relationship of this group to Dionysia Fenzl.

summary Primula subgenus Sphondylia is composed of eight localized and probably relictual taxa distributed from Ethiopia to the west Himalaya. It is considered to occupy an ancestral position in the genus, and to demonstrate stages in the evolution of dimorphic heterostyly. Previous authors have suggested that the heterostylous genus Dionysia evolved from forerunners of this group.It has previously been reported that, in five of the species, only prolate 3‐colporoidate pollen is found, dimorphic in size for heterostylous species. However, the pollen of the heterostylous species P. edelbergii, P. gauheana and P. darisii is dimorphic for shape and colpus number, as well as for size. Thus, our study reports for the first time, a major morphological pollen dimorphism, and 1‐ and 2‐colpor(oid)ate pollen in the Primulaceae.We found that three distinct trends in the development of pollen dimorphism can be traced in this group, two of which appear to have no major phyletic implication. However, it is possible that P. floribunda represents phyletic links between subgenus Sphondylia and later heterostylous developments in Primula.Pollen in Dionysia is said to be weakly dimorphic for shape and colpus number, and our findings agree with this. We suggest that Dionysia is not closely related to Primula subgenus Sphondylia and that strong superficial resemblances between certain taxa in these groups may have resulted from parallel evolution.

A new heterostylous species of Streptopetalum (lurneraceae) from Somalia

Streptopetalum arenarium sp. nov., a heterostylous species apparently closely related to the homostylous 5. hildebrandtü in Kenya and north Tanzania, is described from deciduous bushland on sand in central and southern Somalia.