Tristylous Species Research Articles

RECONSTRUCTION OF THE EVOLUTION OF REPRODUCTIVE CHARACTERS IN PONTEDERIACEAE USING PHYLOGENETIC EVIDENCE FROM CHLOROPLAST DNA RESTRICTION-SITE VARIATION.

We reconstructed the phylogenetic history of Pontederiaceae using chloroplast DNA restriction-site variation from approximately two-thirds of the species in this family of aquatic monocotyledons. The molecular phylogeny was used to evaluate hypotheses concerning the evolution of reproductive characters associated with the breeding system. The family has four main genera, two of which (Eichhornia and Pontederia) have tristylous, predominantly outcrossing species, while two (Monochoria and Heteranthera) have enantiostylous taxa. Self-incompatibility is restricted to some but not all tristylous species. In Eichhornia and Pontederia, predominantly selfing species with small monomorphic flowers (homostyly) have been hypothesized to result from the multiple breakdown of tristyly. Restriction-site variation provided a well supported phylogeny of ingroup taxa, enabling the mapping of reproductive characters onto trees. Two contrasting optimization schemes were assessed, differing in the relative weights assigned to shifts in character states. The reconstructed sequence of floral character-state change was used to assess competing hypotheses concerning the origin and breakdown of tristyly, and the relationships between tristylous and enantiostylous syndromes. Our results indicate that the class of optimization scheme used was the most critical factor in reconstructing character evolution. Despite some topological uncertainties and difficulty in reconstructing the primitive floral form in the family, several broad conclusions were possible when an unordered, unequally-weighted optimization scheme was used: (1) tristyly originated either once or twice, while the occurrence of enantiostyly in Monochoria and Heteranthera was always found to have independent origins; (2) tristyly has repeatedly broken down leading to selfing, homostylous taxa; and (3) self-incompatibility probably arose after the origin of floral trimorphism, a sequence of events that conflicts with some evolutionary models.

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.

Multiple origins of self‐fertilization in tristylous Eichhornia paniculata (Pontederiaceae): Inferences from style morph and isozyme variation

AbstractPopulations of Eichhornia paniculata (Pontederiaceae) exhibit a wide range of mating systems, from predominant outcrossing to high levels of self‐fertilization. The origin of self‐fertilization in this tristylous species is associated with the loss of style‐length morphs from populations and the spread of self‐pollinating, floral variants. We examined geographic variation in style morph and allozyme frequencies to determine whether the loss of style morphs and transition to selfing could have multiple origins in E. paniculata. Surveys of floral variation in 167 populations from six states in northeastern Brazil revealed that at least one style morph was absent from 29.3%. Non‐trimorphic populations occurred in all states and ranged in frequency from 9% in Ceará to 68% in Alagoas. Selfing variants occurred in 8.5% and 55% of trimorphic and non‐trimorphic populations, respectively, and were distributed among five of six states with primary concentrations in Alagoas and Pernambuco. A comparison of electrophoretic variation at 24 isozyme loci in 28 trimorphic, 13 dimorphic and 3 monomorphic populations indicated that non‐trimorphic populations contained 84% of the allelic variation present in trimorphic populations and were markedly differentiated from one another. Analyses of genetic distance and the distribution of rare alleles indicated that non‐trimorphic populations were often more similar to neighbouring trimorphic populations than to one another. Populations with selfing variants occurred at low frequency in three genetically distinct parts of the range. These results, in combination with genetic and morphological evidence suggest that style morphs are lost repeatedly from populations of E. paniculata and that selfing variants may have originated on at least three separate occasions in northeastern Brazil.

STOCHASTIC LOSS OF STYLE MORPHS FROM POPULATIONS OF TRISTYLOUS LYTHRUM SALICARIA AND DECODON VERTICILLATUS (LYTHRACEAE).

Despite the theoretical importance of stochastic processes in evolution there have been few empirical studies of the interaction between genetic drift and selection on the maintenance of polymorphisms in plant populations. We used computer models to investigate the interaction between drift and frequency-dependent selection in affecting style morph frequencies in populations of tristylous species. Drift produces a distinct pattern of morph frequency variation involving: 1) the loss of the S morph and, to a lesser extent, the M morph; 2) no consistent bias in frequencies within populations; 3) a restricted pattern of variation involving a deficiency of one morph and equal excesses of the other two. Morph frequencies were surveyed in 137 populations of Lythrum salicaria from both its native range in Europe (N = 35) and recent adventive range in Ontario (N = 102), and 133 populations of Decodon verticillatus from four regions in eastern North America with different glacial histories to assess these theoretical predictions. There was a negative relationship between morph loss and population size in both species; the relationship was weaker in D. verticillatus than in L. salicaria. Morph loss was more frequent in the adventive than native range of L. salicaria, and in populations of D. verticillatus from glaciated northern regions compared with the unglaciated southern portion of its range. Simulations incorporating variation in life history, regeneration strategy and mating patterns revealed that the degree of morph loss was strongly influenced by year to year survival, clonal propagation, self-fertilization and departures from disassortative mating. Comparing the pattern of morph frequency variation between species supported these predictions. Morph loss was lower in self-incompatible L. salicaria (0% in Europe; 23% in Ontario), which reproduces through seed compared to self-compatible, clonal D. verticillatus (52%). A stochastic model provides the most parsimonious explanation for observed patterns of morph frequency variation in both species.

HISTORICAL FACTORS AND ANISOPLETHIC POPULATION STRUCTURE IN TRISTYLOUS PONTEDERIA CORDATA: A REASSESSMENT.

Theoretical models of floral-morph frequencies in tristylous species predict a single equilibrium with all three morphs represented in equal proportions (isoplethy). North American populations of Pontederia cordata exhibit considerable heterogeneity of morph frequencies between populations, with the short-styled morph often in excess of isoplethic expectations and the long-styled morph commonly underrepresented. In a previous study, it was proposed that anisoplethic population structure in P. cordata is the result of differential male fertility, owing to genetic differences in pollen production among the morphs. In this study, the influence of historical factors on morph frequencies prior to equilibrium was investigated using a deterministic computer model. Nonequilibrium frequencies are strongly influenced by the genotypes of founding individuals, and, because tristyly is under the control of two diallelic loci, phenotypic equilibrium is approached asymptotically. The model indicates that in nonequilibrium populations the short-styled morph will be in excess and the long-styled morph will be underrepresented. This suggests that historical factors play an important role in determining population structure in P. cordata. Several features of the population ecology of the species lend support to this interpretation. Historical factors should be taken into account when interpreting data from population surveys of morph frequencies in tristylous species and of other genetic polymorphisms not under single-locus control.

Tristyly in Pontederia cordata (Pontederiaceae)

Pontederia cordata L. (Pontederiaceae) is a perennial, entomophilous, emergent aquatic and possesses a tristylous breeding system. A survey of 74 North American populations indicates that populations usually contain the three floral morphs. A strong pollen trimorphism is associated with differences in stamen and style length among the morphs. Pollen size is proportional to stamen height, while pollen production is inversely proportional. There are two size classes of anthers in P. cordata. Long-level anthers of mid- and short-styled plants and mid-level anthers of the short-styled morph are significantly larger than short-level anthers of long- and mid-styled plants and the mid-level anthers of the long-styled morph. The larger mid-level anthers of the short-styled morph produce nearly twice as many pollen grains as the equivalent level in the long-styled morph. It is suggested that this difference may be associated with varying patterns of stamen insertion and development in the floral morphs.Comparisons of various reproductive parameters among the floral morphs in natural populations suggest that there are no significant differences in flowering patterns, inflorescence and flower production, seed production, and germination levels. In addition, bumble bees show no apparent preferences among the floral morphs during foraging activity. Tristyly appears to be a relatively stable breeding system in P. cordata in comparison with tristylous species of the related Eichhornia.

Style morph distribution in new world populations of Eichhornia crassipes (Mart.) Solms-Laubach (water hyacinth)

Eichhornia crassipes (Mart.) Solms-Laubach (Water Hyacinth) exhibits the rare genetic polymorphism tristyly. Populations of tristylous species usually contain three floral morphs which differ in style length and stamen height. In a survey of style morph representation in 196 New World populations, 77.0% were monomorphic, 18.4% were dimorphic and 4.6% were trimorphic. The three floral morphs were found in Brazil and Argentina. The short-styled morph predominated in the Amazon Basin and Mato Grosso of Brazil but was absent from North and Central America and the Caribbean. The mid-styled form predominated in the introduced range of the species and in parts of the native range. The long-styled form rarely gains ascendancy over the other style morphs and occurred less frequently in both the native and introduced ranges. The patterns of style morph distribution suggest Amazônia as the centre of origin of E. crassipes, with natural spread from there to other areas of the South American continent and introduction by man to North and Central America and the Caribbean.

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.

Features of Pollen Flow in Dimorphic Species of Lythrum Section Euhyssopifolia

The North American Lythrum lineare L., L. alatum Pursh, L. curtissii Fernald, and L. californicum T. & G. have distylous flowers that differ in a number of traits. In the two species examined, pins have a stronger incompatibility system than thrums. Pins outnumber thrums in natural populations, but the ratio of the two may change radically during the course of a year, probably as a result of sexual reproduction. Exotic honeybees visiting L. californicum exhibited preferential collection of pin pollen over thrum pollen. The relative proportion of pin and thrum pollen grains transferred to stigmas is not dependent upon the proportion in which these pollen grains are produced in a population. Analyses of stigmatic pollen loads of L. lineare and L. californicum indicate very high levels of intramorph pollen flow. Although distyly is likely derived from tristyly in Lythrum, pollen flow patterns in trimorphic species seem to operate more “efficiently” than in dimorphic ones. It is probable that distyly has evolved from tristyly several times in the Lythraceae, but comparisons between pollen flow patterns in distylous species and those in a tristylous species provide no clear insights into the selective pressures that have led to this fundamental change in floral morphology and reproductive system.

FEATURES OF POLLEN FLOW IN DIMORPHIC SPECIES OF LYTHRUM SECTION EUHYSSOPIFOLIA

The North American Lythrum lineare L., L. alatum Pursh, L. curtissii Fernald, and L. californicum T. & G. have distylous flowers that differ in a number of traits. In the two species examined, pins have a stronger incompatibility system than thrums. Pins outnumber thrums in natural populations, but the ratio of the two may change radically during the course of a year, probably as a result of sexual reproduction. Exotic honeybees visiting L. californicum exhibited preferential collection of pin pollen over thrum pollen. The relative proportion of pin and thrum pollen grains transferred to stigmas is not dependent upon the proportion in which these pollen grains are produced in a population. Analyses of stigmatic pollen loads of L. lineare and L. californicum indicate very high levels of intramorph pollen flow. Although distyly is likely derived from tristyly in Lythrum, pollen flow patterns in trimorphic species seem to operate more “efficiently” than in dimorphic ones. It is probable that distyly has evolved from tristyly several times in the Lythraceae, but comparisons between pollen flow patterns in distylous species and those in a tristylous species provide no clear insights into the selective pressures that have led to this fundamental change in floral morphology and reproductive system.

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.

Tristyly in Eichhornia crassipes (Mart.) Solms (Water Hyacinth)

Tristyly in Eichhornia crassipes (Mart.) Solms (Water Hyacinth)

The genetic control of tristyly in Oxalis section Ionoxalis

Progeny ratios from crosses utilising six tristylous species of Oxalis section Ionoxalis indicate that expression of style forms in this section is generally controlled by two loci which are tightly linked. In diploid species one locus controls the expression of the short style form versus non-short, while the second locus controls the expression of the mid and long style forms. The short allele is epistatic to the mid-long locus, where mid is dominant to long. Control of tristyly is similar in polyploid species, although linkage cannot be detected because of chromosome duplication. Fixation or loss of the mid-long locus would allow the remaining short versus non-short locus to segregate equal numbers of shorts and longs, thus providing a genetic basis for control of distyly.

POLLEN FLOW IN LYTHRUM JUNCEUM, A TRISTYLOUS SPECIES

SUMMARYStudies of the pollen loads present on stigmas of flowers of the self‐incompatible tristylous Lythrum junceum in Morocco indicate that the position of the stigma has an important effect on the proportion of pollen from long‐level anthers that is deposited on the stigmas. The greatest amount of large pollen from the longest set of stamens is found on stigmas of long‐styled flowers. Because of the inability to discriminate between small pollen grains from mid‐level anthers and those from short‐level anthers it is not clear how stigma position may influence the distribution of these small pollen grains. In the Moroccan population studied, plants with long‐, mid‐, and short‐styled flowers are present in a 1:1:1 ratio. The chief pollinator during the period of study was the honey bee, Apis mellifera, which preferentially removes large pollen grains from flowers. Longs and Mids produce approximately equal numbers of pollen grains per flower, and Shorts produce c. 77% of the pollen of each of these two forms. Acetolysis of stigmas provides more accurate estimates of stigmatic pollen loads than does microscopic examination of intact stigmas, although the proportional representation of the two size classes of pollen is similar with either method. This study represents the first published analysis of pollen flow in a tristylous species within its native range and suggests that tristyly serves to promote compatible pollinations, thus supporting the classical interpretation of the biological significance of tristyly.