Consequences of a mixed reproductive system in the hog peanut,Amphicarpaea bracteata, (Fabaceae)

Summary The forest annual, Amphicarpaea bracteata L. can reproduce via aerial chasmogamous, aerial cleistogamous, and subterranean cleistogamous flowers. Both plant size and light intensity influenced the utilization of the three modes of reproduction. chasmogamous and aerial cleistogamous flower number and the ratio of chasmogamous flowers to the total number of aerial flowers increased with plant size. The latter demonstrated a shift to xenogamy and outbreeding in larger plants. Light intensity indirectly influenced reproductive modes through its infuence on plant size. Seed set by both types of aerial flowers was low and unrelated to plant size. Subterranean seed number and the total dry weight of subterranean seeds per plant increased with size. The subterranean seeds of Amphicarpaea bracteata are thirty-four times larger than the aerial seeds (fresh weight). Under field conditions, subterranean seeds had greater germination after one year than acrial seeds. The plants arising from subterranean seeds were significantly larger and more fecund than those from aerial seeds. Seeds produced by aerial cleistogamous, hand selfpollinated chasmogamous, and naturally pollinated chasmogamous flowers had equivalent germination rates and produced plants of equal size and fecundity. This suggests that the outbred progeny from chasmogamous flowers have no advantage over the inbred progeny from aerial cleistogamous flowers.     

Why is cleistogamy a selected reproductive strategy in Impatiens capensis (Balsaminaceae)?

Cleistogamy (self-fertilization in closed flowers) differs from chasmogamy (open-pollinated fertilization) mainly in sustaining selfing. Why numerous species develop both of the reproductive modes on the same individuals has long puzzled biologists. In a novel hypothesis presented here, I propose that cleistogamy could be a means by which inbred lines are created and maintained in natural populations; these lines would continuously experience self-improvement via natural selection and via crosses among lines at the chasmogamous flowers to benefit the populations. Supporting evidence for the hypothesis was found in Impatiens capensis where cleistogamous ovules were fertilized proportionately less (56%) than chasmogamous ovules (67%) in natural populations, but crosses among cleistogamous progeny in the greenhouse led to a nearly 10% increase of fertilized chasmogamous ovules. I established a novel fitness model specific to the cleistogamous species to further examine how various aspects of the mating system affect plant performance. A low inbreeding depression (0.07) was consequently found for the surveyed natural populations of I. capensis , suggesting that the individual-level percentage of cleistogamy and the population-level selfing rate may have evolved in the direction of reducing the overall inbreeding depression. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 75 , 543–553.     

Plasticity in the reproductive strategy of a clonal cleistogamous species, <Emphasis Type="Italic">Pseudostellaria heterophylla</Emphasis>

The presence of cleistogamous and chasmogamous flowers on the same plant individual is considered to represent a “mixed” reproductive strategy. If a cleistogamous species also exhibits clonal propagation, then competition for limited resources is assumed to exist among the three reproductive modes. To date, however, the relationships and interactions among cleistogamous, chasmogamous, and clonal modes of reproduction have received little attention. In this study, we performed manipulative experiments to investigate the interactions among these different types of reproduction in the perennial herbaceous plant species Pseudostellaria heterophylla. The results showed that 66.4%–87.6% of individuals produce chasmogamous flowers and that the fruiting rates of these flowers in each surveyed population were between 23.5% and 77.4%. Furthermore, we found that 8.3% of the individuals of this species show inbreeding depression. We also detected significant negative correlations between the production of chasmogamous and cleistogamous flowers and between cleistogamous flower production and root tuber mass. However, chasmogamous flower production in an individual plant was found to have little influence on its subsequent clonal propagation. We propose that the plasticity of reproductive strategies observed in P. heterophylla is due to changes in the resource pool and resource allocation.     

A unique growth pattern associated with cleistogamy in a tropical legume, Vigna minima (Roxb.) Ohwi & Ohashi (Leguminosae)

Obligate subterranean cleistogamy, observed in a natural population of Vigna minima , is associated with the production of one or two negatively geotropic, leafy shoots and several positively geotropic, highly pigmented, leafless shoots. The latter branch profusely after penetrating the soil and produce much reduced, cleistogamous flowers. The undehisced anthers contain germinated pollen grains. The seeds developing from the cleistogamous flowers differ in size, weight and surface features from those produced by the chasmogamous flowers of other natural populations within the species.     

Reproductive Biology of an Amphicarpic Annual, Polygonum thunbergii (Polygonaceae): Spatio-temporal Changes in Growth, Structure and Reproductive Components of a Population over an Environmental Gradient

Abstract The process and mechanisms of spatio-temporal changes in growth, population structure, as well as various yield and reproductive components of a population of an amphicarpic annual, Polygonum thunbergii (Polygonaceae), with two reproductive systems (aerial chasmogamous flowers and subterranean cleistogamous flowers) along an environmental gradient (light, moisture and soil nitrogen levels) were investigated in the field.
The results clearly demonstrate that growth and allocation patterns, population structure, and reproductive output of individuals changed sharply along the environmental gradient in response to seasonal and spatial changes in resource availability. Models predicted that light conditions bring about one-sided competition, whereas nutrient conditions in the soil engender two-sided competition. As expected, the degree of one-sided competition was prominent in the case of a planophile, Polygonum thunbergii. Allocation patterns, seed outputs, individual seed size as well as relative energy costs of chasmogamous and cleistogamous seed as affected by light and nutrient levels were also critically analyzed. The most noteworthy finding was that the size of chasmogamous seeds sharply decreased in response to a decrease in the light regime, while cleistogamous seed size remained constant along the gradient. However, relative cost of both chasmogamous and cleistogamous seeds sharply increased with decrease in the light level, reflecting different degrees of environmental stress, biotic interference, or both.     

Evolution of floral dimorphism in a cleistogamous annual, <Emphasis Type="Italic">Impatiens noli-tangere</Emphasis> L. occurring under different environmental conditions

The resource allocation models for the evolution of a mixed production of cleistogamous and chasmogamous flowers were tested in four natural populations of Impatiens noli-tangere L. When we incorporated the estimated parameter values into our basic model, under the assumption that the environmental conditions did not change through the reproductive season, the model predicted the obligate chasmogamy in all four populations. However, including the fluctuation of the fertility of chasmogamous flowers in the model, the seasonal switching of chasmogamous and cleistogamous flower production becomes an evolutionary stable strategy, which explains the reproductive behavior of the individuals in two populations. Only after the relationship between the geitonogamy of chasmogamous flowers and the number of chasmogamous flower production was considered in the model did the simultaneous production of both of the dimorphic flowers become an evolutionary stable strategy. Further, the complete model clarifies the reproductive behavior of the individuals in the other two populations.     

Genetic diversity of an amphicarpic species, Amphicarpaea edgeworthii Benth. (Leguminosae) based on RAPD markers

Amphicarpaea edgeworthii Benth. is an amphicarpic legume widespread in China. Amphicarpy describes the phenomenon that a plant produces aerial as well as subterranean fruits. A. edgeworthii can reproduce via three kinds of flowers: aerial chasmogamous flowers, aerial cleistogamous flowers, and subterranean cleistogamous flowers. Although there are some studies on the population genetic structure of species with both chasmogamous and cleistogamous flowers, none has been done for that of an amphicarpic species so far. The present study uses random amplified polymorphic DNA (RAPD) to assess level and pattern of genetic variation in 15 natural populations of A. edgeworthii. A total of 131 stable and clearly scored RAPD bands were achieved from 13 primers. The average genetic diversity within populations estimated by Shannon's information index was 0.218 at the population level, but ranged from 0.119 to 0.302, which was significantly different (P < 0.01). Different statistical analyses revealed a high level of genetic differentiation among populations (G_ST = 0.473–0.527). Thus, the pattern of genetic structure of A. edgeworthii is consistent with that of an inbreeding species.     

Floral sex ratios and gynomonoecy in Solidago (Asteraceae)

Gynomonoecy is the sexual system in which individual plants bear both female and bisexual flowers. Little attention has been paid to the adaptive significance of this sexual system, which is particularly prevalent in the Asteraceae. We investigated one hypothesized advantage of having two flower types, namely that this arrangement permits flexibility in allocation of resources to male and female reproductive functions. We examined six species of goldenrod ( Solidago ), a genus of gynomonoecious, perennial herbs. In greenhouse experiments, we varied one or more of three environmental variables – light, nutrients and water – and/or examined heads in different positions on the plants. Most variables had little or no effect on the proportion of ray flowers. Significant effects were found for light in 0 of 5 experiments, for nutrients in 4 of 9 experiments and for water in 0 of 3 experiments. Heads in different positions in the inflorescence differed in the proportion of ray flowers in half of the experiments, though the differences were small. We also monitored temporal patterns in four species and found that the proportion of ray flowers increased significantly over the blooming period and the number of flowers per head declined. Because of the small number of significant effects and their modest magnitude, we conclude that the presence of two flower types in goldenrods is probably not advantageous in allowing flexibility in sex expression. It seems likely that this sexual system has been more important either in increasing pollinator attraction or in reducing pollen–pistil interference. The small observed changes in floral ratios were generally accompanied by changes in disc size in a manner consistent with an explanation based on allometry.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 413–422.     

Cleistogamy in the rare high Andean perennial herb Cryptantha capituliflora (Boraginaceae)

 Axial and apical flowers of Cryptantha capituliflora were analyzed with regard to morphology and pollen tube growth to assess the occurrence of cleistogamy. Although intermediate floral forms do occur, cleistogamous flowers were significantly smaller than chasmogamous flowers, had fewer anthers, and showed a distinctive stigmatic surface. Chasmogamous flowers can be cross-pollinated. Nevertheless, the growth of self-pollen tubes in few chasmogamous buds jointly with flower characters suggests that these flowers can probably produce fruits through autonomous selfing. The mean seed number per fruit did not differ between fruits from chasmogamous and cleistogamous flowers. Cleistogamous flowers were only observed in axial inflorescences, which are completely covered by the leaf. Other species of section Cryptantha also show the same trend, with cleistogamous flowers located in the lower half of the stems. This pattern is discussed in relation to dissimilarities in the outcrossing opportunities between flower types within the plant. Received May 22, 2002; accepted November 14, 2002 Published online: March 20, 2003     

Reproductive investment in a cleistogamous morph of <Emphasis Type="Italic">Polygonum jucundum</Emphasis> (Polygonaceae)

Cleistogamy, a breeding system with permanently closed and self-pollinated flowers, is expected to assure reproductive success at a lower cost. Previous studies have inferred the occurrence of cleistogamous flowers in Polygonum, but there are no detailed studies on their reproductive investment compared with that of the chasmogamous flowers in this genus. Here, we studied a cleistogamous morph of P. jucundum to investigate the investment in pollen number, tepal and nectary size. The number of pollen grains per flower was counted with a light microscope. Nectaries and perianths were observed via scanning electron microscope and light microscopy, photographed and measured via ImageJ. The perianths of the cleistogamous flowers, as well as the pollen numbers and nectary sizes, were significantly smaller than those of the chasmogamous flowers. The pollen numbers of the CL flowers were seven times lower than those in the CH flowers. The tepal areas of the CL flowers were, on average, approximately 38% those of the CH flowers. The nectary areas of the CH flowers were almost twice those of the CL flowers. In addition, the nectaries of the cleistogamous flowers were degenerated and inconspicuous, in distinct contrast with the well-developed and conspicuous nectaries of the chasmogamous flowers. Self-fertilization was completed and produced seeds. The cleistogamous P. jucundum, compared with chasmogamous individuals, exhibited lower costs in male function, pollinator attraction and reward structure investment. This cleistogamy appears to be favourable for the plant reproduction under suboptimal conditions.     

DISPERSAL OF HETEROMORPHIC SEEDS IN AMPHICARPAEA BRACTEATA (FABACEAE)

The dispersal of the chasmogamous, aerial cleistogamous, and subterranean cleistogamous seeds of Amphicarpaea bracteata was examined. The chasmogamous and aerial cleistogamous seeds are ballistically dispersed. Chasmogamous seeds were dispersed farther than the aerial cleistogamous seeds due to the height advantage of the chasmogamous pods. There was no difference in the firing angle or the initial velocity of the seeds discharged from the two aerial pod types. The subterranean cleistogamous seeds are “dispersed” the shortest distance by the elongation of runners. Differential dispersal of the three types of seeds may be a factor involved in the evolution of cleistogamy in A. bracteata.     

青藏高原东缘块茎堇菜鳞茎分配的个体大小依赖性

块茎堇菜(Viola tuberifera)为青藏高原特有两型闭锁花植物,属多年生草本,具独特的混和交配系统,既可通过早春开放花异花受精和夏季地上地下闭锁花自花受精有性繁殖,还可通过秋季新鳞茎无性繁殖产生后代。高山环境下,异花受精常因花粉限制而无法正常进行,自花受精和克隆繁殖成为保障植物种群正常繁衍的不二之选,而克隆繁殖更能在植株资源消耗最小的情况下保障子代的存活。该文以青藏高原东缘高寒草甸的混合繁育植物块茎堇菜为研究对象,探索其生长期内鳞茎分配的个体大小依赖性,以及植株如何权衡鳞茎的资源分配以适应个体大小的变化。结果表明：块茎堇菜生活史阶段的鳞茎分配具有个体大小依赖性,鳞茎分配与个体大小呈极显著负幂指数相关关系(P<0.01),个体越大,鳞茎分配越小;反之,个体越小,鳞茎分配越高。即块茎堇菜对鳞茎的资源投入受个体大小的制约,通过鳞茎分配比例的高低响应植株自身资源状况的变化,保障在高寒环境下植物种群的生存和繁衍。该研究结果为高山植物克隆繁殖的生活史进化提供了依据。     

关于四棱草的二型花的研究

陈介(1964)在四棱草属(Schnabelia)中发现具有二型花,即开花授粉型的花(chasmogamous)和闭花授粉型的花(cleistogamous)。他根据当时所掌握的材料,认为二型花"似乎是异株"。笔者在采自安徽祁门的四棱草(S.oligophylla)上发现,二型花无疑是生在同一个体上,但这两种花的花期和花的着生位置是不同的。开花授粉型花的花期早,持续时间短,为一次性开花;闭花授粉型的花是不断地从叶腋发出的,花期持续时间长。     

RESOURCE ALLOCATION AND REPRODUCTION IN POPULATIONS OF AMPHICARPUM PURSHII (GRAMINEAE)

Five New Jersey populations of Amphicarpum purshii (an annual panicoid grass) were investigated as to total allocation of biomass to reproduction and its distribution between aerial chasmogamous and subterranean cleistogamous inflorescences. Germination of both types of seed was documented, for the first time, in not only the field but under three laboratory temperature regimes. Overall, approximately 29 % of the shoot biomass was allocated to reproduction. On a population basis, subterranean inflorescences accounted for 37–100 % of the reproductive biomass, and these seed (5 × heavier but fewer in number) were the source of most surviving seedlings. Subterranean spikelets contained caryopses significantly more frequently than aerial spikelets. The ratio of the number of viable aerial seed to the number of viable subterranean seed increased from 0/4 to 4/2 with recentness and/or frequency of disturbance. As a pioneer species in secondary succession, Amphicarpum purshii produces a larger subterranean propagule, with greater seedling vigor and a higher probability of local reproductive success, and also a smaller aerial propagule in larger numbers with potentially greater genetic variability.     

Heterocarpy in Salvia roemeriana (Lamiaceae)

Although Salvia roemeriana has long been known to produce both chasmogamous and cleistogamous flowers, the mericarps resulting from those flowers have received little attention. We germinated seeds from chasmogamous and cleistogamous flowers, recorded germination times, and fit time‐to‐germination, three‐parameter log‐logistic regressions to analyze differences in germination progress. Additionally, we compared the mass and size of mericarps from both kinds of flowers. Our results show that the mericarps produced from chasmogamous flowers are larger and heavier than those from cleistogamous flowers. In addition, seeds from chasmogamous flowers had a longer dormancy than those from cleistogamous flowers. This is the first report of heterocarpy in Salvia and in the family Lamiaceae. Together, cleistogamy and heterocarpy are a multiple strategy that may be advantageous in heterogeneous environments.     

The maintenance of mixed mating by cleistogamy in the perennial violet Viola septemloba (Violaceae)

The production of both potentially outcrossed (chasmogamous) and obligately self-fertilized (cleistogamous) flowers presents a clear exception to the prediction that the only evolutionarily stable mating systems are complete selfing and complete outcrossing. Although cleistogamy has evolved repeatedly, the reason for its stability is not known for any species. We tested the hypothesis that the production of cleistogamous and chasmogamous flowers by a perennial violet constitutes adaptive phenotypic plasticity. We manipulated the season of flowering for each flower type and determined fruit set and the germination percentage of seeds produced by cleistogamous and chasmogamous flowers to test the hypothesis that adaptive plastic response to seasonal environmental variation makes mixed mating stable. Cleistogamous flowers had greater fruit set in all seasons and produced seeds with germination percentages as great as or greater than those from chasmogamous flowers. The consistent advantage of cleistogamous flowers is clearly not consistent with a role of adaptive plastic response to seasonal variation. The biomass cost of seed production by chasmogamous flowers was nearly three times that for cleistogamous flowers. Explaining why chasmogamous flower have not been eliminated by natural selection requires that this difference be balanced by an advantage to chasmogamous flowers that has not yet been identified.     

THE HETEROCHRONIC ORIGIN OF THE CLEISTOGAMOUS FLOWER IN ASTRAGALUS CYMBICARPOS (FABACEAE)

Members of the species Astragalus cymbicarpos form chasmogamous and cleistogamous flowers, as well as a large variety of intermediate floral types. Bivariate allometry and Gould's clock models were used to investigate the possible heterochronic evolution of the cleistogamous flower from the chasmogamous flower. In three of the whorls analyzed (pistil, stamens, and corolla) comparison of chasmogamous, pseudocleistogamous, and cleistogamous flowers revealed a progressive “juvenilization” of the adult form. This paedomorphic morphology proved to be partly the result of a process of progenesis, also evident in acceleration of sexual maturity. The retardation of shape with respect to size in these three whorls suggests, however, the existence of a heterochronic process other than progenesis.     

VARIATION IN THE DEGREE OF CLEISTOGAMY WITHIN AND AMONG SPECIES OF THE GRASS DANTHONIA

North American species of the grass Danthonia bear distinct chasmogamous and cleistogamous flowers. Four taxa occurring in North Carolina (D. compressa, D. epilis, D. sericea, and D. spicata) were examined for variation in the degree of cleistogamy. The flowering culms bear a single terminal panicle consisting of 4 to 12 spikelets of chasmogamous flowers. In each leaf axil, at the nodes of the flowering culm, is a single spikelet of cleistogamous flowers completely surrounded by the leaf sheath. The percentage of cleistogamous flowers produced on any culm depends on the number of chasmogamous and cleistogamous spikelets and the number of flowers in each type of spikelet. All four characters vary among the taxa examined. Danthonia compressa produces, on the average, 50% cleistogamous flowers; D. spicata, 25% cleistogamous flowers; D. sericea and D. epilis, 5% cleistogamous flowers. The degree of cleistogamy in D. spicata is associated with certain habitat features. Populations from mountain sites, disturbed sites, and non-woodland sites produced higher percentages of cleistogamous flowers than did populations from piedmont, undisturbed, and woodland sites, respectively. Grazing may favor increased cleistogamy because cleistogamous flowers are produced lower on the plant. In North Carolina, the most frequently grazed Danthonia taxa also produce the highest percentage of cleistogamous flowers.     

REPRODUCTIVE BEHAVIOR OF AMPHICARPAEA BRACTEATA (LEGUMINOSAE), AN AMPHICARPIC ANNUAL

Amphicarpaea bracteata, an annual legume common in woodland communities in the eastern United States, produces three distinct types of flower: subterranean cleistogamous (SCL), aerial cleistogamous (ACL), and aerial chasmogamous (ACH). We sought to quantitatively describe the growth and reproduction of four diverse A. bracteata populations in an effort to explain the adaptive significance of this species’ variable reproductive modes. Virtually all plants develop 1 to 3 SCL seeds on subterranean cotyledonary shoots, starting in late July. Larger plants produce additional SCL seeds later from the tips of axillary shoots which bury. Seeds produced by SCL flowers are large (39 to 134 mg), have restricted dispersal, lack dormancy, have high germination , and produce relatively vigorous seedlings. ACL flowers develop from early August through plant senescence in early October, while ACH flowers appear in a pulse in late August. The number of each aerial flower type was positively correlated with plant size. The ACL flowers take significantly less time to develop mature fruits than do ACH flowers. Both aerial seeds are smaller than the subterranean (mean weights: ACL 12.1, ACH 8.7 mg), have lower germination (ACL 20.2%, ACH 15.3%), appear relatively resistant to environmental extremes, and have the potential for more widespread dispersal. Plants derived from subterranean seeds are much larger than plants derived from aerial seeds, which makes them more likely to produce axillary SCL and aerial seeds. Only larger plants derived from subterranean seeds and growing in favored sites produce ACH flowers. This imposes an alternation of selfing with outcrossing generations. This pattern of reproductive behavior in A. bracteata is similar to that found in several other amphicarpic species.     

The selection of cleistogamy and heteromorphic diaspores

Models for the evolution of a mixture of cleistogamous (closed, autogamous) flowers and chasmogamous (open) flowers are described. The 'basic' model takes into account features associated with cleistogamous self-pollination, including the greater economy and certainty of cleistogamous fertilization and the inability of cleistogamous flowers to contribute pollen to the outcrossed pollen pool. Complete cleistogamous selfing is favoured when allocation to maternal function, fertilization rate, and viability of progeny are sufficiently greater for the cleistogamous component, and when the resources spent on ancillary structures in cleistogamous flowers, cleistogamous seed costs, and inbreeding depression are low. The result is discussed with respect to the cost of sex argument and relevant ecological data. Suggestions for the apparent rarity of cleistogamy are presented. The 'complex habitat' model extends the basic model to situations in which the success of reproduction by cleistogamy or chasmogamy varies according to the environment of the parent. In this situation, reproduction by both cleistogamy and chasomogamy is sometimes selected. A 'near and far dispersal' model addresses the question of the evolution of dual modes of dispersal, which occur in some cleistogamous and non-cleistogamous plants. A dual mode of dispersal may evolve if a narrowly dispersed seed type is more successful in establishing at the sites located within its dispersal range compared with a second, more widely dispersed seed type which experiences less sib competition. The prediction is discussed with respect to data from amphicarpic plants.