The cleistogamous breeding system: a review of its frequency, evolution, and ecology in angiosperms.
Abstract Introduction Types of Cleistogamy Dimorphic Cleistogamy Complete Cleistogamy Induced Cleistogamy Occurrence of Cleistogamy Description of Survey Survey Results Evolution of Cleistogamy in Angiosperms Phylogenetic Implications Advantages and Disadvantages of CH and CL Flowers Selection for Cleistogamy Variable Environments Inbreeding Depression and Geitonogamy Differential Seed Dispersal Variable Ecological Factors and Plant Size Implications for Future Research Acknowledgments Literature Cited
Cleistogamy, a sexual breeding system defined as the production of permanently closed, self-pollinated flowers, has intrigued botanists for centuries and is now recognized as an important system found in a variety of plant taxa. The term was first used by Kuhn in 1867 to describe bud-like flowers that never opened but yet developed into fruit. He called these cleistogamous flowers (literally, "closed marriage"). Darwin (1877) noted that in a cleistogamous species, these flowers may be the only type produced or they may also appear together on the same plant along with open, typically insect-pollinated flowers (known as chasmogamous or "open marriage" flowers). He described cleistogamy in genera such as Impatiens, Oxalis, and Viola as evidence of natural selection. Cleistogamy was also discussed by Darwin's contemporaries over subsequent decades (e.g., Kerner yon Marilaun, 1902). Since then, many scientists have investigated the ecological, developmental, and evolutionary aspects of cleistogamous (CL) and chasmogamous (CH) flower production in a variety of plant species (e.g., Schemske, 1978; Waller, 1979; Mitchell-Olds & Waller, 1985; Antlfinger, 1986; Schmitt & Ehrhardt, 1987, 1990; McCall et al., 1989; Bennington & McGraw, 1995; Culley, 2002). The production of CH and CL flowers was once thought to be directly analogous to outcrossing and selfing, but CH flowers of some species are now known to occasionally self-pollinate before anthesis via delayed self-pollination (Culley, 2000, 2002) as well as geitonogamy (Stewart, 1994). The number of studies involving species with cleistogamous flowers has risen dramatically in recent years (Fig. 1). Today, cleistogamy is a multifaceted term used to refer to this unique floral type and its subsequent fruits and seeds, and also to the plant species that produce these closed flowers.
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Despite the attention that cleistogamous species have received in the literature, the extent of cleistogamy within angiosperms is still not fully understood. Cleistogamous species and genera have been frequently listed in the literature (Darwin, 1877; Kerner von Marilaun, 1902; Ritzerow, 1908; Rickett, 1932; Uphof, 1938; Camp & Gilly, 1943; Maheshwari, 1962), but the most recent comprehensive reviews of cleistogamy (Connor, 1979; Lord, 1981; Campbell et al., 1983) are well over 20 years old. Furthermore, two of these reviews (Connor, 1979; Campbell et al., 1983) focus strictly on the Poaceae, and a later paper (Plitmann, 1995) focuses on floral dimorphisms in general. There is also some discrepancy in the literature as to what constitutes a cleistogamous species. Confusion may be due to the use of the term "cleistogamy" to refer to species with only CL flowers and to those that produce both CL and CH flower types.
Relative to other breeding systems, the evolution of cleistogamy has received relatively little attention, despite recent advances in molecular techniques that have spurred the development of comprehensive angiosperm phylogenies (e.g., Soltis et al., 2000, 2005; Angiosperm Phylogeny Group, 2003; Hilu et al., 2003). Mapping the cleistogamous trait onto these phylogenies would provide an estimate of the number of times cleistogamy has evolved. The purpose of this review is to (1) clarify the different types of cleistogamy that exist, (2) quantify how often cleistogamy occurs within angiosperm genera and species, (3) estimate the number of times that cleistogamy has evolved within angiosperms, and (4) identify ecological factors that may promote the evolution of cleistogamy in plants.
Types of Cleistogamy
Cleistogamy is a sexual breeding system in which the necessity of floral visitation for fertilization depends upon the type of flower produced. Fertilization within individual cleistogamous flowers occurs without pollinator intervention, either by direct transfer of pollen grains from anther to stigma or through germination of pollen grains in the anther and pollen tube growth into the adjoining style within the bud (Mayers & Lord, 1983b). Hence, cleistogamy differs from asexual systems such as apomixis, in which double fertilization is not required for full seed set. Open chasmogamous flowers may be pollinated by floral visitors or may sometimes self-pollinate through prior or delayed selfing. We consider here three major types of cleistogamy that vary in terms of their developmental pathways (Fig. 2). In all cases, the floral forms are influenced to varying degrees by the environment in which they occur. CL flowers are often favored under poor growth conditions, presumably because they are energetically less costly (Waller, 1979; but see Cheplick, 2005b). The types of cleistogamy described below are adapted in part from Lord (1981) and Campbell et al. (1983), both of whom modified their definitions from Hackel (1906).
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Dimorphic cleistogamy is the same as Lord's (1981) category of true cleistogamy, in which prominent differences in CL and CH floral morphology result from divergent developmental pathways. CL flowers are modified early in development and are characterized by a reduction in corolla size and stamen size and/or stamen number relative to CH flowers. This category is most commonly associated with cleistogamy in general, as exemplified by many Impatiens and Viola species (e.g., Darwin, 1877). On a given plant, both types of flower can appear at the same time but in different positions (spatially separated; Lloyd's  multiple strategy), or they may be produced sequentially during the season (temporally separated; Lloyd's  conditional strategy). Spatial floral separation is evident, for example, in Amphicarpaea bracteata (Trapp & Hendrix, 1988) and Vigna minima (Gopinathan & Babu, 1987), in which aerial CH, aerial CL, and subterranean CL flowers are all produced. In the case of temporal separation, the sequence of CH and CL flower production depends upon the species. In the forest herb Viola pubescens, CH flowers are produced only in the early spring, followed by the appearance of CL flowers a few weeks later, once light levels fall as the forest canopy forms (Culley, 2002). In other species, CL flowers appear before CH flowers, as in Ceratocapnos heterocarpa (Ruiz de Clavijo & Jimenez, 1993), in which CH flower production is eventually triggered by a specific photoperiod and temperature in the spring. Dichanthelium clandestinum also produces CL flowers during spring, with CH flowers subsequently appearing in late summer (T. Bell, pers. comm.). Multiple flower-type sequences can also occur throughout the season, as in Viola canadensis (CH-CL-CH; Culley, 2000) and Centaurea melitensis (CL-CH-CL; Porras & Munoz Alvarez, 1999). Finally, some species are capable of both temporal and spatial separation of floral types. For example, in Impatiens, individual plants can produce CH and CL flowers simultaneously (Waller, 1979; Antlfinger, 1986), but seasonal trends are more often detected in populations with either flower type produced first (e.g., Simpson et al., 1985; Masuda & Yahara, 1994; Lu, 2002). This may reflect populational differences in light availability, with high light or dense shade triggering CH or CL floral production, respectively (Schemske, 1978).
Changes in floral type during the season in dimorphic cleistogamy are due to alterations in the initial production of primordial buds, which then develop into either CH or CL flowers. Individual buds are incapable of converting from one floral form into another once the developmental pathway has been determined. For example, if the light environment of Viola pubescens suddenly declines, all CH buds on individual plants typically abort within a few days, and plants begin producing new CL buds soon thereafter (Culley, 2002). The ability to produce CH and CL flowers has a discrete genetic basis, which is affected by a number of abiotic and biotic factors such as light levels, nutrient availability, pollinator availability, and herbivory. We have renamed this category dimorphic instead of true cleistogamy or facultative cleistogamy to emphasize the dual production of different floral forms and to avoid any confusion with the following category.
Defined as the production of only CL flowers on an individual, complete cleistogamy has been reported in several species, especially in orchids and grasses. For example, the Hawaiian endemic Schiedea trinervis self-pollinates in the bud, which never opens (Wagner et al., 2005). This category has been maintained in previous reviews of cleistogamy (Hackel, 1906; Connor, 1979; Lord, 1981). Most indications of complete cleistogamy are based on observations of only a few individuals, often in artificial environments such as a greenhouse. This is especially true of orchid species, which are often cultivated under highly artificial conditions, with only a few individuals per species. Darwin (1877) was skeptical about reported cases of complete cleistogamy and recommended further study under natural conditions to ensure that no CH flowers are ever produced. Thus, to verify complete cleistogamy within a plant species, investigations must include monitoring the flowering phenology of multiple individuals in the natural environment.
This is the same as Lord's (1981) category of pseudocleistogamy and Uphof's (1938) ecological cleistogamy. In this case, the environment arrests the development of CH flowers prior to anthesis and results in a mechanical failure of the flower to open, resulting in the production of a CL flower (Schoen & Lloyd, 1984). In contrast to dimorphic cleistogamy, there are no morphological differences between CL and CH flowers other than lack of floral expansion and anthesis in CL flowers (Lord, 1981). Shifts from CH to CL flower production occur more quickly during the season in this category than in dimorphic cleistogamy. In addition, there are no fixed developmental trajectories that differ for the two floral types (Fig. 2). In this category, unfavorable conditions such as drought and low temperatures often promote CL flower production (Uphof, 1938). For example, several Festuca species in the Far East Arctic that often generate masses of CH flowers produce CL flowers only under conditions of low temperature and high relative humidity (Connor, 1998). Portulaca species in Hawaii often produce CL flowers under conditions of reduced light and temperature, resulting in a failure of buds to open (Kim & Carr, 1990). We have renamed this category from Lord's (1981) and Uphof's (1938) designations to emphasize the effect of the environment in inducing a change in flower type.
Another reported category of cleistogamy is that of preanthesis cleistogamy, in which self-pollination occurs first in the bud, followed by anthesis and opportunities for outcrossing. For example, self-fertilization of Lacandonia schismatica occurs in flower buds, as pollen grains germinate within the anthers and pollen tubes grow within the receptacle before the flower opens (Marquez-Guzman et al., 1993). CH flowers of the in-breeder Mimulus nasutus are also capable of self-fertilization prior to anthesis (Diaz & Macnair, 1999). Because these flowers do not remain closed, we do not consider them to be an example of cleistogamy, but rather of prior self-pollination in CH flowers (Lloyd & Schoen, 1992). Consequently, examples of this floral morphology will not be considered further in this review.
The three types of cleistogamy presented here occur along a gradient of morphological change influenced by the environment. That is, in response to different environmental conditions, individuals within a species may be able to alter their CH/CL flower production within a short period of time (induced cleistogamy) or gradually in response to seasonal changes (dimorphic cleistogamy), or they may produce only CL flowers regardless of the environment (complete cleistogamy). It would not be unexpected to find cases of cleistogamy that are difficult to partition into these categories, especially as more species are examined in the future.
The type of cleistogamy can also vary among populations in some species, such as the orchid Corallorhiza bentleyi, in which populations produce either CL flowers or varying numbers of both CH and CL flowers (Freudenstein, 1999; J. Freudenstein, pers. comm.). In populations of Vigna minima, individual plants produce only one type of flower or a combination of aerial CH flowers, induced aerial CL flowers, and subterranean CL flowers (Gopinathan & Babu, 1987). In some species, cleistogamy is not the only method of self-pollination. For example, in addition to cleistogamy in Drosophyllum lusitanicum (Droseraceae), selfing can occur simultaneously on an individual plant in CH flowers via prior selfing, delayed selfing, or geitonogamy (Ortega-Olivencia et al., 1998).
In some species, the ratio of CH to CL flowers may also fluctuate among individuals and populations. In a population of Viola pubescens, for example, 74% of sampled individuals produced both types of flowers during a single season, 13% produced only CH flowers, 9% produced only CL flowers, and the remaining 4% were vegetative; all of these individuals had produced both CH and CL flowers the previous year (Culley, 2002). Similarly, individuals of Viola sororia may not always produce both flower types every year (Solbrig, 1981). Percentage cleistogamy (defined as the number of CL buds divided by total bud number) differed substantially among populations of Impatiens pallida (range, 69-100%; Schemske, 1978) and I. biflora (80-98%; Schemske, 1978). In addition, the proportion of flowering plants producing CL flowers varied within populations of Oxalis montana (range, 25-68%; Jasieniuk and Lechowicz, 1987) and Danthonia spicata (0-94%; Clay, 1983b; Cheplick, 2005b).
To fully investigate the occurrence of cleistogamy within a species in future studies, it will be necessary to monitor the flowering phenology and floral production in several populations and individuals within populations over several seasons. Because the categories presented here are based on ecological and genetic factors, they can be very useful in describing the breeding system of any given plant species.
Occurrence of Cleistogamy
In one of the most frequently cited reviews of angiosperms, Lord (1981) reported that cleistogamous flowers were detected in 56 families and 287 species. These initial figures included all types of cleistogamy (including preanthesis cleistogamy). Taxa that exhibit only dimorphic cleistogamy are listed in her Table I, and consist of 29 families, 67 genera, and at least 148 species. In a later review, Plitmann (1995) reported cleistogamy in 112 genera and 202 species, with 81% of the latter possessing dimorphic cleistogamy. To update Lord's (1981) estimate and to include subsequent reviews and papers (e.g., Campbell et al., 1983, for Poaceae), we conducted an extensive literature search with a goal of classifying angiosperm species into the three categories of cleistogamy presented above. In contrast to previous reviews (e.g., Camp & Gilly, 1943; Maheshwari, 1962) that were based on species or genera lists derived from older anecdotal sources (e.g., Rickett, 1932), our approach was to consider only those species as cleistogamous that were well-supported in the literature with floral descriptions or empirical data. Thus, our study is more thorough and conservative than many previous reviews.
DESCRIPTION OF SURVEY
The literature survey was performed using online databases and supplemented with printed journals when appropriate. A number of different online search engines were used to locate publications from 1914 (the earliest that many search engines can currently access) to the present that contained the keywords "cleistogamy," "cleistogamous," or "autogamy." The primary search engines used in this analysis were the following: Academic Search Premier, BioOne, BIOSIS, Blackwell-Synergy, Ingenta Online Journals, Ingenta Select, JSTOR Ecology and Botany Collection, Ohiolink Electronic Journal Center, Oxford Journals Online, ProQuest Research Library, and Wilson OmniFile-Full Text Mega Edition. Articles, including several Ph.D. dissertations, were acquired in electronic or printed formats. A few cases of purported complete cleistogamy were verified by using online search engines and virtual herbaria to locate additional information or floral images of the species in question.
Based on descriptions of floral morphology and/or development in each article, species were placed into one of the three categories of cleistogamy. In some cases, the author's classification of cleistogamy type was revised based upon the criteria presented above. All grass species cited by Campbell et al. (1983) were considered dimorphic unless they were described as having complete cleistogamy. In our review, studies clearly indicated that CL flowers were present in certain species, but these studies lacked sufficient morphological or developmental descriptions of the CH flowers. These species could not be assigned to one of the three categories with confidence and were therefore placed in an "unclear" category of cleistogamy. In a few cases, the literature indicated that certain species produced both CH and CL flowers, but the species could not be further assigned to a dimorphic or induced category, so they were also left as "unclear." The taxonomy of species, genera, and families was also updated to reflect currently accepted nomenclature. Selected investigations were excluded from the analysis if (1) the description of cleistogamy was ambiguous in that it could potentially include prior selfing, (2) cultivated species were genetically modified or bred to produce cleistogamous flowers, (3) taxa consisted of cleistogamous hybrids or mutants, or (4) cleistogamy was reported from only a few individuals of a given species grown in an artificial environment. Thus, this review is a conservative estimate of the total number of cleistogamous species documented in literature.
We found that cleistogamy in general is present in 693 angiosperm species, distributed over 228 genera and 50 families [[TR I]](Table I; species list available from T. Culley upon request). This species estimate is more than twice the number of cleistogamous species reported by Lord (1981). The number of families was lower in our survey than indicated by Lord (1981) because of modern taxonomical rearrangements (Angiosperm Phylogeny Group, 2003; Soltis et al., 2005) and the more conservative nature of our review. This review includes five families (Aizoaceae, Aristolochiaceae, Bromeliaceae Orobanchaceae, and Urticaceae) not previously recognized as containing cleistogamy (Darwin, 1877; Kerner von Marilaun, 1902; Ritzerow, 1908; Rickett, 1932; Uphof, 1938; Camp & Gilly, 1943; Maheshwari, 1962; Lord, 1981). We found that cleistogamy was most often reported within the Poaceae (n=326 species), Violaceae (80), Fabaceae (61), Orchidaceae (24), and Acanthaceae (19). This result differs slightly from Darwin (1877), who noted that cleistogamy was most common in the Fabaceae, Acanthaceae, and the Malpighiaceae. Within genera, cleistogamy was most commonly reported in Viola (Violaceae; 80 species), Stipa (Poaceae; 41), Dichanthelium (Poaceae; 19), Danthonia (Poaceae; 17), Schizachyrium (Poaceae; 17), Acleisanthes (Nyctaginaceae; 16), Vulpia (Poaceae; 15), Briza (Poaceae; 14), Plantago (Plantaginaceae; 13), and Lespedeza (Fabaceae; 13). In most cases, the type of cleistogamy reported was dimorphic (536 of 693 species, or 77.3%), similar to Plitmann's (1995) estimate of 81.7% (165 of 202 species). Complete cleistogamy (72 species, 10.4%) and induced cleistogamy (61 species, 8.8%) were scattered throughout various genera and families (Table I). Only 24 species (3.5%) that produced cleistogamous flowers could not be assigned further to a specific category type because of lack of reported information. These counts are undoubtedly underestimates and are biased toward species and genera that have been more widely studied (e.g., those in Violaceae or Poaceae).
Evolution of Cleistogamy in Angiosperms
The widespread distribution of cleistogamy within angiosperms suggests that this breeding system may have evolved repeatedly over time. Selective factors favoring its evolution may differ, given its occurrence in various plant families and habitats. Both the number of times that cleistogamy has evolved as well as the theory and potential selective pressures behind such events are reviewed below.
Recent advances in molecular genetics and taxonomy make it possible to estimate the number of times cleistogamy has evolved within the angiosperms by mapping the trait onto phylogenetic trees. We did this for three comprehensive, family-based angiosperm phylogenies derived from 18S rDNA, rbcL and atpB sequences (Soltis et al., 2000), matK sequences (Hilu et al., 2003), and a supertree generated from 27 source trees from published and unpublished studies (Soltis et al., 2005). Of the 50 cleistogamous families identified in our review, 44 were listed in the Soltis et al. (2000) phylogeny and 36 in the Hilu et al. (2003) phylogeny, while all 50 were found in the Soltis et al. (2005) phylogeny. Cleistogamy was widespread across monocot and dicot families, having evolved multiple times (Fig. 3). Analysis on a family level across the angiosperms suggested that the breeding system evolved approximately 34 to 41 times (Table II). Cleistogamy evolved at least six to eight times within monocots, but was much more common in dicots, where it evolved at least 24 to 31 different times (Table II).
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These values are most likely underestimates because cleistogamy may also have evolved repeatedly within certain families and genera. For example, complete cleistogamy has evolved three separate times within Schiedea (Caryophyllaceae), a Hawaiian endemic genus containing diverse breeding systems (Wagner et al., 2005). In the primarily chasmogamous genus Acleisanthes (Nyctaginaceae), the joint production of CL and CH flowers has evolved at least twice (Levin, 2000, 2002). Alternatively, the ability to produce cleistogamous flowers can be lost over time, as is evident in Viola (Ballard et al., 1999), where species that produce only CH flowers, (e.g. V. pedata, V. maviensis, V. helenae) are embedded within clades containing species with both flower types (Fig. 4). Interestingly, most of the seven Hawaiian Viola species appear to possess only CH flowers (Wagner et al., 1990), with one exception, V. kauensis (Ballard et al., 1999). The most parsimonious explanation is that the ancestral colonist to Hawaii may have been completely chasmogamous, with dimorphic cleistogamy subsequently evolving in situ. Alternatively, dimorphic cleistogamy could have been the ancestral condition, with the toss of CL flowers occurring shortly after radiation to the different islands. Within Viola, species lacking CL flowers often inhabit relatively stable environments, such as the shaded understory of tropical mesic forests (V. chamissoniana), or the high-light environments of open bogs (V. maviensis) or savannah (V. pedata, V. pedunculata), where insect pollinators are common. The relationship between loss of CL flowers and stable abiotic environments and/or pollinator activity is an area of promising research for future phylogenetic or ecological investigations.
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ADVANTAGES AND DISADVANTAGES OF CH AND CL FLOWERS
In order for cleistogamy to evolve, CL flowers must exhibit fitness advantages distinct from those of CH flowers. A variety of these fitness advantages have already been identified. First, CL flowers may offer reproductive assurance when pollinators are rare or absent (Mitchell-Olds & Waller, 1985; but see Cheplick, 2005b). Rather than acting solely as a fail-safe mechanism for back-up reproduction, CL flowers of some species may actually increase seed production in the event that CH flowers are left unpollinated (Redbo-Torstensson & Berg, 1995; Berg & Redbo-Torstensson, 1998). Second, CL flowers in some species may be energetically less costly to produce, resulting in more resources available for seed production (Waller, 1984) or for larger CL seeds with higher fitness. Third, CL flowers possess an inherent automatic selfing advantage because both maternal sets of genes can be passed on to the progeny (Mitchell-Olds & Waller, 1985), in contrast to only one set of genes passed on to outcrossed offspring. Fourth, CL selfing prevents disruption of locally adapted gene complexes by avoiding the recombination that frequently accompanies outcrossing (Waller, 1984). In addition, CL seeds do not disperse very far in some species, further preserving locally adapted complexes but also potentially leading to sibling competition (Schmitt et al., 1985). Fifth, consistent selfing through CL flowers can eliminate deleterious recessive alleles within populations (Clay & Antonovics, 1985); over time, this could lead to a decrease in the level of inbreeding depression, especially in those species with complete CL. Disadvantages to CL reproduction include decreased genetic variation and increased genetic drift, high levels of inbreeding depression (if caused by expression of several deleterious alleles of small effect that cannot be purged), and increased sibling competition among CL seeds that are dispersed within the immediate vicinity of the maternal plant.
In order for CH flowers to be maintained in species with dimorphic cleistogamy, they must offer a selective advantage different from that of CL flowers. First, CH seeds may exhibit heterosis (Mitchell-Olds & Waller, 1985; Schmitt & Gamble, 1990) if they result from outcrossing events between genetically distinct individuals. Second, genetically variable progeny produced by CH flowers (Antlfinger, 1986) would be favored in spatially or temporally heterogeneous habitats (Mitchell-Olds & Waller, 1985; Holsinger, 1986). Finally, CH seeds are often dispersed farther from the maternal plant, thus avoiding sibling competition (Schmitt et al., 1985). Disadvantages to CH flower production include high energetic cost of production in some species as well as pollinator reliance for fertilization.
SELECTION FOR CLEISTOGAMY
The evolutionary pathway to cleistogamy remains relatively understudied compared with more widely investigated breeding systems such as dioecy (e.g., Charlesworth & Charlesworth, 1978). A number of different ideas, however, have been proposed to account for the production of one or both flower types within populations, and these theories consolidate several of the ideas presented above (see also Oakley et al., in prep).
Two related sets of models (Lloyd, 1984; Schoen & Lloyd, 1984) demonstrate that dimorphic cleistogamy can be selected for in two types of heterogeneous environments based on the relative fitness and cost of CH and CL flowers. First, environments can vary simultaneously within a given plant (the fine-grained environment of Lloyd, 1984 and Schoen & Lloyd, 1984), as when flowers at different spatial positions experience varying numbers of pollinator visits or levels of herbivory. In this case, a phenotype that produces both CH and CL flowers at a single time would exhibit the highest fitness if each flower type is produced in the environment for which it is best suited. More often, however, environments vary across an area or season (a coarse-grained environment; Lloyd, 1984; Schoen & Lloyd, 1984), and the fitness of a phenotype would be optimized by the production of a different flower type within each environment to maximize reproductive success.
Flowering phenology in several angiosperm species is consistent with these models. In Impatiens, CH flowers are typically produced in areas of high light intensity, as along edges of populations (Schemske 1984), while CL flowers are produced in more shaded areas (Schemske 1978). CL seed production in Impatiens is also higher in more stressful (Bennington and McGraw, 1995) or unpredictable environments (Waller, 1979) because CL flowers may be less costly, even though their fitness may still be considerably less than that of CH flowers. Fitness may also increase for CH flowers produced when pollinators are most active, while less costly CL flowers only appear when pollinators are less frequent and as CH flowers decline in fertility. Thus, the ability of plants to assess and respond appropriately in a heterogeneous environment can lead to selection for a phenotype that produces both flower types, either sequentially or simultaneously, depending upon the nature of the environment (Lloyd, 1984). If a plant cannot properly assess the environment, the least costly flower type would be favored (i.e., complete cleistogamy in most species) as long as the fitness benefits outweigh the cost, assuming no inbreeding depression (see below). These environmental effects were also invoked by Darwin (1877), who suggested that dimorphic and complete cleistogamy may have evolved from induced cleistogamy as environmental conditions became more predictable and plants were able to track environmental changes.
Inbreeding Depression and Geitonogamy
The role of inbreeding depression has been invoked in several evolutionary models. Masuda et al. (2001) expanded on Schoen and Lloyd's (1984) multiple strategy model by incorporating inbreeding depression and CH geitonogamy. Their results reinforce the importance of CH fertility in CL flower production; they showed that both flower types will be favored when some geitonogamy occurs in CH flowers and inbreeding depression is severe. Similarly, Stewart (1994) suggested that increased allocation to CH reproduction may increase geitonogamy, resulting in diminished fitness gains because cross-fertilization is less likely. This could constrain selection for greater CH reproduction, while inbreeding depression would constrain selection for greater CL reproduction. Consequently, the dual production of CH and CL flowers may be an evolutionarily stable strategy even if the level of inbreeding depression is substantial, as long as there is a positive correlation between geitonogamy and CH flower production. The level of inbreeding depression, however, has generally been low in dimorphic cleistogamous plant species, ranging from 0-0.10 (Wilken, 1982; Culley, 2000; Lu, 2002; Eckstein and Otte 2005). Inbreeding depression may be reduced in these populations because of a past history of CL selfing and purging of deleterious alleles. Even if CH progeny exhibit a high overall level of inbreeding, CH flowers may still be favored because they serve to maintain gene flow and thus significantly reduce gene fixation in populations (Knight and Waller, 1987).
Differential Seed Dispersal
CH and CL seeds of many angiosperms, especially grasses, exhibit heteromorphism with discrete seed types often produced concurrently on individual plants (e.g., Cheplick & Clay, 1989; Cheplick, 1996). These seeds may be differentially dispersed, with CL seeds distributed around the natal site and CH seeds dispersed further away (Schmitt et al., 1985). Such differential seed dispersal may explain in part the maintenance of dimorphic cleistogamy. According to Holsinger (1986), intermediate selfing rates will be stable if less-fit selfed progeny are less successful migrants than outcrossed progeny, especially in areas with spatial environmental heterogeneity (Schmitt et al., 1985) in which local adaptation occurs. Although CH progeny are not always outcrossed, these ideas can be expanded to explain the maintenance of dimorphic cleistogamy in cases where CH progeny are primarily outcrossed.
In such species, dimorphic or induced cleistogamy will be maintained within populations if the dispersal of selfed CL seeds locally and outcrossed CH seeds more distantly results in higher fitness gains for both seed types. CL seeds would have highest fitness in the maternal environment, since both sets of chromosomes come from the maternal plant, which may already be adapted to its local environment. In contrast, recombination and the possible appearance of new alleles in outcrossed CH progeny would disrupt locally adapted gene complexes, resulting in depressed CH fitness within the maternal environment. Hence, different allelic combinations in CH seeds may favor adaptation to a wider array of heterogeneous habitats, as well as reduced sibling competition. In one of the few investigations of differential seed dispersal, CL progeny of Impatiens capensis exhibited higher fitness within the maternal location than they did 12 m away, but, paradoxically, CH flowers also had higher fitness at the maternal site as well (Schmitt & Gamble, 1990). Considered within a metapopulational context, differential dispersal of CH seeds may also serve to increase the distribution of a species, while CL seeds serve to ensure populational survival within a given site (Koller & Roth, 1964).
Variable Ecological Factors and Plant Size
Cheplick (2005b) suggested that variation in the expression of cleistogamy in some species may reflect the influence of environmental factors such as density, soil moisture and nutrition, light levels, and plant size. In a review of several grass species, he found that the CH/CL ratio declined with increasing density in Amphicarpum purshii because plant size was reduced by intraspecific competition. In Microstegium vimineum, the CH/CL ratio was lowest in greenhouse plants exposed to a sunny environment but was highest in small plants from the shady interior. In contrast, the CH/CL ratio of Dichanthelium clandestinum was not affected by light levels (Cheplick, 2005b), although an earlier study found significant effects among different populations (Bell & Quinn, 1987). Relative amounts of CH and CL flowering is also known to vary in other angiosperm species in relation to day length and temperature (Evans, 1956; Mayers & Lord, 1983a) or to light and nutrient availability (Le Corff, 1993).
Plant size also affects reproductive output of certain species exhibiting dimorphic cleistogamy. In some taxa, individual plants must attain a certain size before reproduction of any type can occur, as in Impatiens capensis (Waller, 1979). In general, plant size affects either CH reproduction or a combination of CH and CL reproduction. For example, greater plant size was associated with an increase in percentage chasmogamy in Mimulus nasutus (Diaz & Macnair, 1999), and only larger plants produced CH flowers in Viola sororia (Solbrig, 1981) and Danthonia spicata (Clay, 1982). In the grass Amphicarpaea bracteata, light intensity influenced plant size, which was associated with increased aerial CH flower production (Trapp & Hendrix, 1988). Greater plant size was related to both CH and CL flower production in Oxalis montana, but size explained a significantly greater proportion of variation in CL flower number (Jasieniuk & Lechowicz, 1987). CH and CL flower production also increased substantially with plant weight and density in Collomia grandiflora (Wilken, 1982). Although plant size is generally less likely to directly affect CL reproduction, more cleistogamous plant species need to be examined in future studies.
Implications for Future Research
Continued research on cleistogamous plant species will offer further insight into the evolutionary history and prevalence of this breeding system in angiosperms. Cleistogamy will undoubtedly be discovered in additional species as the reproductive biology of more species is examined in the future. New discoveries of cleistogamy are especially likely in families related to those in which cleistogamy has already been documented (Table I), as in the Surianaceae which is sister to the Polygalaceae and Fabaceae (Soltis et al., 2000). As more cleistogamous species are identified, they can be used to test evolutionary theories and origins of cleistogamous taxa, especially as phylogeny resolutions increase with greater taxonomic sampling. Empirical data are also needed to test evolutionary theories previously developed (Lloyd, 1984; Schoen & Lloyd, 1984; Masuda et al., 2001). This information will be invaluable for understanding the selective pressures and factors favoring the evolution of cleistogamy as well as the evolutionary loss of this breeding system, a subject that has received little attention to date.
Although the expression of cleistogamy is affected by the environment in many species, for most species, the necessary reproductive and ecological information is often not reported. For example, variation of floral types within and between individuals and populations needs to be quantified. In many species, there is little indication of the degree to which the expression of cleistogamy is a phenotypic trait influenced by the environment (but see Cheplick, 2005b), or how it is affected by the interaction of genetic and environmental factors. Investigations would also greatly benefit from the application of developmental and genetic techniques to identify the genes responsible for the production of CH and CL flowers in different species.
We encourage future investigators to classify the cleistogamous breeding system using the three primary categories as outlined in this paper to facilitate future comparisons among taxa. In particular, reports of cleistogamy in the literature need to include a detailed description of the reproductive ecology and developmental biology of the various floral types, preferably in multiple populations and over several seasons. Ultimately, by further investigating the role of the environment and its influence on floral gene expression, we may come to better understand the factors directly influencing the transition from CH to CL flower production and the evolution of cleistogamy in angiosperms.
We thank Timothy Bell, who kindly shared his original notes from his cleistogamy survey of the grasses, and Harvey Ballard and his group at Ohio University for their suggestions. Anne Wick and MaryAnn Paul assisted in portions of the JSTOR literature review for Figure 1, and the librarians at the Chemistry-Biology library at the University of Cincinnati and the Lloyd Library in Cincinnati were indispensable in locating certain references. Harvey Ballard kindly supplied the information for Figure 4. Valuable comments on the manuscript and data set were provided by Timothy Bell and Gregory Cheplick. This study was made possible through funding from the University Research Council at the University of Cincinnati.
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THERESA M. CULLEY AND MATTHEW R. KLOOSTER
Department of Biological Sciences
University of Cincinnati
614 Rieveschl Hall
Cincinnati 45221-0006, U.S.A.
Table I List of cleistogamous families and genera in angiosperms. Shown are the number of species within each genera classified as exhibiting complete, induced, dimorphic, or unclear cleistogamy. Additional references for some species can be found in Lord (1981) Com- In- Dimor- Un- Family Genus plete duced phic clear ... Acanthaceae Aechmanthera ... 1 ... ... Blechum ... 1 ... ... Dianthera ... 1 ... ... Dicliptera ... 1 ... ... Dipteracanthus ... ... 1 ... Eranthemum ... 2 1 ... Ruellia ... ... 9 ... Schaueria ... ... 1 ... Stenandrium ... 1 ... ... Aizoaceae Sarcozona ... ... ... 1 Alismatacea Luronium ... 1 ... ... Aristolochiaceae Aristolochia ... ... 1 ... Asteraceae Ainshaea ... ... 2 ... Catanche ... ... 1 ... Centaurea ... ... 1 ... Gymtarrhena ... ... 1 ... Balsaminaceae Impatiens ... ... 4 ... Boraginaceae Cryptantha ... ... 3 ... Lithospermum ... ... 6 ... Brassicaceae Cardamine ... ... 1 ... Draba ... ... 1 ... Geococcus ... ... 1 ... Subularia ... 1 ... ... Thlaspi ... 1 ... ... Bromeliaceae Tillandsia ... ... 2 ... Campanulaceae Campanula ... ... 1 ... Githopsis ... ... 1 ... Howellia ... ... 1 ... Triodanis ... ... 1 1 Caryophyllaceae Illecebrum ... 1 ... ... Polycarpon ... ... 1 ... Schiedea 3 ... ... ... Stellaria ... 1 ... ... Cistaceae Halimium ... ... 1 ... Helianthemum ... ... 1 ... Lechea 1 ... ... ... Tuberaria 1 ... ... ... Commelinaceae Commelina ... ... 4 ... Commelinantia ... ... 1 ... Murdannia ... 1 ... ... Plowmanianthus 2 ... 2 ... Tradescantia ... ... 1 ... Droseraceae Drosera ... ... 1 ... Drosophyllum ... ... ... 1 Elatinaceac Elatine 1 3 ... ... Ericaceac Vaccinium ... ... 1 ... Fabaceae Amphicarpaea ... ... 3 ... Astragalus ... ... 1 ... Clitoria ... ... 2 ... Galactica ... ... 1 ... Glycine ... ... 4 1 Lathyrus ... ... 3 ... Lespedeza ... ... 13 ... Lotononis ... 12 ... ... Macroptilium ... 1 ... ... Medicago ... ... 6 ... Ononis ... ... 3 ... Phaseolus ... ... 3 ... Pisum ... ... 1 ... Rhynchosia ... ... 1 ... Tephrosia ... ... 2 ... Trifolium ... ... 1 ... Vicia ... ... 1 ... Vigna ... ... 1 ... Voandzeia ... ... 1 ... Gentianaceae Sebaea ... ... 1 ... Gesneriaceae Streptocarpus ... ... 1 ... Hydrocharitaceae Blyxa ... 2 ... ... Ottelia ... 1 1 ... Juncaceae Juncus ... ... 1 ... Lamiaceae Ajuga ... ... 1 ... Lamium ... 1 1 1 Salvia 1 ... 1 ... Scutellaria ... ... 1 ... Lentibulariaceae Utricularia 1 ... 4 ... Liliaceae Narthecium ... 1 ... ... Lythraceae Ammannia 1 ... ... ... Lythrum ... 1 ... ... Malpighiaceae Aspicarpa ... ... 3 ... Camarea ... ... 1 ... Gaudichaudia ... ... 1 ... Janusia ... ... 1 ... Malvaceae Gossypium ... ... 4 ... Malva ... ... ... 1 Marantaceae Calathea ... ... 1 ... Mayacaceae Mayaca ... 1 ... ... Nyctaginaceae Acleisanthes ... ... 16 ... Mirabilis ... ... 1 ... Nymphaeaceae Ear Vale ... ... 1 ... Orchidaceae Appendicula ... ... ... 1 Bletia ... 1 ... ... Bulbophyllum 1 ... ... 2 Calanthe 1 ... ... ... Caularthron ... ... ... 1 Cheirostylis ... ... ... 1 Chloraea ... ... ... 1 Corallorhiza 2 ... ... ... Dendrobium 3 ... 2 ... Liparis ... 2 ... ... Oberonia ... ... ... 1 Plocoglottis 1 ... ... ... Polystchya ... 1 ... ... Spiranthes 1 ... ... ... Thelasis ... ... ... 1 Thelymitra 1 ... ... ... Orobanchaceae Epifagus ... ... 1 ... Oxalidaceae Oxalis ... ... 6 ... Papaveraceac Papaver ... 3 ... ... Ceratocapnos ... ... 1 ... Corydalis ... ... 1 ... Plantaginaceae Plantago 11 ... 1 1 Poaceae Achnatherum ... ... 1 ... Aciachne 1 ... ... ... Aciachne 1 ... ... ... Agrostis ... ... 1 ... Amphibromus 1 ... 2 ... Amphicarpum ... ... 2 ... Andropogon ... ... 10 ... Aristida ... ... 4 ... Astrebla ... ... 2 ... Austrodanthonia ... ... 1 ... Avena ... ... 4 ... Bothriochloa ... ... 6 ... Bouteloua 2 ... 1 ... Brachyachne 1 ... 1 ... Briza 3 ... 11 ... Bromus ... ... 8 ... Calamagrostis ... ... 2 ... Calyptochloa ... ... 1 ... Catapodium ... ... 1 ... Chasmanthium ... ... 1 ... Chloris ... ... 1 ... Cleistochloa ... ... 2 ... Cleistogenes ... ... 3 ... Cottea ... ... 1 ... Dactyloctenium ... ... 1 ... Danthonia ... ... 17 ... Deschampsia 7 ... 1 ... Desmazeria ... ... 1 ... Dichanthelium ... ... 19 ... Dichanthium ... ... 1 ... Dichelachne ... ... 1 ... Digitaria ... ... 5 ... Dimorphochloa ... ... 1 ... Diplachne ... ... 3 ... Echinochloa ... ... 1 ... Ectrosia ... ... 4 ... Ehrharta ... ... 1 ... Eleusine ... ... 1 ... Enneapogon ... ... 4 ... Enteropogon 1 ... ... ... Eragrostis 2 ... 4 ... Eremitis ... ... 4 ... Eriachne ... ... 3 ... Erianthus ... ... 1 ... Erioneuron ... ... ... 1 Festuca ... 4 2 1 Garnotia 1 ... ... ... Gimnachne 1 ... ... ... Gymnopogon ... ... 2 ... Habrochloa 1 ... ... ... Helichtotrichon ... ... 1 ... Heterachne ... ... 3 ... Hordeum ... ... 4 ... Hypseochloa ... ... 1 ... Leersia ... ... 2 ... Leptochlou 1 ... 1 ... Melica ... ... 3 ... Microlaena ... ... 1 ... Microstegium ... ... 1 ... Muhlenbergia ... ... 1 ... Nassella 3 ... 2 ... Oryza ... ... 1 ... Panicum ... ... 2 ... Pappophorum ... ... 3 ... Paspalum ... ... 1 ... Pennisetum ... ... 3 ... Pheidochloa ... ... 1 ... Piptatherum ... ... 1 ... Piptochaetium 2 ... 7 ... Poa 1 ... 2 ... Puccinellia ... ... 1 ... Relchela ... ... 1 ... Rottboellia ... ... 2 ... Rytidosperma ... ... 1 ... Schizachyrium ... ... 17 ... Secale ... ... 1 ... Setaria ... ... 1 ... Sorghum ... ... 2 1 Spathia ... ... 1 ... Sporobolus 1 ... 10 ... Stipa 2 ... 39 ... Tetrapogon 1 ... ... ... Thyridolepis 1 ... 2 ... Tridens 2 ... 1 ... Triodia ... ... 1 ... Triplasis ... ... 2 ... Trisetum 1 ... 1 ... Vulpia ... ... 15 ... Podostemaceae Griffithella 1 ... ... ... Polemoniaceae Collomia ... ... 1 ... Polygalaceae Polygala ... ... 2 ... Polygonaceae Emex ... ... 1 ... Polygonum ... 3 1 ... Pontederiaceae Heteranthera ... 1 2 ... Monochoria ... ... 1 ... Portulacaceae Portulaca ... 2 ... ... Ranunculaceae Ranunculus 1 3 ... ... Rosaceae Aremonia ... ... 1 ... Rubiaceae Houstonia ... ... 2 ... Relbunium 1 ... ... ... Scrophulariaceae Antirrhinum ... ... ... 4 Glossostigma ... ... 1 ... Limosella ... 1 ... ... Linaria ... 1 ... ... Mimulus ... ... ... ... Neogaerrhinum ... ... 1 ... Nuttallanthus ... ... 1 ... Sairocarpus ... ... 2 ... Scrophularia ... ... 1 ... Triphysaria 1 ... ... ... Vandellia ... ... 2 ... Solanaceae Nicotiana ... ... ... 1 Salpiglossis ... ... 1 ... Solanum ... ... 1 ... Urticaceae Fleurya ... ... 1 ... Violaceae Hybanthus ... ... 1 ... Viola ... 2 78 ... ... ... Total 72 61 536 24 Family References Acanthaceae Maheshwari,1962 Uphof, 1938 Maheshwari, 1962 Uphof, 1938 Uphof, 1938 Darwin, 1877; Uphof, 1938 Lord, 1981; Sigrist & Sazima, 2002 Lord, 1981 Uphof, 1938 Aizoaceae Keighery, 1988 Alismatacea Kerner von Marilaun, 1902 Aristolochiaceae Pfeifer, 1966 Asteraceae Watanabe et al., 1992 Kaul et al., 2000 Porras & Munoz Alvarez, 1999 Lord, 1981 Balsaminaceae Lord, 1981; Masuda & Yahara, 1994 Boraginaceae Calvino & Galetto, 2003; Grau..., 1981 Lord, 1981; Gleason & Cronquist, 1991 Brassicaceae Lord, 1981 Cruden, 1977 Kaul et al., 2000 Kerner von Marilaun, 1902 Uphof, 1938; Maheshwari, 1962 Bromeliaceae Gardner, 1982; Gilmartin & Brown, 1985 Campanulaceae Kerner von Marilaun, 1902 Morin, 1983 Lesica et al., 1988 Lord, 1981; Ritzerow, 1908; Trent, 1939; Maheshwari, 1962 Caryophyllaceae Kerner von Marilaun, 1902 Maheshwari, 1962 Wagner et al., 2005 Maheshwari, 1962 Cistaceae Lord, 1981 Lord, 1981 Nandi, 1998 Herrera, 1992: Nandi, 1998 Commelinaceae Lord, 1981 Maheshwari, 1962 Lord, 1981 Hardy & Faden, 2004 Maheshwari, 1962 Droseraceae Darwin, 1877 Ortega-Olivencia et :d., 1998 Elatinaceac Maheshwari, 1962: Keighery, 1984 Ericaceac Vander Kloet, 1993 Fabaceae Lord, 1981; Trapp & Hendrix, 1988; Trapp, 1988 Gallardo et al., 1993 Gomez & Kalamani, 2003 Kaul et al., 2000 Lord, 1981: Schoen & Brown, 1991; Takahashi et al., 2001: Moyle et al., 2004 Lord, 1981: Kaul et al., 2000 Lord, 1981; Cole & Biesboer, 1992 Van Wyk, 1990 Drewes & Hoc, 2000 Novosyelova, 1998 Lord, 1981 Lord & Kohorn, 1986: Delgado-Salinas, 2000: Kaul et al., 2000 Kaul et al., 2000 Lord, 1981 Lord, 1981; Kaul et al., 2000 Kaul et al., 2000 Lord, 1981 Gopinathan & Babu, 1987; Kaul et al., 2000 Lord, 1981 Gentianaceae Lord, 1981 Gesneriaceae Lord, 1981 Hydrocharitaceae Jiang & Kadono, 2001 Lord, 1981; Jiang & Kadono, 2001 Juncaceae Lord, 1981 Lamiaceae Ruiz de Clavijo, 1997 Lord, 1981; Trent, 1939; Maheshwari, 1962 Kerner von Marilaun, 1902; Uphof, 1938; Plitmann, 1995 Sun, 1999 Lentibulariaceae Lord, 1981; Gleason & Cronquist, 1991; Khosla et al., 1998; Yamamoto & Kadono, 1990 Liliaceae Jacquemart & Desloover, 1992 Lythraceae Maheshwari, 1962 Kerner von Marilaun, 1902 Malpighiaceae Lord, 1981 Lord, 1981 Lord, 1981 Lord, 1981 Malvaceae Lord, 1981 Trent, 1939 Marantaceae Le Corff, 1993 Mayacaceae Uphof, 1938; Maheshwari, 1962 Nyctaginaceae Lord, 1981; Levin, 2000; Levin, 2002 Lord, 1981 Nymphaeaceae Kadono & Schneider, 1987 Orchidaceae Uphof, 1938; Maheshwari, 1962; Catling, 1990 Catling, 1990 Uphof, 1938; Maheshwari, 1962 Maheshwari, 1962 Pupulin, 1998 Jones, 1997 Uphof, 1938; Maheshwari, 1962 Catling, 1990; Freudenstein, 1994, 1999 Uphof, 1938; Maheshwari, 1962; Catling, 1990 Uphof, 1938: Catling, 1990 Uphof, 1938; Catling, 1990 Maheshwari, 1962 Catling, 1990 Catling, 1990 Uphof, 1938; Maheshwari, 1962 Catling, 1990 Orobanchaceae Howes, 1999 Oxalidaceae Darwin, 1877; Lord, 1981; Jasieniuk & Lechowicz, 1987; Berg, 2003 Papaveraceac Uphof, 1938 Ruiz de Clavijo & Jimenez, 1993 Endress, 1999 Plantaginaceae Primack, 1978; Lord, 1981 Poaceae Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983; Connor, 1979 Campbell et al., 1983; Connor, 1979 Crozier & Thomas, 1993; Campbell et al., 1983; Cheplick & Clay, 1989 Lord, 1981; Cheplick 2005b Campbell, 1982: Campbell et al., 1983 Lord, 1981; Campbell et al., 1983 Campbell et al., 1983 Lord, 1981 Uphof, 1938; Lord, 1981; Campbell et al., 1983 Lord, 1981; Campbell et al., 1983 Campbell et al., 1983; Columbus, 1998 Campbell et al., 1983 Campbell et al., 1983 Lord, 1981; Campbell et al., 1983; Bartlett et al., 2002 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Lord, 1981; Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Lord, 1981; Campbell et al., 1983; Clay, 1983a; Cheplick & Clay, 1989; Cheplick, 2005b Campbell et al., 1983; Holderegger et al., 2003 Campbell et al., 1983 Lord, 1981; Campbell et al., 1983; Bell & Quinn, 1985; Cheplick, 2005b Campbell et al., 1983 Campbell et al., 1983; Edgar & Connor, 1982 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Lord, 1981 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983; Judziewicz & Peterson, 1990 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983; Connor, 1998 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Lord, 1981: Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Lord, 1981 Ehrenfeld, 1999: Cheplick, 2005a, 2005b Campbell et al., 1983 Lord, 1981: Campbell et al., 1983 Kerner von Marilaun, 1902 Campbell et al., 1983 Campbell ct al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Uphof, 1938: Maheshwari, 1962: Campbell et al., 1983 Campbell et al- 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983; Lazarides et al., 1991 Campbell et al., 1983 Lord, 1981: Campbell et al., 1983: Gleason & Cronquist, 1991 Campbell et al., 1983: Jacobs et al., 1989 Uphof, 1938: Campbell et al., 1983 Campbell et al., 1983 Campbell et al., 1983 Lord, 1981 Lord, 1981: Campbell et al., 1983; Cheplick, 1996 Campbell et al., 1983 Lord, 1981; Campbell et al., 1983 Podostemaceae Khosla et al., 2001 Polemoniaceae Lord, 1981 Polygalaceae Lord, 1981 Polygonaceae Kaul et al., 2000 Kerner von Marilaun, 1902; Lord, 1981 Pontederiaceae Wylie, 1917; Uphof, 1938; Lord, 1981 Lord, 1981 Portulacaceae Kim & Carr, 1990 Ranunculaceae Uphof, 1938; Maheshwari, 1962; Deyuan, 1990 Rosaceae Kerner von Marilaun, 1902 Rubiaceae Lord, 1981 Freitas et al., 1995 Scrophulariaceae Oyama & Baum, 2004 Beardsley & Olmstead, 2002 Kerner von Marilaun, 1902 Maheshwari, 1962 Trent, 1939 Lord, 1981 Lord, 1981 Lord, 1981 Kaul et al., 2000 Jamison & Yoder, 2001 Lord, 1981 Solanaceae Trent, 1939 Lord, 1981 Lord, 1981 Urticaceae Kaul et al., 2000 Violaceae Lord, 1981 Darwin, 1877: Kerner von Marilaun, 1902: Nieuwland, 1914, 1916; Uphof, 1938; Maheshwari, 1962; Beattie, 1969: Munz, 1974: Culver & Beattie, 1978; Lord, 1981: Wagner et al., 1990; Kim et al., 1991: Masuda & Yahara, 1992; Ballard & Wujek, 1994; Ballard, 1994; Sakai & Sakai, 1996: Gil-Ad, 1997; Elisafenko, 1998; Cutley, 2000: Kaul et al., 2000: Dinc & Yildirimli, 2002: Berg, 2003: Dinc et al., 2003: Marcussen, 2003: Cortes-Palomec, 2004: Oakley, 2004; Eckstein and Otte, 2005 Total Table II Estimate of the number of times cleistogamy has evolved within the angiosperms, based on three phylogenies generated by Soltis et al. (2000), Hilu et al. (2003), and Soltis et al. (2005). Shown are the total number of angiosperm families within each phylogeny that was identified in the Current review as containing cleistogamy Soltis et al. Hilu et al. Soltis et al. (2000) (2003) (2005) Number of families 44 36 50 Eumagnolids 2 2 2 Monocots 8 6 8 Dicots 24 26 31 Total 34 34 41
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|Author:||Culley, Theresa M.; Klooster, Matthew R.|
|Publication:||The Botanical Review|
|Date:||Jan 1, 2007|
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