Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-10T10:18:51.998Z Has data issue: false hasContentIssue false
  • English
  • Français

A classification system for seed (diaspore) monomorphism and heteromorphism in angiosperms

Published online by Cambridge University Press:  22 February 2024

Jerry M. Baskin  and
Carol C. Baskin Open the ORCID record for Carol C. Baskin [Opens in a new window]
Jerry M. Baskin
Affiliation:
Department of Biology, University of Kentucky, Lexington, KY40506, USA
Carol C. Baskin*
Affiliation:
Department of Biology, University of Kentucky, Lexington, KY40506, USA Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY 40546, USA
*
Corresponding author: Carol C. Baskin; Email: Carol.Baskin@uky.edu
Rights & Permissions [Opens in a new window]

Abstract

‘Seed heteromorphism’ is a broadly- and loosely-defined term used to describe differences in size/mass, morphology, position on mother plants and ecological function (e.g. dispersal, dormancy/germination) of two or more seeds or other diaspores produced by an individual plant. The primary aim of this review paper was to characterize via an in-depth classification scheme the physical structural design (‘architecture’) of diaspore monomorphism and diaspore heteromorphism in angiosperms. The diaspore classification schemes of Mandák and Barker were expanded/modified, and in doing so some of the terminology that Zohary, Ellner and Shmida, and van der Pijl used for describing diaspore dispersal were incorporated into our system. Based on their (relative) size, morphology and position on the mother plant, diaspores of angiosperms were divided into two divisions and each of these into several successively lower hierarchical layers. Thus, our classification scheme, an earlier version of which was published in the second edition of ‘Seeds’ by Baskin and Baskin, includes not only heteromorphic but also monomorphic diaspores, the Division to which the diaspores of the vast majority of angiosperms belong. The scheme will be useful in describing the ecology, biogeography and evolution of seed heteromorphism in flowering plants.

Keywords

amphi-basicarpyamphicarpybasicarpychasmogamycleistogamygeocarpyheteroarthrocarpyseed (diaspore) heteromorphism
Type
Review Paper
Information
Seed Science Research , Volume 33 , Issue 4 , December 2023 , pp. 193 - 202
Check for updates
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution and reproduction, provided the original article is properly cited.
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press

Introduction

‘Seed (diaspore) heteromorphism’ is a broadly- and loosely-defined term used to describe differences in size/mass, morphology, position on mother plant and ecological function (e.g. dispersal, dormancy/germination) of two or more seeds or other diaspores produced by an individual plant. Thus, the term is applied to a variety of situations concerning degree of distinctness of differences in size/mass, morphology and position of diaspores on a plant. For example, Aethionema arabicum (Brassicaceae) produces two morphologically distinct aerial diaspores with no intermediates (Arshad et al., Reference Arshad, Sperber, Steinbrecher, Nichols, Jansen, Leubner-Metzger and Mummenhoff2019), Heterosperma pinnatum (Asteraceae) produces two morphologically distinct diaspores connected by a series of morphologically intermediate ones (Venable et al., Reference Venable, Búrquez, Corral, Morales and Espinosa1987, Reference Venable, Dyreson and Morales1995; Martorell and Martínez-López, Reference Martorell and Martínez-López2014) and Ceratocarpus arenarius (Amaranthaceae) produces two morphologically distinct ground-level diaspores and a series of aerial diaspores that differ continuously in size and morphology from top to bottom of the plant canopy (Lu et al., Reference Lu, Tan, Baskin and Baskin2013). It is no wonder, then, that in a recent paper Scholl et al. (Reference Scholl, Calle, Miller and Venable2020) stated that defining seed heteromorphism is a challenge.

The aim of this review paper is to provide an in-depth classification scheme, an earlier version of which was published in the second edition of ‘Seeds’ by Baskin and Baskin (Reference Baskin and Baskin2014), based on size, morphology and position on the mother plant that will give more exactness to use of the term ‘seed heteromorphism’. More generally, our aim was to characterize the diversity of structural design (‘architecture’) of diaspore monomorphism and heteromorphism in angiosperms.

Methods

Our classification scheme is based on information in the literature on the size/mass, morphology and position (e.g. aerial, basal and subterranean) on the mother plants of the diaspores of angiosperm taxa. Basically, we greatly expanded/modified the diaspore classification schemes of Mandák (Reference Mandák1997) and Barker (Reference Barker2005), sometimes using terminology that Zohary (Reference Zohary1937, Reference Zohary1962), Ellner and Shmida (Reference Ellner and Shmida1981) and van der Pijl (Reference van der Pijl1982) applied to diaspore dispersal. Seeds (diaspores) were first divided into two major categories (monomorphic and heteromorphic) called divisions and each Division into several successively lower hierarchical layers.

Our scheme does not include the terms that Zohary (Reference Zohary1937, Reference Zohary1962), Ellner and Shmida (Reference Ellner and Shmida1981), van der Pijl (Reference van der Pijl1982) and/or Gutterman (Reference Gutterman1993, Reference Gutterman1994b) used to describe agents/modes of dispersal such as anemochory (wind), hydrochory (water), ombrohydrochory (rain) and zoochory (animals). Neither does it include genetic polymorphism, in which (1) two or more kinds of diaspores are produced by a species, (2) a population may be diaspore-monomorphic or dimorphic/polymorphic and (3) individual plants produce only one kind of diaspore, which is determined by Mendelian inheritance, i.e. a genetic segregation, not a somatic differentiation (see Appendix A).

In general, we follow Scholl et al.'s (Reference Scholl, Calle, Miller and Venable2020) definition of ‘seed heteromorphism.’ According to these authors, variation in the morphology of heteromorphic diaspores can be discrete or continuous. However, if the variation is continuous the most extreme diaspores need to be widely divergent morphologically, such as occurs in H. pinnatum (see Introduction), for them to qualify as heteromorphic. Diaspores that do not meet one of these two criteria are, by default, considered to be monomorphic.

Results and discussion

The classification scheme we assembled for diaspore monomorphism and heteromorphism is shown in Table 1. However, as pointed out by Imbert (Reference Imbert2002) and Scholl et al. (Reference Scholl, Calle, Miller and Venable2020) seed heteromorphism (and thus monomorphism) is not easy to define. According to Harper et al. (Reference Harper, Lovell and Moore1970), most individual plants and populations have a normal or skewed (continuous) distribution for seed size or shape, but that ‘It is, however, characteristic of some species to produce two or more sharply defined types of seed.’ Thus, the word ‘monomorphic’ does not mean that all seeds on an individual plant have a single size/mass or morphology (or that they have the same degree of dormancy). In fact, there is considerable variation in these traits (especially mass) among monomorphic seeds on an individual plant and even among those on the same infructescence or within a fruit as various authors have reported (e.g. Janzen, Reference Janzen1977a, Reference Janzenb; Ernst, Reference Ernst1981; Thompson, Reference Thompson1981; Pitelka et al., Reference Pitelka, Thayer and Hansen1983; Stanton, Reference Stanton1984; Thompson, Reference Thompson1984; Wolf et al., Reference Wolf, Hainsworth, Mercier and Benjamin1986; Wulff, Reference Wulff1986; Michaels et al., Reference Michaels, Benner, Hartgerink, Lee and Rice1988; McGinley, Reference McGinley1989; Winn, Reference Winn1991; Fenner, Reference Fenner1992; Susko and Lovett-Doust, Reference Susko and Lovett-Doust2000). Monomorphic simply means that seeds cannot easily be sorted into two or more clearly-defined (distinct) groups based on traits such as size/mass and/or morphology. Monomorphic seeds may show differences in dormancy/germination: cryptic polymorphism (i.e. ecological differentiation in the absence of obvious morphological differences) of Venable (Reference Venable1985). Heteromorphic seeds, on the other hand, means that seeds on an individual plant readily can be sorted into two or more distinct groups that differ in size/mass and/or morphology.

Table 1. A classification system for monomorphic and heteromorphic diaspores in angiosperms based on size/mass, morphology and position on mother plant.

An excellent example of cryptic seed heteromorphism has been reported by Liyanage et al. (Reference Liyanage, Ayre and Ooi2016) for two species of Fabaceae (Bossiaea heterophylla and Viminaria juncea) whose seeds have physical dormancy. They found that individual plants of the two species, which occur in fire-prone ecosystems in southeastern Australia, produce seeds with a high threshold temperature and a low threshold temperature for physical dormancy break. There were no significant differences in mass or visible differences in shape or color of high- and low threshold temperature seeds from individual plants of either species. Seeds with a low threshold temperature for dormancy break could germinate after exposure to temperatures of a low-intensity fire (40–60°C), whereas those with a high threshold temperature for dormancy break could germinate only after exposure to temperatures of a high-intensity fire (≥80°C). Further, under competition with seedlings of Acacia linifolia (Fabaceae), a co-occurring species, seedlings of B. heterophylla emerging after low-intensity fire temperature grew better than those emerging after high-intensity fire temperature. Competition would be more intense following low- than high-intensity fire due to the survival of more plants in the low- than high-intensity-burned community. Thus, although low and high threshold temperature seeds did not exhibit differences in mass or morphology they differed in their dormancy-breaking response to fire intensity and in seedling growth response to competition resulting from different fire intensities.

Overall, we show that there is considerable structural diversity in design (‘architecture’) of diaspore-heteromorphic angiosperm species based on diaspore size, morphology and position on the mother plant and of diaspore-monomorphic angiosperms based on diaspore position (e.g. aerial, basal and subterranean) on the mother plant. To date, only a few hundred of the >250,000 extant angiosperm species have been reported to produce heteromorphic diaspores (Imbert, Reference Imbert2002; Wang et al., Reference Wang, Tan, Baskin and Baskin2010; Baskin et al., Reference Baskin, Lu, Baskin, Tan and Wang2014; Scholl et al., Reference Scholl, Calle, Miller and Venable2020; Zhang et al., Reference Zhang, Baskin, Baskin, Cheplick, Yang and Huang2020), apparently meaning that the vast majority of flowering plants produce monomorphic diaspores.

In a recent survey for homomorphic (=our monomorphic) and heteromorphic species in the North American deserts, using information in various floras for the area, Scholl et al. (Reference Scholl, Calle, Miller and Venable2020) identified 458 monomorphic species and 101 heteromorphic taxa, of which 75 of the latter were annuals. They also reported that their study brought the total number of known seed heteromorphic species to 378. The flora of this area contains many annuals, the climate is arid/semiarid and amount and timing of rainfall is unpredictable, which are conditions that favor bet-hedging via diaspore heteromorphism as a life history strategy (Scholl et al., Reference Scholl, Calle, Miller and Venable2020; Gianella et al., (Reference Gianella, Bradford and Guzzon2021). Thus, the North American deserts undoubtedly are highly over-represented in proportion of heteromorphic species compared to other bioclimatic regions. In which case, we should expect that the proportion of diaspore-heteromorphic species in the world's flora is much lower than that in the North American deserts.

Mandák's (Reference Mandák1997) classification scheme for seed (diaspore) heteromorphism divides heteromorphic diaspores into Amphicarpy and Heterodiaspory and distinguishes three subgroups for the latter category: heterocarpy (Heteromericarpy of van der Pijl, Reference van der Pijl1982), heteroarthrocarpy and heterospermy. (See Table 1 for definition of each of these three terms and of those mentioned in the following.) Barker's (Reference Barker2005) diaspore classification scheme deals only with basicarpy, geocarpy and amphicarpy. His scheme includes full geocarpy, with three subtypes, i.e. active geocarpy, geophytic geocarpy and passive geocarpy; and basicarpy, also with three subtypes, i.e. aerial amphicarpy, amphi-geocarpy and amphi-basicarpy. Note that all of the categories in Mandák's (Reference Mandák1997) scheme fit under our Division II (Heteromorphic), whereas the scheme of Barker (Reference Barker2005) includes terms under both our Division I (e.g. Full geocarpy) and Division II (e.g. Amphi-basicarpy). Imbert (Reference Imbert2002) recognized two categories of diaspore heteromorphism: heterocarpy and heterospermy.

Many species of grasses (Poaceae) produce cleistogamous (CL) axillary spikelets within leaf sheaths at nodes on flowering culms (Connor, Reference Connor1979, Reference Connor1981; Campbell et al., Reference Campbell, Quinn, Cheplick and Bell1983). Some grasses, e.g. the well-studied species Triplaris purpurea (e.g. Chase, Reference Chase1908, Reference Chase1918; Cheplick, Reference Cheplick1996; Cheplick and Sung, Reference Cheplick and Sung1998), produce these clandestine spikelets at all nodes on the flowering culm, which is terminated by an inflorescence of chasmogamous (CH) spikelets. Caryopsis mass decreases continuously [in a log-linear (or nearly so) fashion] from the lowermost to one of the upper leaf sheaths, above which there is little or no change in mass of caryopses, including those in the terminal CH spikelets. Chase (Reference Chase1908, Reference Chase1918) used the term ‘cleistogene’ to describe the solitary sessile single floret with palea and lemma but without glumes in the lower leaf sheaths of T. purpurea. Chase (Reference Chase1918) applied the term ‘chasmogene’ to the terminal (‘ordinary’) spikelet. Her illustrations clearly show that the caryopsis from the cleistogene is much larger than that from the chasmogene. We have (cautiously) suggested that T. pupurea might fit subgroup B of amphi-basicarpy (Table 1).

Monomorphic aerial CH/CL plants/populations may produce only CH or only CL flowers (Wilken, Reference Wilken1982; Sun, Reference Sun1999; Hayamizu et al., Reference Hayamizu, Hosokawa, Kimura and Ohara2014). Corallorhiza bentleyi (Orchidaceae), is an example of a species in which some populations produce only CL and others both CH and CL (see Freudenstein, Reference Freudenstein1999; Culley and Klooster, Reference Culley and Klooster2007). Small or young individuals of some CL species or individuals growing under unfavorable conditions produce only CL (Coker, Reference Coker1962; Minter and Lord, Reference Minter and Lord1983; Oakley et al., Reference Oakley, Moriuchi and Winn2007; Hayamizu et al., Reference Hayamizu, Hosokawa, Kimura and Ohara2014). Epifagus virginiana (Orobanchaceae) is an annual CL holoparasite with ‘dust seeds’ and an undifferentiated embryo that is host-specific on the roots of American beech (Fagus grandifolia). However, most, and sometimes all, of the flowers are CL, and the CH flowers usually are sterile. Thus, most seeds are produced by CL flowers (Schrenk, Reference Schrenk1894; Cooke and Schively, Reference Cooke and Schively1904; Thieret, Reference Thieret1969, Reference Thieret1971; Musselman, Reference Musselman1982).

Lloyd and Schoen (Reference Lloyd and Schoen1992) state that CH and CL seeds in most CL species differ in size, dispersal and germination. However, seeds from CH and CL flowers of our Group B of Supergroup 1 (monomorphic aerial) may or may not differ in these respects (Baskin and Baskin, Reference Baskin and Baskin2014, Reference Baskin and Baskin2017). When there is a difference in mass of CH and CL seeds, the mass of CH seeds usually is greater than that of CL seeds (e.g. Cope, Reference Cope1966; Hiratsuka and Inoue, Reference Hiratsuka and Inoue1988; Cheplick, Reference Cheplick2005; Eckstein et al., Reference Eckstein, Hölzel and Danihelka2006; Albert et al., Reference Albert, Campbell and Whitney2011; Huebner, Reference Huebner2011; Munguía-Rosas et al., Reference Munguía-Rosas, Parra-Tabla, Ollerton and Cervera2012). Differences in germination of CH and CL diaspores are more likely to occur in amphicarpic sensu stricto species than in aerial CL species. In 58 of 65 case studies (89.2%) for amphicarpic sensu stricto species, seeds from CH and Cl flowers differed in germination percentage, whereas in aerial CL species 83 of 132 case studies (62.9%) of seeds from CH and Cl flowers differed in germination percentage (Baskin and Baskin, Reference Baskin and Baskin2017). Further study may show that a new category needs to be split out of Group B (Supergroup I, Division I) and incorporated into Division II. The new category would include species in which fruits/seeds produced by CH and CL flowers are morphologically distinct and (presumably) differ in ecology.

In Ceratocarpus arenarius, the basicarps differ in morphology and mass (and in embryo mass) from the aerial dispersal/germination units, which show continuous variation (increase or decrease) in morphology (see Supplementary Table S1 in Lu et al., Reference Lu, Tan, Baskin and Baskin2013). Thus, there is discontinuous variation in this species between the basicarps (a) and aerial dispersal units (b)–(f) (Lu et al., Reference Lu, Tan, Baskin and Baskin2013). Gao and Wei (Reference Gao and Wei2007) and Gao et al., (Reference Gao, Wei and Yan2008) recognized only two morphological types of fruits on plants of this species, namely subterranean (the two basicarps, which are, in fact, basal and not subterranean) and aerial.

In Pisum fulvum (Fabaceae), there is a gradient from amphicarpic plants (sensu stricto) with both aerial and subterranean flowers and fruits to plants that produce only aerial flowers and fruits (Mattatia, Reference Mattatia1977). One of the stages in the gradient is a basicarpic form that produces CH flowers near the soil surface, which Mattatia (Reference Mattatia1977) called ‘subamphicarpic.’ Thus, this species consists of both monomorphic (e.g. basicarpic form) and heteromorphic (e.g. amphicarpic form) plants.

Some species may exhibit plasticity as to the diaspore classification category to which they belong. For example, species that are amphicarpic and produce both aerial and subterranean diaspores under favorable environmental conditions may produce only underground fruits under stressful conditions and thus be ‘facultatively geocarpic’, e.g. Amphicarpaea edgeworthii (Fabaceae) (Zhang et al., Reference Zhang, Baskin, Baskin, Yang and Huang2017), Amphicarpum amphicarpon (Poaceae) Cheplick and Quinn, Reference Cheplick and Quinn1983) and Gymnarrhena micrantha (Asteraceae) (Koller and Roth, Reference Koller and Roth1964; Zeide, Reference Zeide1978; Loria and Noy-Meir, Reference Loria and Noy-Meir1979/80). In which cases, individuals of these two annual species have the capacity to be either diaspore-heteromorphic (amphicarpic) or monomorphic (geocarpic).

Unlike these amphicarpic species, the cold desert annual diaspore-polymorphic amphi-basicarpic species Ceratocarpus arenarius produces both basal (typically two) and aerial diaspores in the most stressful conditions in which it grows in its cold desert habitat. In the cold deserts of northwest China, we have observed that the smallest (5 cm tall, no branches) and largest (35 cm tall, bushy) plants of this species produce both basal and aerial diaspores, albeit in different basal morph:aerial morph and within-aerial morph ratios. Detailed experimental garden studies on the effect of abiotic (e.g. soil physicochemistry) and biotic (i.e. inter- and intraspecific competition) stress on phenotypic plasticity of the growth and reproduction of C. arenarius, including variation in diaspore morph ratios, have been published by Gan et al. (Reference Gan, Lu, Baskin, Baskin and Tan2020) and Lu et al. (Reference Lu, Gan, Tan, Baskin and Baskin2021).

Concluding remarks

We have documented via a hierarchical-based classification system the considerable diversity in structural design (‘architecture’) of diaspore monomorphism and heteromorphism in angiosperms. The scheme will enable investigators working on the broad topic of ‘seed heteromorphism’ to more precisely communicate their research to others, in part at least by giving more exactness to the term. It also will aid plant biologists in the preparation of a profile (spectrum) of the kinds (hierarchical categories) of diaspore monomorphism and heteromorphism for the various ecological and biogeographical units on earth. Finally, a detailed classification scheme that includes both diaspore monomorphism and hetermorphism is required for addressing the phylogenetic/evolutionary aspects of ‘seed heteromorphism’ in angiosperms (e.g. see Fernández et al., Reference Fernández, Aguilar, Panero and Feliner2001; Cruz-Mazo et al., Reference Cruz-Mazo, Buide, Samuel and Narbona2009, Reference Cruz-Mazo, Narbona and Buide2010). All that being said, however, it is likely that more hierarchical categories will need to be added to our system and/or existing ones revised/refined as literature and field research continues on diaspore monomorphism and heteromorphism in angiosperms.

Conflict of interest

The authors declare that they have no competing interests.

Appendix A Genetic diaspore polymorphism in angiosperms

Genetic diaspore polymorphism is best known in the family Valerianaceae, including Plectritis (Ganders et al., Reference Ganders, Carey and Griffiths1977a,Reference Ganders, Carey and Griffithsb; Carey and Ganders, Reference Carey and Ganders1980) and Valerianella (Eggers Ware, Reference Eggers Ware1983). In Plectritis congesta, experimental crosses showed that the kind of fruit morph is monogenically inherited with the allele for winged fruits dominant over wingless fruits (Ganders et al., Reference Ganders, Carey and Griffiths1977a). In Plectritis brachystemon, homozygous winged plants (i.e. selfed plants produced only winged fruits) x homozygous wingless fruits (i.e. selfed plants produced only wingless fruits) → F1 hybrids, all of which produced winged fruits. The F2 (F1 selfed) consisted of 27 plants that produced winged fruits and nine that produced wingless fruits (a 3:1 ratio). Thus, fruit dimorphism in P. brachystemon is controlled by a single locus with the allele for winged fruit dominant (Ganders et al., Reference Ganders, Carey and Griffiths1977b). In Valerianella ozarkana, crosses between forma ozarkana (winged) and forma bushii (fusiform) indicated that there was a simple monogenic relationship in which the ozarkana (winged) allele is dominant over the bushii (fusiform) allele (Eggers-Ware, Reference Eggers Ware1983). It should be pointed out that not all species that produce two or more kinds of diaspores fit either somatic polymorphism or genetic polymorphism, i.e. they neither fit one nor the other. Fedia cornucopiae and F. grandflora (Valerianaceae) have been shown to exhibit both somatic and genetic polymorphism (Mathez and Xena de Enrich, Reference Mathez, Xena de Enrich, Jacquar, Heim and Antonovics1985a, Reference Mathez and Xena de Enrich1985b).,

Genetic diaspore heteromorphism (only one morph per plant) has been reported in the two grass species Aegilops speltoides (e.g. Zohary and Imber, Reference Zohary and Imber1963; Belyayev and Raskina, Reference Belyayev and Raskina2013; Ruban and Badaeva, Reference Ruban and Badaeva2018) and Achnatherum hymenoides (Jones and Nielson, Reference Jones and Nielson1999; Jones et al., Reference Jones, Redinbaugh, Larson, Zhang and Dow2007). In one of the two morphotypes of A. speltoides (i.e. form aucheri), the spike is the dispersal unit, and in the other morphotype (form ligustica) the spikelet is the dispersal unit. In A. hymenoides, seed size, i.e. jumbo > globose > elongate) is under genetic control, and degree of seed dormancy decreases from jumbo to globose to elongate.

A kind of genetic polymorphism for capitulum type occurs in British populations of Senecio vulgaris (Asteraceae). Plants of this species have radiate and non-radiate capitulum morphs, which are under genetic control. The radiate morph originated via introgressive hybridization between the native non-radiate allotetraploid S. vulgaris and the introduced diploid radiate S. squalidus. Two tightly-linked genes of S. squalidus were introgressed into S. vulgaris. A short-rayed form (a heterozygote) is produced from crosses between radiate and non-radiate forms of S. vulgaris. Fresh cypselae from radiate and non-radiate morphs differ in germination phenology. There also were differences in germination percentages after cypselae from radiate and non-radiate morphs were stored in the laboratory from October to June, during which time after-ripening may have occurred (e.g. Trow, Reference Trow1912; Richards, Reference Richards1975; Ingram et al., Reference Ingram, Weir and Abbott1980; Abbott, Reference Abbott1986, Reference Abbott, Ashton and Forbes1992; Abbott et al., Reference Abbott, Horrill and Noble1988, Reference Abbott, Ashton and Forbes1992, Reference Abbott, Bretagnolle and Thébaud1998; Abbott and Horrill, Reference Abbott and Horrill1991; Chapman and Abbott, Reference Chapman and Abbott2010).

Spergula and Spergularia are two genera in the Caryophyllaceae containing species that produce heteromorphic seeds with a genetic component. Spergula arvensis produces papilate (P) and smooth, i.e. non-papilate (NP), seeds and a hybrid (P × NP) intermediate between the two morphs; the hybrid is produced in a low frequency. Inheritance of seed coat character is controlled by one gene, one locus and two alleles. The intermediate morph is heterozygous with incomplete dominance (New, Reference New1958, Reference New1959, Reference New1961, Reference New1978; New and Herriott, Reference New and Herriott1981; Wagner, Reference Wagner1986, Reference Wagner1988; Kucewicz and Gojło, Reference Kucewicz and Gojło2013).

Several species of Spergularia (e.g. S. marina and S. media) produce winged and non-winged seeds and a heterzygous intermediate with a narrow wing produced in a low frequency (Salisbury, Reference Salisbury1958; Sterk, Reference Sterk1969a,Reference Sterkb,Reference Sterkc,Reference Sterkd; Sterk and Dijkhuizen, Reference Sterk and Dijkhuizen1972; Telenius and Torstensson, Reference Telenius and Torstensson1989, Reference Telenius and Torstensson1991; Telenius, Reference Telenius1992; Ceynowa-Giełdon, Reference Ceynowa-Giełdon1993; Redbo-Torstensson, Reference Redbo-Torstensson1994; Redbo-Torstensso and Telenius, Reference Redbo-Torstensson and Telenius1995; Reference Telenius and Torstensson1999; Mazer and Lowrey, Reference Mazer and Lowrey2003; Memon et al., Reference Memon, Bhatti, Khalid, Arshad, Mirbahar and Qureshi2010). Seeds of Spergularia diandra collected near Sede Boker in the Negev Desert of Israel consisted of three genotypes (hairy, partly-hairy and smooth). Each genotype had three seed-color phenotypes (black, brown and yellow), and there were differences in germination of the phenotypes. Thus, there were nine seed morphs, i.e. 3 phenotypes × 3 genotypes = 9 types of seed morphs (Gutterman, Reference Gutterman1994a, Reference Gutterman1996, Reference Gutterman1997a, Reference Gutterman, Ellis, Black, Murdoch and Hongb, Reference Gutterman and Ambasht1998, Reference Gutterman2000).

References

Abbott, RJ (1986) Life history variation associated with the polymorphism for capitulum type and outcrossing rate in Senecio vulgaris L. Heredity 56, 381–391.CrossRefGoogle Scholar
Abbott, RJ (1992) Plant invasions, interspecific hybridization and the evolution of new plant taxa. Trends in Ecology and Evolution 7, 401–406.CrossRefGoogle ScholarPubMed
Abbott, RJ and Horrill, JC (1991) Survivorship and fecundity of the radiate and non-radiate morphs of groundsel, Senecio vulgaris L., raised in pure stand and mixture. Journal of Evolutionary Biology 4, 241–257.CrossRefGoogle Scholar
Abbott, RJ, Horrill, JC and Noble, GDG (1988) Germination behavior of the radiate and non-radiate morphs of groundsel, Senecio vulgaris L. Heredity 60, 15–20.CrossRefGoogle Scholar
Abbott, RJ, Ashton, PA and Forbes, DG (1992) Introgressive origin of the radiate groundsel, Senecio vulgaris L. var. hibernicus Syme: Aat-3 evidence. Heredity 68, 425–436.CrossRefGoogle Scholar
Abbott, RJ, Bretagnolle, FD and Thébaud, C (1998) Evolution of a polymorphism for outcrossing rate in Senecio vulgaris: influence of germination behavior. Evolution 52, 1593–1601.Google ScholarPubMed
Ackerman, JD (2006) Sexual reproduction of seagrasses: pollination in the marine context, pp. 89–109 in Larkum, AWD; Orth, RJ; Duarte, CM (Eds) Seagrasses: Biology, Ecology and Conservation, Dordrecht, Springer.Google Scholar
Albert, LP, Campbell, LG and Whitney, KD (2011) Beyond simple reproductive assurance: cleistogamy allows adaptive plastic responses to pollen limitation. International Journal of Plant Sciences 172, 862–869.CrossRefGoogle Scholar
Arshad, A, Sperber, K, Steinbrecher, T, Nichols, B, Jansen, VAA, Leubner-Metzger, G and Mummenhoff, K (2019) Dispersal biophysics and adaptive significance of dimorphic diaspores in the annual Aethionema arabicum (Brassicaceae). New Phytologist 221, 1434–1446.CrossRefGoogle ScholarPubMed
Arthur, JC (1895) Delayed germination of cocklebur and other paired seeds. Proceedings of the Sixteenth Annual Meeting of the Society for the Promotion of Agricultural Science 16, 70–79.Google Scholar
Arthur, JC (1906) The paired seeds of cocklebur. The Plant World 9, 227–232.Google Scholar
Baker, GA and O'Dowd, DJ (1982) Effects of parent plant density on the production of achene types in the annual Hypochoeris glabra. Journal of Ecology 70, 201–215.CrossRefGoogle Scholar
Barbour, MG (1970) Germination and early growth of the strand plant Cakile maritima. Bulletin of the Torrey Botanical Club 97, 13–22.CrossRefGoogle Scholar
Barker, NP (2005) A review and survey of basicarpy, geocarpy, and amphicarpy in the African and Madagascan flora. Annals of the Missouri Botanical Garden 92, 445–462.Google Scholar
Baskin, CC and Baskin, JM (2014) Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination (2nd Edn). San Diego, Elsevier/Academic Press.Google Scholar
Baskin, JM and Baskin, CC (2017) Seed germination in cleistogamous species: theoretical considerations and a literature survey of experimental results. Seed Science Research 27, 84–98.CrossRefGoogle Scholar
Baskin, JM and Baskin, CC (2022) Germination and seed/embryo size in holoparasitic flowering plants with “dust seeds” and an undifferentiated embryo. The Botanical Review 88, 1–49.CrossRefGoogle Scholar
Baskin, JM, Lu, JJ, Baskin, CC, Tan, DY and Wang, L (2014) Diaspore dispersal ability and degree of dormancy in heteromorphic species of cold deserts of northwest China: a review. Perspectives in Plant Ecology, Evolution and Systematics 16, 93–99.CrossRefGoogle Scholar
Belyayev, A and Raskina, O (2013) Chromosomes evolution in marginal populations of Aegilops speltoides and consequences. Annals of Botany 111, 531–538.CrossRefGoogle ScholarPubMed
Bolin, JF, Maass, E, Tennakoon, KU and Musselman, L (2009) Host-specific germination of the root holoparasite Hydnora triceps (Hydnoraceae). Botany 87, 1250–1254.CrossRefGoogle Scholar
Borchenius, F and Olesen, JM (1990) The Amazonian root holoparasite Lophohytum mirabile (Balanophoraceae) and its pollinators and herbivores. Journal of Tropical Ecology 6, 501–505.CrossRefGoogle Scholar
Browning, J (1992) Hypogynous bristles and scales in basal florets in amphicarpous Schoenoplectus species (Cyperaceae). Nordic Journal of Botany 12, 171–175.CrossRefGoogle Scholar
Bruhl, JJ (1994) Amphicarpy in the Cyperaceae, with novel variation in the wetland sedge Eleocharis caespitosissima Baker. Australian Journal of Botany 42, 441–448.CrossRefGoogle Scholar
Burtt, BL (1970) The evolution and taxonomic significance of a subterranean ovary in certain monocotyledons. Israel Journal of Botany 19, 77–90.Google Scholar
Burtt, BL (1977) Aspects of diversification in the capitulum, pp. 41–59 in Heywood, VH; Harborne, JB; Turner, BL (Eds) The Biology and Chemistry of the Compositae, London, Academic Press.Google Scholar
Campbell, CS, Quinn, JA, Cheplick, GP and Bell, TJ (1983) Cleistogamy in grasses. Annual Review of Ecology and Systematics 13, 411–441.CrossRefGoogle Scholar
Carey, K and Ganders, FR (1980) Heterozygote advantage at the fruit wing locus in Plectritis congesta (Valerianaceae). Evolution 34, 601–607.CrossRefGoogle ScholarPubMed
Carlquist, S (1976) Alexgeorgea, a bizarre new genus of Restionaceae from Western Australia. Australian Journal of Botany 24, 281–295.CrossRefGoogle Scholar
Ceynowa-Giełdon, M (1993) The variability of seeds in Spergularia marina (L.) Griseb. (=S. salina J. et C. Presl) growing on seacoast and inland saline soils in Poland. Acta Societatis Botanicorum Poloniae 62, 185–191.CrossRefGoogle Scholar
Chapman, MA and Abbott, RJ (2010) Introgression of fitness genes across a ploidy barrier. New Phytologist 186, 63–71.CrossRefGoogle ScholarPubMed
Chase, A (1908) Notes on cleistogamy of grasses. Botanical Gazette 45, 135–136.CrossRefGoogle Scholar
Chase, A (1918) Axillary cleistogenes in some American grasses. American Journal of Botany 5, 254–258.CrossRefGoogle Scholar
Cheplick, GP (1996) Cleistogamy and seed heteromorphism in Triplasis purpurea (Poaceae). Bulletin of the Torrey Botanical Club 123, 25–33.CrossRefGoogle Scholar
Cheplick, GP (2005) Biomass partitioning and reproductive allocation in the invasive, cleistogamous grass Microstegium vimineum: influence of the light environment. Bulletin of the Torrey Botanical Society 132, 214–224.CrossRefGoogle Scholar
Cheplick, GP and Clay, K (1989) Convergent evolution of cleistogamy and seed heteromorphism in two perennial grasses. Evolutionary Trends in Plants 3, 127–136.Google Scholar
Cheplick, GP and Quinn, JA (1983) The shift in aerial/subterranean fruit ratio in Amphicarpum purshii: causes and significance. Oecologia 57, 374–379.CrossRefGoogle ScholarPubMed
Cheplick, GP and Sung, LY (1998) Effects of maternal nutrient environment and maturation position on seed heteromorphism, germination, and seedling growth in Triplasis purpurea (Poaceae). International Journal of Plant Sciences 159, 338–350.CrossRefGoogle Scholar
Coker, PD (1962) Biological flora of the British Isles. Corrigiola litoralis L. Journal of Ecology 50, 833–840.CrossRefGoogle Scholar
Connor, HE (1979) Breeding systems in the grasses: a survey. New Zealand Journal of Botany 17, 547–574.CrossRefGoogle Scholar
Connor, HE (1981) Evolution of reproductive systems in the Gramineae. Annals of the Missouri Botanical Garden 68, 48–74.CrossRefGoogle Scholar
Cope, WA (1966) Growth rate and yield in sericea lespedeza in relation to seed size and outcrossing. Crop Science 6, 566–568.CrossRefGoogle Scholar
Cooke, E and Schively, AF (1904) Observations on the Structure and Development of Epiphegus virginiana, vol. 2. Contributions from the Botanical Laboratory of the University of Pennsylvania. Philadelphia, University of Pennsylvania Press. pp. 352–398. + plates XXIX-XXXII.Google Scholar
Crocker, W (1906) Role of seed coats in delayed germination. Botanical Gazette 42, 265–291.CrossRefGoogle Scholar
Cruz-Mazo, G, Buide, ML, Samuel, R and Narbona, E (2009) Molecular phylogeny of Scorzoneroides (Asteraceae): evolution of heterocarpy and annual habit in unpredictable environments. Molecular Phylogenetics and Evolution 53, 835–847.CrossRefGoogle ScholarPubMed
Cruz-Mazo, G, Narbona, E and Buide, ML (2010) Germination patterns of dimorphic achenes in three related species of Scorzoneroides (Asteraceae, Lactuceae) growing in different environments. Annales Botanici Fennici 47, 337–345.CrossRefGoogle Scholar
Culley, TM and Klooster, MR (2007) The cleistogamous breeding system: a review of its frequency, evolution, and ecology in angiosperms. The Botanical Review 73, 1–30.CrossRefGoogle Scholar
Darwin, C (1888) The Power of Movement in Plants. New York, D. Appleton and Company.Google Scholar
Datta, SC, Evenari, M and Gutterman, Y (1970) The heteroblasty of Aegilops ovata L. Israel Journal of Botany 19, 463–483.Google Scholar
Dobrenz, AK and Beetle, AA (1966) Cleistognes in Danthonia. Journal of Range Management 19, 292–296.CrossRefGoogle Scholar
Donald, WE and Ogg, AG Jr (1991) Biology and control of jointed goatgrass (Aegilops cylindrica), a review. Weed Technology 5, 3–17.CrossRefGoogle Scholar
Donohue, K (1997) Seed dispersal in Cakile edentula var. lacustris: decoupling the fitness effects of density and distance from the home site. Oecologia 110, 520–527.CrossRefGoogle ScholarPubMed
Dowling, RE (1933) The reproduction of Plantago coronopus: an example of morphological and biological seed dimorphism. Annals of Botany 47, 861–872.CrossRefGoogle Scholar
Dyer, AR (2004) Maternal and sibling factors induce dormancy in dimorphic seed pairs of Aegilops triuncialis. Plant Ecology 172, 211–218.CrossRefGoogle Scholar
Eckstein, RL, Hölzel, N and Danihelka, J (2006) Biological flora of Central Europe: Viola elatior, V. pumila and V. stagnina. Perspectives in Plant Ecology, Evolution and Systematics 8, 45–66.CrossRefGoogle Scholar
Eggers Ware, DM (1983) Genetic fruit polymorphism in North American Valerianella (Valerianaceae) and its taxonomic implications. Systematic Botany 8, 33–44.CrossRefGoogle Scholar
Ellner, S and Shmida, A (1981) Why are adaptations for long-range seed dispersal rare in desert plants? Oecologia 51, 133–144.Google Scholar
Ernst, WHO (1981) Ecological implication of fruit variability in Phleum arenarium L., an annual dune grass. Flora 171, 387–398.CrossRefGoogle Scholar
Esashi, Y and Leopold, AC (1968) Physical forces in dormancy and germination of Xanthium seeds. Plant Physiology 43, 871–876.CrossRefGoogle ScholarPubMed
Fandrich, L and Mallory-Smith, CA (2006) Factors affecting germination of jointed goatgrass (Aegilops cylindrica) seed. Weed Science 54, 677–684.CrossRefGoogle Scholar
Fenner, M (1992) Environmental influences on seed size and composition. Horticultural Reviews 13, 183–213.CrossRefGoogle Scholar
Fernández, IA, Aguilar, JF, Panero, JL and Feliner, GN (2001) A phylogenetic analysis of Doronicum (Asteraceae, Senecioneae) based on morphological, nuclear ribosomal (ITS), and chloroplast (trnL-F) evidence. Molecular Phylogenetics and Evolution 20, 41–64.CrossRefGoogle Scholar
Flores-Olvera, H, Vrijdaghs, A, Ochoterena, H and Smets, E (2011) The need to re-investigate the nature of homoplastic characters: an ontogenetic case study of the ‘bracteoles’ in Atripliceae (Chenopodiaceae). Annals of Botany 108, 847–865.CrossRefGoogle ScholarPubMed
Freudenstein, JV (1999) A new species of Corallorhiza (Orchidaceae) from West Virginia, U.S.A. Novon 9, 511–513.CrossRefGoogle Scholar
Gan, L, Lu, J, Baskin, JM, Baskin, CC and Tan, D (2020) Phenotypic plasticity in diaspore production of a amphi-basicarpic cold desert annual that produces polymorphic diaspores. Scientific Reports 10, 11142.CrossRefGoogle ScholarPubMed
Ganders, FR, Carey, K and Griffiths, AJF (1977a) Natural selection for a fruit dimorphism in Plectritis congesta (Valerianaceae). Evolution 31, 873–881.CrossRefGoogle ScholarPubMed
Ganders, FR, Carey, K and Griffiths, AJF (1977b) Outcrossing rates in natural populations of Plectritis brachystemon (Valerianaceae). Canadian Journal of Botany 55, 2070–2074.CrossRefGoogle Scholar
Gao, R and Wei, Y (2007) Amphicarpy of Ceratocarpus arenarius (Chenopodiaceae) in Junggar Desert. Acta Botanica Yunnanica 29, 300–302. (in Chinese with English abstract)Google Scholar
Gao, R, Wei, Y and Yan, C (2008) Amphicarpy and seed germination behavior of Ceratocarpus arenarius L. (Chenopodiaceae). Chinese Journal of Ecology 27, 23–27. (in Chinese with English abstract)Google Scholar
Gianella, M, Balestrazzi, A, Pagano, A, Müller, JV, Kyratzis, AC, Kikodze, D, Canella, M, Mondoni, A, Rossi, G and Guzzon, F (2020) Heteromorphic seeds of wheat wild relatives show germination niche differentiation. Plant Biology 22, 191–202.CrossRefGoogle ScholarPubMed
Gianella, M, Balestrazzi, A, Ravasio, A, Mondoni, A, Börner, A and Guzzon, F (2022) Comparative seed longevity under genebank storage and artificial ageing: a case study in heteromorphic wheat wild relatives. Plant Biology 24, 836–845.CrossRefGoogle ScholarPubMed
Gianella, M, Bradford, KJ and Guzzon, F (2021) Ecological, (epi)genetic and physiological aspects of bet-hedging in angiosperms. Plant Reproduction 34, 21–36.CrossRefGoogle ScholarPubMed
Gomez-Cabellos, A, Toorop, PE, Cañal, MJ, Iannetta, PPM, Fernández-Pascual, E, Pritchard, HW and Visscher, AM (2022) Global DNA methylation and cellular 5-methylcytosine and H4 acetylated patterns in primary and secondary dormant seeds of Capsella bursa-pastoris (L.) Medik. (shepherd's purse). Protoplasma 259, 595–614.CrossRefGoogle ScholarPubMed
Gutterman, Y (1993) Seed Germination in Desert Plants. Berlin, Springer-Verlag.CrossRefGoogle Scholar
Gutterman, Y (1994a) In memoriam – Michael Evenari and his desert. Seed dispersal and germination strategies of Spergularia diandra compared with some other desert annual plants inhabiting the Negev Desert of Israel. Israel Journal of Plant Sciences 42, 261–274.CrossRefGoogle Scholar
Gutterman, Y (1994b) Strategies of seed dispersal and germination in plants inhabiting deserts. The Botanical Review 60, 373–425.CrossRefGoogle Scholar
Gutterman, Y (1996) Environmental influences during seed maturation and storage affecting germinability in Spergularia diandra genotypes inhabiting the Negev Desert, Israel. Journal of Arid Environments 34, 313–323.CrossRefGoogle Scholar
Gutterman, Y (1997a) Effect of daylength on flowering and seed morphology of Spergularia diandra occurring in the Negev Desert, Israel. Journal of Arid Environments 36, 611–622.CrossRefGoogle Scholar
Gutterman, Y (1997b) Genotypic, phenotypic and opportunistic germination strategies of some common desert annuals compared with plants with other seed dispersal and germination strategies, pp. 611–622 in Ellis, RH; Black, M; Murdoch, AJ; Hong, TD (Eds) Basic and Applied Aspects of Seed Biology, Dordrecht, Kluwer Academic Publishers.CrossRefGoogle Scholar
Gutterman, Y (1998) Ecological strategies of desert annual plants, pp. 203–231 in Ambasht, RS (Ed) Modern Trends in Ecology and Environment, Leiden, Backhuys Publishers.Google Scholar
Gutterman, Y (2000) Environmental factors and survival strategies of annual plant species in the Negev Desert, Israel. Plant Species Biology 15, 113–125.CrossRefGoogle Scholar
Guzzon, F, Orsenigo, S, Gianella, M, Müller, JV, Vagge, I, Rossi, G and Mondoni, A (2018) Seed heteromorphy influences seed longevity in Aegilops. Seed Science Research 28, 277–285.CrossRefGoogle Scholar
Haines, R (1971) Amphicarpy in east African Cyperaceae. Mitteilungen der Botanischen Staatssammlung Munchen 10, 534–538.Google Scholar
Haines, RW and Lye, KA (1977) Studies in African Cyperaceae. XV. Amphicarpy and spikelet structure in Trianoptiles solitaria. Botaniska Notiser 130, 235–240.Google Scholar
Hall, JC, Tisdale, TE, Donohue, K, Wheeler, A, Al-Yahya, MA and Kramer, EM (2011) Convergent evolution of a complex fruit structure in tribe Brassiceae (Brassicaceae). American Journal of Botany 98, 1989–2003.CrossRefGoogle ScholarPubMed
Harper, JL (1977) Population biology of plants. London, Academic Press.Google Scholar
Harper, JL, Lovell, PH and Moore, KG (1970) The shapes and sizes of seeds. Annual Review of Ecology and Systematics 1, 327–356.CrossRefGoogle Scholar
Hayamizu, M, Hosokawa, I, Kimura, O and Ohara, M (2014) Intraspecific variation in life history traits of Viola brevistipulata (Violaceae) in Hokkaido. Plant Species Biology 29, 85–91.CrossRefGoogle Scholar
Hiratsuka, A and Inoue, O (1988) Dispersability of dimorphic seeds in Impatiens noli-tangere and I. textori (Balsaminaceae). Ecological Review 21, 157–161.Google Scholar
Hocking, PJ (1982) Salt and mineral nutrient levels in fruits in two strand species, Cakile maritima and Arctotheca populifolia, with special reference to the effect of salt on the germination of Cakile. Annals of Botany 50, 335–343.Google Scholar
Hockling, PJ and Liddle, MJ (1986) The biology of Australian weeds: 15. Xanthium occidentale Bertol. complex and Xanthium spinosum L. Journal of the Australian Institute of Agricultural Science 52, 191–221.Google Scholar
Horovitz, A, Ezrati, S and Anikster, Y (2013) Are soil seed banks relevant for agriculture in our day? Crop Wild Relatives 9, 27–30.Google Scholar
Huebner, CD (2011) Seed mass, viability, and germination of Japanese stiltgrass (Microstegium vimineum) under variable light and moisture conditions. Invasive Plant Science and Management 4, 274–283.CrossRefGoogle Scholar
Imbert, E (2002) Ecological consequences and ontogeny of seed heteromorphism. Perspectives in Plant Ecology, Evolution and Systematics 5, 13–36.CrossRefGoogle Scholar
Imbert, E and Ronce, O (2001) Phenotyic plasticity for dispersal ability in the seed heteromorphic Crepis sancta (Asteraceae). Oikos 93, 126–134.CrossRefGoogle Scholar
Ingram, R, Weir, J and Abbott, RJ (1980) New evidence concerning the origin of inland radiate groundsel, S. vulgaris L. var. hibernicus Syme. New Phytologist 84, 543–546.CrossRefGoogle Scholar
Janzen, DH (1977a) Variation in seed weight in Costa Rican Cassia grandis (Leguminosae). Tropical Ecology 18, 177–186.Google Scholar
Janzen, DH (1977b) Variation in seed size within a crop of a Costa Rican Mucuna andreana (Leguminosae). American Journal of Botany 64, 347–349.CrossRefGoogle Scholar
Jones, TA and Nielson, DC (1999) Intrapopulation genetic variation for seed dormancy in Indian ricegrass. Journal of Range Management 52, 646–650.CrossRefGoogle Scholar
Jones, A, Redinbaugh, MG, Larson, SR, Zhang, Y and Dow, BD (2007) Polymorphic Indian ricegrass populations result from overlapping waves of migration. Western North American Naturalist 67, 338–346.CrossRefGoogle Scholar
Katznelson, J and Morley, FHW (1965) A taxonomic revision of sect. Calycomorphum of the genus Trifolium. I. The geocarpic species. Israel Journal of Botany 14, 112–134.Google Scholar
Keddy, PA (1980) Population ecology in an environmental mosaic: Cakile edentula on a gravel bar. Canadian Journal of Botany 58, 1095–1100.CrossRefGoogle Scholar
Keddy, PA (1982) Population ecology on an environmental gradient: Cakile edentula on a sand dune. Oecologia 52, 348–355.CrossRefGoogle Scholar
Koller, D and Roth, N (1964) Studies on the ecological and physiological significance of amphicarpy in Gymnarrhena micrantha (Compositae). American Journal of Botany 51, 26–35.CrossRefGoogle Scholar
Kucewicz, M and Gojło, E (2013) Ecological importance of seed dimorphism in corn spurry (Spergula arvensis L.) 1. The effects of day length on seed germinability. Polish Journal of Ecology 61, 665–673.Google Scholar
Kuo, J and Kirkman, H (1992) Fruits, seeds and germination in the seagrass Halophila ovalis (Hydrocharitaceae). Botanica Marina 35, 197–204.CrossRefGoogle Scholar
Lerner, PD, Bai, Y and Morici, EFA (2008) Does seed heteromorphism have different roles in the fitness of species with contrasting life history strategies? Botany 86, 1404–1415.CrossRefGoogle Scholar
Liyanage, GS, Ayre, DJ and Ooi, MKJ (2016) Seedling performance covaries with dormancy thresholds: maintaining cryptic seed heteromorphism in a fire-prone system. Ecology 97, 3009–3018.CrossRefGoogle Scholar
Lloyd, DG and Schoen, DJ (1992) Self- and cross-fertilization in plants. I. Functional dimensions. International Journal of Plant Sciences 153, 358–369.CrossRefGoogle Scholar
Lord, EM (1981) Cleistogamy: a tool for the study of floral morphogenesis, function and evolution. The Botanical Review 47, 421–449.CrossRefGoogle Scholar
Loria, M and Noy-Meir, I (1979/80) Dynamics of some annual populations in a desert loess plain. Israel Journal of Botany 28, 211–225.Google Scholar
Lu, JJ, Tan, DY, Baskin, JM and Baskin, CC (2010) Fruit and seed heteromorphism in the cold desert annual ephemeral Diptychocarpus strictus (Brassicaceae) and possible adaptive significance. Annals of Botany 105, 999–1014.CrossRefGoogle ScholarPubMed
Lu, JJ, Tan, DY, Baskin, JM and Baskin, CC (2012) Phenotypic plasticity and bet-hedging in a heterocarpic winter annual/spring ephemeral cold desert species of Brassicaceae. Oikos 121, 357–366.CrossRefGoogle Scholar
Lu, JJ, Tan, DY, Baskin, JM and Baskin, CC (2013) Tradeoffs between seed dispersal and dormancy in an amphi-basicarpic cold desert annual. Annals of Botany 112, 1815–1827.CrossRefGoogle Scholar
Lu, JJ, Gan, L, Tan, DY, Baskin, JM and Baskin, CC (2021) Effects of the habitat-soil factor on transgenerational plasticity in a diaspore-polymorphic cold desert annual. Plant and Soil 461, 355–367.CrossRefGoogle Scholar
Mandák, B (1997) Seed heteromorphism and the life cycle of plants: a review. Preslia 69, 129–159.Google Scholar
Mandák, B and Pyšek, P (1999) Effects of plant density and nutrient levels on fruit polymorphism in Atriplex sagittata. Oecologia 119, 63–72.Google ScholarPubMed
Marañon, T (1989) Variations in seed size and germination in three Aegilops species. Seed Science & Technology 17, 583–588.Google Scholar
Martin, RJ and Carnahan, JA (1983) The effect of field storage and laboratory conditions on germination of five Xanthium species. Australian Journal of Agricultural Research 34, 249–260.CrossRefGoogle Scholar
Martorell, C and Martínez-López, M (2014) Informed dispersal in plants: Heterosperma pinnatum (Asteraceae) adjusts its dispersal mode to escape from competition and water stress. Oikos 123, 225–231.CrossRefGoogle Scholar
Mathez, J and Xena de Enrich, N (1985a) Heterocarpy, fruit polymorphism and discriminating dissemination in the genus Fedia (Valerianaceae), pp. 431–441 in Jacquar, P; Heim, G; Antonovics, J (Eds) Genetic Differentiation and Dispersal in Plants, Berlin, Springer-Verlag.CrossRefGoogle Scholar
Mathez, J and Xena de Enrich, N (1985b) Le polymorphisme genetique de la morphologie des fruits du genere Fedia Gaertn. (Valerianaceae). I. Determination du mecanisme de controle genetique chez les especies F. cornucopiae (L.) Gaertn. et F. graciliflora Fisch. & Meyer. Candollea 40, 425–434.Google Scholar
Mattatia, J (1977) Amphicarpy and variability in Pisum fulvum. Botaniska Notiser 130, 27–34.Google Scholar
Maun, MA and Payne, AM (1989) Fruit and seed polymorphism and its relation to seedling growth in the genus Cakile. Canadian Journal of Botany 67, 2743–2750.CrossRefGoogle Scholar
Maun, MA, Boyd, RS and Olson, L (1990) The biological flora of coastal dunes and wetlands. 1. Cakile edentula (Bigel.) Hook. Journal of Coastal Research 6, 137–156.Google Scholar
Mazer, SJ and Lowrey, DE (2003) Environmental, genetic, and seed mass effects on winged seed production in the heteromorphic Spergularia marina (Caryophyllaceae). Functional Ecology 17, 637–650.CrossRefGoogle Scholar
McGinley, MA (1989) Within and among plant variation in seed mass and pappus size in Tragopogon dubious. Canadian Journal of Botany 67, 1298–1304.CrossRefGoogle Scholar
Memon, RS, Bhatti, GR, Khalid, S, Arshad, M, Mirbahar, AA and Qureshi, R (2010) Microstructural features of seeds of Spergularia marina (L.) Griseb. (Caryophyllaceae). Pakistan Journal of Botany 42, 1423–1427.Google Scholar
Meney, KA, Pate, JS and Dixon, KW (1990) Comparative morphology, anatomy, phenology and reproductive biology of Alexgeorgea spp. (Restionaceae) from south-western Western Australia. Australian Journal of Botany 38, 523–541.CrossRefGoogle Scholar
Michaels, HJ, Benner, B, Hartgerink, AP, Lee, TD and Rice, S (1988) Seed size variation: magnitude, distribution, and ecological correlates. Evolutionary Ecology 2, 157–166.CrossRefGoogle Scholar
Minter, TC and Lord, EM (1983) Effects of water stress, abscisic acid, and gibberellic acid on flower production and differentiation in the cleistogamous species Collomia grandiflora Dougl. ex Lindl. (Polemoniaceae). American Journal of Botany 70, 618–624.CrossRefGoogle Scholar
Munguía-Rosas, MA, Parra-Tabla, V, Ollerton, J and Cervera, JC (2012) Environmental control of reproductive phenology and the effect of pollen supplementation on resource allocation in the cleistogamous weed, Ruellia nudiflora (Acanthaceae). Annals of Botany 109, 343–350.CrossRefGoogle Scholar
Musselman, LJ (1982) The Orobanchaceae of Virginia. Castanea 47, 266–275.Google Scholar
Nave, M, Avni, R, Ben-Zvi, B, Hale, I and Distelfeld, A (2016) QTLs for uniform grain dimensions and germination selected during wheat domestication are co-located on chromosome 4B. Theoretical and Applied Genetics 129, 1303–1315.CrossRefGoogle ScholarPubMed
New, JK (1958) A population study of Spergula arvensis. I. Two clines and their significance. Annals of Botany 22, 457–477.CrossRefGoogle Scholar
New, JK (1959) A population study of Spergula arvensis. II. Genetics and breeding behaviour. Annals of Botany 23, 23–33.CrossRefGoogle Scholar
New, JK (1961) Biological flora of the British Isles. Spergula arvensis L. Journal of Ecology 49, 205–215.CrossRefGoogle Scholar
New, JK (1978) Change and stability of clines in Spergula arvensis L. (corn spurrey) after 20 years. Watsonia 12, 137–143.Google Scholar
New, JK and Herriott, JC (1981) Moisture for germination as a factor affecting the distribution of the seed coat morphs of Spergula arvensis L. Watsonia 13, 323–324.Google Scholar
Oakley, CG, Moriuchi, KS and Winn, AA (2007) The maintenance of outcrossing in predominantly selfing species: ideas and evidence from cleistogamous species. Annual Review of Ecology, Evolution and Systematics 38, 437–457.CrossRefGoogle Scholar
Orth, RJ, Harwell, MC and Inglis, GJ (2006) Ecology of seagrass seeds and seagrass dispersal processes, pp. 111–133 in Larkum, AWD; Orth, RJ; Duarte, CM (Eds) Seagrasses: Biology, Ecology and Conservation, Dordrecht, Springer.Google Scholar
Ortiz, PL, Berjano, R, Talavera, M and Arista, M (2009) The role of resources and architecture in modeling floral variability for the monoecious amphicarpic Emex spinosa (Polygonaceae). American Journal of Botany 96, 2062–2073.CrossRefGoogle ScholarPubMed
Payne, AM and Maun, MA (1981) Dispersal and floating ability of dimorphic fruit segments of Cakile edentula var. lacustris. Canadian Journal of Botany 59, 2595–2602.CrossRefGoogle Scholar
Pitelka, LF, Thayer, ME and Hansen, SB (1983) Variation in achene weight in Aster acuminatus. Canadian Journal of Botany 61, 1415–1420.CrossRefGoogle Scholar
Redbo-Torstensson, P (1994) Variation in plastic response to a salinity gradient within a population of the halophytic plant Spergularia marina. Oikos 70, 349–358.CrossRefGoogle Scholar
Redbo-Torstensson, P and Telenius, A (1995) Primary and secondary seed dispersal by wind and water in Spergularia salina. Ecography 18, 230–237.CrossRefGoogle Scholar
Richards, AJ (1975) The inheritance and behavior of the rayed gene complex in Senecio vulgaris. Heredity 34, 95–104.CrossRefGoogle Scholar
Robinson, D, Bogdanova, T, Cohen, O and Gruntman, M (2023) Trade-off between dispersal traits in a heterocarpic plant across its invasive route. American Journal of Botany 110, e16192.CrossRefGoogle Scholar
Rodman, JE (1974) Systematics and evolution of the genus Cakile (Cruciferae). Contributions from the Gray Herbarium 205, 3–146.CrossRefGoogle Scholar
Ruban, AS and Badaeva, ED (2018) Evolution of the S-genomes in Triticum-Aegilops alliance: evidences from chromosome analysis. Frontiers in Plant Science 9, 1756.CrossRefGoogle ScholarPubMed
Ruiz de Clavijo, E (1994) Heterocarpy and seed polymorphism in Ceratocapnos heterocarpa (Fumariaceae). International Journal of Plant Sciences 155, 196–202.CrossRefGoogle Scholar
Ruiz de Clavijo, E (1995) The ecological significance of fruit heteromorphism in the amphicarpic species Catananche lutea (Asteraceae). International Journal of Plant Sciences 156, 824–833.CrossRefGoogle Scholar
Ruiz de Clavijo, E and Jiménez, MJ (1998) The influence of achene type and plant density on growth and biomass allocation in the heterocarpic annual Catananche lutea (Asteraceae). International Journal of Plant Sciences 159, 637–647.CrossRefGoogle Scholar
Salisbury, EJ (1958) Spergularia salina and Spergularia marginata and their heteromorphic seeds. Kew Bulletin 1, 41–51.CrossRefGoogle Scholar
Schat, H (1981) Seed polymorphism and germination ecology of Plantago coronopus L. Acta Oecologica 2, 367–380.Google Scholar
Scholl, JP, Calle, L, Miller, N and Venable, DL (2020) Offspring polymorphism and bet hedging: a large-scale, phylogenetic analysis. Ecology Letters 23, 1223–1231.CrossRefGoogle ScholarPubMed
Schrenk, H (1894) Parasitism of Epiphegus [Epifagus] virginiana. Proceedings of the American Microscopical Society 15, 91–127. Sixteenth Annual Meeting. Part II (January 1894), pp. 91-127 + plates I-X.CrossRefGoogle Scholar
Smith, BW (1950) Arachis hypogaea. Aerial flower and subterranean fruit. American Journal of Botany 37, 802–815.CrossRefGoogle Scholar
Smith, M, Ammann, S, Parker, N and Mettler-Cherry, P (2006) A quantitative study of styles and achenes of terminal and basal flowers of Schoenoplectus hallii (Cyperaceae), a rare plant species of transient wetland habitats. Sida 22, 1159–1173.Google Scholar
Stanton, ML (1984) Developmental and genetic sources of seed weight variation in Raphanus raphanistrum L. (Brassicaceae). American Journal of Botany 71, 1090–1098.CrossRefGoogle Scholar
Sterk, AA (1969a) Biosystematic studies of Spergularia media and S. marina in The Netherlands I. The morphological variability of S. media. Acta Botanica Neerlandica 18, 325–338.CrossRefGoogle Scholar
Sterk, AA (1969b) Biosystematic studies of Spergularia media and S. marina in The Netherlands II. The morphological variation of S. marina. Acta Botanica Neerlandica 18, 467–476.CrossRefGoogle Scholar
Sterk, AA (1969c) Biosystematic studies of Spergularia media and S. marina in The Netherlands III. The variability of S. media and S. marina in relation to the environment. Acta Botanica Neerlandica 18, 561–577.CrossRefGoogle Scholar
Sterk, AA (1969d) Biosystematic studies of Spergularia media and S. marina in The Netherlands IV. Reproduction, dissemination, karyogenetics and taxonomy. Acta Botanical Neerlandica 18, 639–650.CrossRefGoogle Scholar
Sterk, AA and Dijkhuizen, L (1972) The relation between the genetic determination and the ecological significance of the seed wing in Spergularia media and S. marina. Acta Botanica Neerlandica 21, 481–490.CrossRefGoogle Scholar
Suetsuga, K (2013) Gastrodia takeshimensis (Orchidaceae), a new mycoheterotrophic species from Japan. Annales Botanici Fennici 50, 375–378.CrossRefGoogle Scholar
Suetsuga, K (2014) Gastrodia flexistyloides (Orchidaceae), a new mycoheterotrophic plant with complete cleistogamy from Japan. Phytotaxa 175, 270–274.CrossRefGoogle Scholar
Suetsuga, K (2016) Gastrodia kuroshimensis (Orchidaceae: Epidendroideae: Gastrodieae), a new mycoheterotrophic and complete cleistogamous plant from Japan. Phytotaxa 278, 265–272.CrossRefGoogle Scholar
Sun, M (1999) Cleistogamy in Scutellaria indica (Labiatae): effective mating system and population genetic structure. Molecular Ecology 8, 1285–1295.CrossRefGoogle ScholarPubMed
Sun, HZ, Lu, JJ, Tan, DY, Baskin, JM and Baskin, CC (2009) Dormancy and germination characteristics of the trimorphic achenes of Garhadiolus papposus (Asteraceae), an annual ephemeral from the Junggar Desert, China. South African Journal of Botany 75, 537–545.CrossRefGoogle Scholar
Susko, DJ and Lovett-Doust, L (2000) Patterns of seed mass variation and their effects on seedling traits in Alliaria petiolata (Brassicaceae). American Journal of Botany 87, 56–66.CrossRefGoogle ScholarPubMed
Talavera, M, Arista, M and Ortiz, PL (2012) Evolution of dispersal traits in a biogeographical context: a study using the heterocarpic Rumex bucephalophorus as a model. Journal of Ecology 100, 1194–1203.CrossRefGoogle Scholar
Talavera, M, Ortiz, PL, Arista, M, Berjano, R and Imbert, E (2010) Disentangling sources of maternal effects in the heterocarpic species Rumex bucephalophorus. Perspectives in Plant Ecology, Evolution and Systematics 12, 295–304.CrossRefGoogle Scholar
Talavera, M, Balao, F, Casimiro-Soriguer, R, Ortiz, MÁ, Terrab, A, Arista, M, Ortiz, PL, Stuessy, TF and Talavera, S (2011) Molecular phylogeny and systematics of the highly polymorphic Rumex bucephalophorus complex (Polygonaceae). Molecular Phylogenetics and Evolution 61, 659–670.CrossRefGoogle ScholarPubMed
Telenius, A (1992) Seed heteromorphism in a population of Spergularia media in relation to the ambient vegetation density. Acta Botanical Neerlandica 41, 305–318.CrossRefGoogle Scholar
Telenius, A and Torstensson, P (1989) The seed dimorphism of Spergularia marina in relation to dispersal by wind and water. Oecologia 80, 206–210.CrossRefGoogle ScholarPubMed
Telenius, A and Torstensson, P (1991) Seed wings in relation to seed size in the genus Spergularia. Oikos 61, 216–222.CrossRefGoogle Scholar
Telenius, A and Torstensson, P (1999) Seed type and seed size variation in the heteromorphic saltmarsh annual Spergularia salina along the coast of Sweden. Plant Biology 1, 585–593.CrossRefGoogle Scholar
Thieret, JW (1969) Notes on Epifagus. Castanea 34, 397–402.Google Scholar
Thieret, JW (1971) The genera of Orobanchaceae in the southeastern United States. Journal of the Arnold Arboretum 52, 404–434.CrossRefGoogle Scholar
Thompson, PA (1981) Variations in seed size within populations of Silene dioica (L.) Clairv. in relation to habitat. Annals of Botany 47, 623–634.CrossRefGoogle Scholar
Thompson, JN (1984) Variation among individual seed masses in Lomatium grayi (Umbelliferae) under controlled conditions: magnitude and partitioning of the variance. Ecology 65, 626–631.CrossRefGoogle Scholar
Toorop, PE, Cuerva, RC, Begg, GS, Locardi, B, Squire, GR and Iannetta, PPM (2012) Co-adaptation of seed dormancy and flowering time in the arable weed Capsella bursa-pastoris (shepherd's purse). Annals of Botany 109, 481–489.CrossRefGoogle ScholarPubMed
Trow, AH (1912) On the inheritance of certain characters in the common groundsel – Senecio vulgaris, Linn. – and its segregates. Journal of Genetics 2, 239–276.CrossRefGoogle Scholar
Uphof, JCT (1938) Cleistogamic flowers. The Botanical Review 4, 21–49.CrossRefGoogle Scholar
van der Pijl, L (1982) Principles of dispersal in higher plants. Third revised and expanded edition. Berlin, Springer.CrossRefGoogle Scholar
Venable, DL (1985) The evolutionary ecology of seed heteromorphism. The American Naturalist 126, 577–595.CrossRefGoogle Scholar
Venable, DL and Búrquez, A (1989) Quantitative genetics of size, shape, life-history, and fruit characteristics of the seed-heteromorphic composite Heterosperma pinnatum. I. Variation within and among populations. Evolution 43, 113–124.Google ScholarPubMed
Venable, DL, Dyreson, E and Morales, E (1995) Population dynamic consequences and evolution of seed traits of Heterosperma pinnatum (Asteraceae). American Journal of Botany 82, 410–420.CrossRefGoogle Scholar
Venable, DL, Búrquez, A, Corral, G, Morales, E and Espinosa, F (1987) The ecology of seed heteromorphism in Heterosperma pinnatum in central Mexico. Ecology 68, 65–76.CrossRefGoogle Scholar
Volis, S (2016) Seed heteromorphism in Triticum dicoccoides: association between seed positions within a dispersal unit and dormancy. Oecologia 181, 401–412.CrossRefGoogle ScholarPubMed
Wagner, LK (1986) Variation in seed-coat morph ratios in Spergula arvensis L. Bulletin of the Torrey Botanical Club 113, 28–35.CrossRefGoogle Scholar
Wagner, LK (1988) Germination and seedling emergence in Spergula arvensis. American Journal of Botany 75, 465–475.CrossRefGoogle Scholar
Waisel, Y and Adler, Y (1959) Germination behavior of Aegilops kotschyi Boiss. Canadian Journal of Botany 37, 741–742.CrossRefGoogle Scholar
Walck, JL and Hidayati, SN (2007) Ombrohydrochory and its relationship to seed dispersal and germination strategies in two temperate North American Oenothera species (Onagraceae). International Journal of Plant Sciences 168, 1279–1290.CrossRefGoogle Scholar
Wang, H and Wei, Y (2007) Seed polymorphism and fruit-set of Salsola affinis. Biodiversity Science 15, 419–424. (in Chinese with English abstract)Google Scholar
Wang, L, Huang, Z, Baskin, CC, Baskin, JM and Dong, M (2008) Germination of dimorphic seeds of the desert annual halophyte Suaeda aralocaspica (Chenopodiaceae), a C4 plant without Kranz anatomy. Annals of Botany 102, 757–769.CrossRefGoogle ScholarPubMed
Wang, AB, Tan, DY, Baskin, CC and Baskin, JM (2010) Effect of seed position in spikelet on life history of Eremopyrum distans (Poaceae) from the cold desert of northwest China. Annals of Botany 106, 95–105.CrossRefGoogle Scholar
Wang, Z, Baskin, JM, Baskin, CC, Yang, X, Liu, G, Ye, X, Huang, Z and Cornelissen, JHC (2021) Great granny still ruling from the grave: phenotypic response of plant performance and seed functional traits to salt stress affects multiple generations of a halophyte. Journal of Ecology 110, 117–128.CrossRefGoogle Scholar
Wang, AB, Baskin, CC, Baskin, JM and Ding, J (2022) Seed position in spikelet as a contributing factor to the success of the winter annal invasive grass Aegilops tauschii. Frontiers in Plant Science 13, 91651.Google Scholar
Wang, AB, Baskin, CC, Baskin, JM and Ding, J (2023) Trade-offs between diaspore dispersal and dormancy within a spike of the invasive annual grass Aegilops tauschii. Planta 257, 121.CrossRefGoogle ScholarPubMed
Warcup, JH (1985) Rhizanthella gardneri (Orchidaceae), its Rhizoctonia endophyte and close association with Melaleuca uncinata (Myrtaceae) in western Australia. New Phytologist 99, 273–280.CrossRefGoogle Scholar
Wareing, PF and Foda, HA (1957) Growth inhibition and dormancy in Xanthium seed. Physiologia Plantarum 10, 266–280.CrossRefGoogle Scholar
Wilken, DH (1982) The balance between chasmogamy and cleistogamy in Collomia grandiflora (Polemoniaceae). American Journal of Botany 69, 1326–1333.CrossRefGoogle Scholar
Winn, AA (1991) Proximate and ultimate sources of within-individual variation in seed mass in Prunella vulgaris (Lamiaceae). American Journal of Botany 78, 838–844.Google Scholar
Wolf, LL, Hainsworth, FR, Mercier, T and Benjamin, R (1986) Seed size variation and pollinator uncertainty in Ipomopsis aggregata (Polemoniaceae). Journal of Ecology 74, 361–371.CrossRefGoogle Scholar
Wulff, RD (1986) Seed size variation in Desmodium paniculatum. I. Factors affecting seed size. Journal of Ecology 74, 87–97.CrossRefGoogle Scholar
Wurzburger, J and Leshem, Y (1967) Gibberellin and hull controlled inhibition of germination in Aegilops kotschyi Boiss. Israel Journal of Botany 16, 181–186.Google Scholar
Wurzburger, J and Koller, D (1976) Differential effects of the parental photothermal environment on development of dormancy in caryopses of Aegilops koschyi. Journal of Experimental Botany 27, 43–48.CrossRefGoogle Scholar
Wurzburger, J, Leshem, Y and Koller, D (1974) The role of gibberellin and the hulls in the control of germination in Aegilops kotschyi caryopses. Canadian Journal of Botany 52, 1597–1601.CrossRefGoogle Scholar
Yang, F, Baskin, JM, Baskin, CC, Yang, X, Cao, D and Huang, Z (2015a) Effects of germination time on seed morph ratio in a seed-dimorphic species and possible ecological significance. Annals of Botany 115, 137–145.CrossRefGoogle Scholar
Yang, F, Yang, X, Baskin, JM, Baskin, CC, Cao, D and Huang, Z (2015b) Transgenerational plasticity provides diversity for a seed heteromorphic species in response to environmental heterogeneity. Perspectives in Plant Ecology, Evolution and Systematics 17, 201–208.CrossRefGoogle Scholar
Zeide, B (1978) Reproductive behavior of plants in time. The American Naturalist 112, 636–639.CrossRefGoogle Scholar
Zhang, J (1994) Early seedling development in relation to seed mass and morph in Cakile edentula. Canadian Journal of Botany 72, 402–406.CrossRefGoogle Scholar
Zhang, K, Baskin, JM, Baskin, CC, Yang, X and Huang, Z (2017) Effect of seed morph and light level on growth and reproduction of the amphicarpic plant Amphicarpaea edgeworthii (Fabaceae). Scienific Reports 7, 39886.CrossRefGoogle ScholarPubMed
Zhang, K, Baskin, JM, Baskin, CC, Cheplick, G, Yang, X and Huang, Z (2020) Amphicarpic plants: definition, ecology, geographic distribution, systematics, life history, evolution and use in agriculture. Biological Reviews 95, 1442–1466.CrossRefGoogle ScholarPubMed
Zohary, M (1937) Die verbreitungsökologischen Verhältnisse der Pflanzen Palästinas. I. Die antitelochorischen Erscheinungen. Beihefte zum Botanischen Zentralblatt 56, 1–55.Google Scholar
Zohary, M (1962) Plant life of Palestine: Israel and Jordan. New York, Ronald Press.Google Scholar
Zohary, M and Fahn, A (1950) On the heterocarpy of Aethionema. Palestine Journal of Botany 5, 28–31.Google Scholar
Zohary, M and Imber, D (1963) Genetic dimorphism in fruit types in Aegilops speltoides. Heredity 18, 223–231.CrossRefGoogle Scholar
Figure 0

Table 1. A classification system for monomorphic and heteromorphic diaspores in angiosperms based on size/mass, morphology and position on mother plant.