The dispersal/germination unit

The dispersal unit of Asteraceae is a single-seeded cypsela (Gleason and Cronquist, Reference Gleason and Cronquist1991), except it is reported to be a drupe in Chrysanthemoides monilifera subsp. monilifera from South America (Reynolds et al., Reference Reynolds, Long, Flematti, Cherry and Turner2013). However, the dispersal unit of Asteraceae is often referred to as an achene, which is not botanically correct. A cypsela is a dry indehiscent fruit originating from an inferior ovary with two carpels and one locule that produces only one seed. In contrast, an achene is a single-seeded dry indehiscent fruit that originates from a superior ovary (Marzinek et al., Reference Marzinek, De-Paula and Oliveira2008). In this paper, we use only ‘cypsela’. The pericarp of Asteraceae cypselae is not adnate to the seed (Frangiote-Pallone and Souza, Reference Frangiote-Pallone and Souza2014), and it is water permeable (e.g. Kagaya et al., Reference Kagaya, Tani and Kachi2005; Genna and Pérez, Reference Genna and Pérez2016; Yuan and Wen, Reference Yuan and Wen2018; Sarmento et al., Reference Sarmento, Pereira, Oliveira, Leal, Torres and Dutra2019; Zhang et al., Reference Zhang, Yao, Zhang and Tao2019). Furthermore, the large well-developed embryo is spatulate in shape, and endosperm is not present in mature cypselae (Martin, Reference Martin1946; Lubbock, Reference Lubbock1892[1978]). In the Baskin and Baskin (Reference Baskin and Baskin2014) classification scheme for variation in position, size, mass and morphology of plant diaspores on individual plants, most Asteraceae fit under Division I. Monomorphic (but see below). Furthermore, diaspores fit under Group A (diaspores are produced only from chasmogamous flowers) of Supergroup 1 (Monomorphic aerial). However, Asteriscus pygmaeus and Arctotheca populifolia fit under Supergroup 2 (Monomorphic basal or subterranean). More specifically A. pygmaeus fits under Group A (Basicarpy) and A. populifolia under Group B (Geocarpy. Subgroup e. Passive geocarpy).

Cypselae of Asteraceae are desiccation-tolerant and thus have orthodox storage behaviour (Dickie and Pritchard, Reference Dickie, Pritchard, Black and Pritchard2002). Hong et al. (Reference Hong, Linington and Ellis1998) list 434 species of Asteraceae: 377 with orthodox cypselae, 55 probable orthodox? and 2 undecided. In their global list of species whose seeds are recalcitrant (desiccation-sensitive), Subbiah et al. (Reference Subbiah, Ramdhani, Pammenter, Macdonald and Sershen2019) do not list any species of Asteraceae. According to Pence et al. (Reference Pence, Bruns, Meyer, Pritchard, Westwood, Linsky, Gratzfeld, Helm-Wallace, Liu, Rivers and Beech2022) ‘exceptional species’ in terms of ex-situ seed storage for conservation may have seeds that are desiccation-sensitive, short-lived under conventional seed banking conditions or deeply dormant. However, these authors listed 187 species of Asteraceae as ‘non-exceptional’ and 151 species of this family as ‘probably non-exceptional’. Cypselae of 18 species in 10 genera of Asteraceae stored dry at −18°C for 24–26 years were predicted to have a P ₅₀ (number of years before 50% of the cypselae lose viability) of 13 (Guizotia abyssinica) to 124 (Zinnia sp.) years (Walters et al., Reference Walters, Wheeler and Grotenhuis2005).

Venable and Levin (Reference Venable and Levin1983) surveyed published floras from Asia, Australia, Africa, North America, Pacific Islands and South America for information on dispersal-related structures on cypselae of Asteraceae. They recorded information for 5893 species, including annuals, biennials, perennials, shrubs and trees, and 71.0, 87.6, 81.2, 86.2 and 83.0%, respectively, had structures on the cypselae that would facilitate dispersal. In all life forms, the rank order of dispersal-facilitating structures was plumes > barb-like > scales, except for annuals in which it was plumes > scales > barb-like structures.

Capitula and breeding systems

A capitulum may consist of both disc and ray flowers, only disc flowers or only ray flowers. A disc flower has three to five corolla lobes, depending on the species, and is actinomorphic, while the corolla lobes of a ray flower are fused into a single strap-shaped (ligulate) structure that is zygomorphic (Jeffrey, Reference Jeffrey, Heywood, Harborne and Turner1977; Leppik, Reference Leppik, Heywood, Harborne and Turner1977; Bremer, Reference Bremer1994). Various types of capitula (and breeding systems) can be distinguished in Asteraceae (Jeffrey, Reference Jeffrey, Funk, Susanna, Stuessy and Bayer2009; Elomaa et al., Reference Elomaa, Zhao and Zhang2018): (1) both disc and ray flowers are perfect (monocliny), for example, Cotula spp. (Lloyd, Reference Lloyd1972a); (2) disc perfect and ray pistillate (gynomonoecy), for example, Aster s.l. (Bertin and Kerwin, Reference Bertin and Kerwin1998) and Solidago (Bertin and Gwisc, Reference Bertin and Gwisc2002); (3) disc staminate and ray pistillate (monoecy), for example, Lecocarpus pinnatifidus (Philipp et al., Reference Philipp, Hansen, Adsersen and Siegismund2004); (4) disc perfect and ray sterile, for example, Helianthus annuus (Elomaa et al., Reference Elomaa, Zhao and Zhang2018) and (5) rarely androdioecy with some perfect flowers and some that are functionally staminate.

Some species of Asteraceae produce two kinds of capitula (Jeffrey, Reference Jeffrey, Funk, Susanna, Stuessy and Bayer2009): (1) pistillate and staminate capitula on different plants (dioecy); (2) pistillate and perfect capitula on different plants (gynodioecy), for example, Bidens sandvicensis (Schultz and Ganders, Reference Schultz and Ganders1996) and Cirsium arvense (Lloyd and Myall, Reference Lloyd and Mayall1976; Kay, Reference Kay1985); (3) perfect and staminate capitula on different plants (androdioecy); and (4) pistillate and staminate capitula on the same plant (monoecy). It should be noted that in some sexually dimorphic plant species, the strictness of malenesss and/or femaleness in individuals in a population may be constant [invariable (strictly unisexual) sexual expression] or inconstant (continuously variable) sex expression, with inconstant males being more common than inconstant females (Lloyd, Reference Lloyd1976; Webb, Reference Webb, Geber, Dawson and Delph1999). Examples of inconstant males and females in sex expression in the Asteraceae include dioecious species of Cotula (Lloyd, Reference Lloyd1972b, Reference Lloyd1975). Also, see Yampolsky and Yampolsky (Reference Yampolsky and Yampolsky1922) and Renner (Reference Renner2014) for information on kinds of sexual systems in Asteraceae.

Species of Asteraceae may be self-incompatible (SI) (Hiscock, Reference Hiscock2000; Stephens, Reference Stephens2008; Allen et al., Reference Allen, Thorogood, Hegarty, Lexer and Hiscock2011), self-compatible (SC) (Carr et al., Reference Carr, Powell and Kyhos1986; Grombone-Guaratini et al., Reference Grombone-Guaratini, Solferini and Semir2004; Picó et al., Reference Picó, Ouborg and van Groenendael2004; Soto-Trejo et al., Reference Soto-Trejo, Kelly, Archibald, Mort, Santos-Guerra and Crawford2013) or partially self-incompatible (PSI) (Ortiz et al., Reference Ortiz, Talavera, García-Castaño, Tremetsberger, Stuessy, Balao and Casimiro-Soriguer2006; Nielsen et al., Reference Nielsen, Siegismund and Hansen2007). Furthermore, populations of some Asteraceae have a mixture of breeding systems (Sun and Ganders, Reference Sun and Ganders1988; Arista et al., Reference Arista, Berjano, Viruel, Ortiz, Talavera and Ortiz2017). In a survey of the breeding system in 571 taxa of Asteraceae, Ferrer and Good-Avila (Reference Ferrer and Good-Avila2007) found that 65, 10 and 25% of the taxa had SI, PSI and SC, respectively. These authors were not able to resolve the ancestral kind of breeding system in Asteraceae, but they did find that SI can be gained and lost. Thus, neither SC nor PSI is a ‘terminal state’. Not surprisingly, a relatively higher percentage of SC than of SI has been found for invasive species of Asteraceae, for example, in China (Hao et al., Reference Hao, Qiang, Chrobock, van Kleunen and Liu2011) and for species on islands (Grossenbacher et al., Reference Grossenbacher, Brandvain, Auld, Burd, Cheptou, Conner, Grant, Hovick, Pannell, Pauw, Petanidou, Randle, Rubio de Casas, Vamosi, Winn, Igic, Busch, Kalisz and Goldberg2017). The latter authors found that 143 of 519 (28.0%) of mainland Asteraceae species had SC, while 162 of 273 (59.3%) of island species had SC.

Some species of Asteraceae produce a low number of cypselae due to a lack of compatible pollen being deposited on the stigma (i.e. pollen limitation); this is especially important for some SI species (Larson and Barrett, Reference Larson and Barrett2000). Pollen limitation has been documented in various Asteraceae species (Totland, Reference Totland1997; Colling et al., Reference Colling, Reckinger and Matthies2004; Muñoz and Arroyo, Reference Muñoz and Arroyo2006; Campbell and Husband, Reference Campbell and Husband2007; Muñoz and Cavieres, Reference Muñoz and Cavieres2008; Ferrer et al., Reference Ferrer, Good-Avila, Montaña, Domínguez and Eguiarte2009; Law et al., Reference Law, Salick and Knight2010; Shabir et al., Reference Shabir, Nawchoo, Wani and Banday2015). In general, pollen limitation decreases cypsela production, and in Scorzonera humilis, it reduces the germination percentage of the cypselae that were produced. In the SI species Achillea ptarmica, there was a significant relationship between pollen viability and the seed/ovule ratio, but ovule abortion did not result in offspring with increased vigour, suggesting that genetic load results in female sterility (Andersson, Reference Andersson1993). The fruit set ratio (number of cypselae/number of female flowers), a measure of female reproductive success, ranged from 0.242 to 0.630 for monoecious and dioecious species of Cotula, respectively (Sutherland, Reference Sutherland1986).

It is well documented that the maternal parent has more influence on seed dormancy/germination than the paternal parent, and this is especially true in the F₁ (seed) progeny. However, the father sometimes has an effect on variation in these traits (Baskin and Baskin, Reference Baskin and Baskin2019). The paternal parent had a positive influence on germination percentage and/or rate for Aster kantoensis (Kagaya et al., Reference Kagaya, Tani and Kachi2011), Crepis tectorum subsp. pumila (Andersson, Reference Andersson1990), Lactuca sativa (Rideau et al., Reference Rideau, Monin, Dommergues and Cornu1976) and Solidago altissima (Schmid and Dolt, Reference Schmid and Dolt1994).

Breeding between closely related organisms may result in the expression of recessive deleterious genes (if purging has not occurred) that have negative effects on the offspring, that is, inbreeding depression (ID). The negative effects of ID on plants may include seed germination (Baskin and Baskin, Reference Baskin and Baskin2015). In the Asteraceae, ID for cypsela germination has been found in several species including Acourtia runcinata (Cabrera and Dieringer, Reference Cabrera and Dieringer1992), Cotula minor (Lloyd, Reference Lloyd1972b) Crepis sancta (Cheptou et al., Reference Cheptou, Lepart and Escarré2001), Fluorensia cernua (Ferrer et al., Reference Ferrer, Good-Avila, Montaña, Domínguez and Eguiarte2009), Hypochaeris radicata (Becker et al., Reference Becker, Colling, Dostal, Jakobsson and Matthies2006), Leontodon autumnalis (Picó and Koubek, Reference Picó and Koubek2003), Olearia adenocarpa (Heenan et al., Reference Heenan, Smissen and Dawson2005), Scorzonera humilis (Colling et al., Reference Colling, Reckinger and Matthies2004), Scalesia affinis (Nielsen et al., Reference Nielsen, Siegismund and Hansen2007), Senecio integrifolius (Widén, Reference Widén1993) and S. pterophorus (Caño et al., Reference Caño, Escarré, Blanco-Moreno and Sans2008). However, inbreeding and outbreeding did not result in significant differences in germination of Arnica montana (Luijten et al., Reference Luijten, Oostermeijer, van Leeuwen and den Nijs1996), Aster amellus (Raabová et al., Reference Raabová, Münzbergová and Fischer2009), Carduus pycnocephalus, C. defloratus subsp. glaucus (Olivieri et al., Reference Olivieri, Swan and Gouyon1983), Crepis sancta (Cheptou et al., Reference Cheptou, Imbert, Lepart and Escarré2000), Eupatorium resinosum (Byers, Reference Byers1998), Gaillardia pulchella (Heywood, Reference Heywood1993), Senecio squalidus (Brennan et al., Reference Brennan, Harris and Hiscock2005), Tetraneuris herbacea (Moran-Palma and Snow, Reference Moran-Palma and Snow1997) or Tragopogon pratensis (Picó et al., Reference Picó, Ouborg and van Groenendael2003). In Cotula pectinata (Lloyd, Reference Lloyd1972b) and Eupatorium perfoliatum (Byers, Reference Byers1998), outbreeding led to a decrease in germination. Although Helianthus verticillatus is a rare diploid SI perennial known from only four locations in southeastern USA, Ellis and McCauley (Reference Ellis and McCauley2009) did not find any evidence for outbreeding depression for germination percentages of F₁ or F₂ cypselae from interpopulation crosses.

As an extension of the concern about effects of ID on germination of cypselae, attention has been given to germination of cypselae produced by Asteraceae species growing in small versus large populations. That is, do small populations have ID that could decrease germination? Germination percentages were significantly lower for cypselae produced in small than in large populations of Arnica montana in Germany (Kahmen and Poschlod, Reference Kahmen and Poschlod2000), Cheirolophus uliginosus (Vitales et al., Reference Vitales, Pellicer, Vallés and Garnatje2013), Centaurea jacea, Cirsium dissectum, Hypochaeris radicata (Soons and Heil, Reference Soons and Heil2002), Lamyropsis microcephala (Mattana et al., Reference Mattana, Fenu and Bacchetta2012), Senecio paludosus (Winter et al., Reference Winter, Lehmann and Diekmann2008) and Solidago albopilosa (Albrecht et al., Reference Albrecht, Dell and Long2020). On the other hand, the size of population was not significantly related to germination percentages for cypselae of Arnica montana in The Netherlands (Luijten et al., Reference Luijten, Dierick, Gerard, Oostermeijer, Raijmann and den Nijs2000), Carduus defloratus (Vaupel and Matthies, Reference Vaupel and Matthies2012), Cirsium dissectum (de Vere et al., Reference de Vere, Jongejans, Plowman and Williams2009), Leucochrysum albicans var. tricolor (Costin et al., Reference Costin, Morgan and Young2001), Rutidosis leptorrhynchoides (Morgan, Reference Morgan1999) and Tragopogon pratensis (Mölken et al., Reference Mölken, Jorritsma-Wienk, van Hoek and de Kroon2005). However, in a later paper, Morgan et al. (Reference Morgan, Meyer and Young2013) concluded that there was a significant positive relationship between population size and mean percentage of cypsela germination for R. leptorrhynchoides.

Kinds of dormancy in Asteraceae

Breaking dormancy in cypselae of Asteraceae

Types of non-deep physiological dormancy in Asteraceae

Six types of non-deep PD have been distinguished based on temperature requirements for seed germination as dormancy-break occurs (Baskin and Baskin, Reference Baskin and Baskin2014, Reference Baskin and Baskin2021; Nur et al., Reference Nur, Baskin, Lu, Tan and Baskin2014; see Figure 3 in Soltani et al., Reference Soltani, Baskin and Baskin2017). In Types 1, 2 and 3, the temperature range over which seeds will germinate widens during dormancy-break. In Type 1, the maximum temperature at which seeds can germinate increases, and in Type 2, the minimum temperature at which seeds can germinate decreases. In Type 3, the maximum temperature for germination increases and the minimum temperate decreases. In Types 4, 5 and 6, the temperature range for germination does not widen during dormancy-break. Seeds with Type 4 gain the ability to germinate only at high temperatures, and those with Type 5 gain the ability to germinate only at low temperatures. Seeds with Type 6 germinate to low percentages over a range of low to high temperatures in the early stages of dormancy-break, and the germination percentage increases at all temperatures as dormancy-break progresses. In addition to changes in the temperature range for germination during dormancy-break of seeds, particularly those with Types 1 and 2 non-deep PD, there is a gradual increase in germination rate (speed) and synchrony and in sensitivity to germination-promoting factors such as GA and light. Furthermore, like temperatures, sensitivity to these factors decreases as ND seeds are induced into secondary dormancy [see Table 4.3 in Baskin and Baskin (Reference Baskin and Baskin2014) and Maleki et al. (Reference Maleki, Baskin, Baskin, Kiani, Alahdadi and Soltani2022)].

Information about the type of non-deep PD in cypselae of Asteraceae is available for 103 species in 75 genera and 18 tribes (Table 1). Types 1, 2, 3, 4, 5 and 6 occur in 10, 13, 7, 3, 3 and 7 tribes of Asteraceae, respectively. The Heliantheae has the most types (1, 2, 3, 4 and 6). Five genera (one genus in each of five tribes) have species with two or three types, and Silybum mariarum has two types (1 and 6) (Monemizadeh et al., Reference Monemizadeh, Ghaderi-Far, Sadeghipour, Siahmarguee, Soltani, Torabi and Baskin2021). The information for types of non-deep PD in tribes of Asteraceae was plotted on the tribe-level phylogeny of Mandel et al. (Reference Mandel, Dikow, Siniscalchi, Thapa, Watson and Funk2019) (supplementary Fig. S1). No clear pattern about relationships between types and tribes was revealed, except that the occurrence of Types 1 and 2 or of Types 1, 2 and 3 in a tribe is fairly common. When plotted on the figure showing the proposed evolutionary history of Asteraceae by Huang et al. (Reference Huang, Zhang, Liu, Hu, Gao, Qi and Ma2016), types of non-deep PD occurred from the Mutisieae to the Heliantheae Alliance (supplementary Fig. S2). Although information about the types of non-deep PD in Asteraceae is rather limited in terms of the number of species studied in detail, the results provide some insight into the great flexibility of cypsela dormancy and germination in the Asteraceae in relation to plant life cycle and environmental conditions in the habitat.

Table 1.

Types (1–6) of non-deep physiological dormancy in Asteraceae species

^a Arguably, this could be Type 6 because fresh cypselae germinated over the entire range of test temperatures, although to a very low percentage at 15/5°C (the lowest test temperature regime).

In temperate regions with generally hot and relatively dry summers and cold moist winters, Type 1 is found in cypselae of winter annual (Baskin et al., Reference Baskin, Baskin and Van Auken1995b; Schütz et al., Reference Schütz and Milberg P2002) and some perennial (Baskin et al., Reference Baskin, Baskin and Van Auken1994) species of Asteraceae. High temperatures during summer promote dormancy-break, and by the time the soil is moist in autumn the maximum temperature at which cypselae can germinate overlaps with temperatures in the habitat. Type 2 occurs in summer annual and many perennial species of Asteraceae (Baskin and Baskin, Reference Baskin and Baskin1988; Baskin et al., Reference Baskin, Baskin and Leck1993, Reference Baskin, Baskin and Chester1995a, Reference Baskin, Baskin and Van Auken1998). Low temperatures and moist soil during winter promote dormancy-break, that is, lowering the minimum temperature at which cypselae can germinate, and germination usually occurs in early to mid-spring. Type 3 occurs in species of Asteraceae that behave as winter annuals (Baskin et al., Reference Baskin, Baskin and Chester1991, Reference Baskin, Baskin and Van Auken1992b) and as perennials (Baskin and Baskin, Reference Baskin and Baskin1988; Baskin et al., Reference Baskin, Baskin and Leck1993, Reference Baskin, Baskin and Van Auken1994, Reference Baskin, Baskin and Van Auken1998) with dormancy being broken in summer and winter, respectively.

Little is known about Type 4 non-deep PD, except that both dormancy-break and germination occur at relatively high temperatures. The four species of Asteraceae known to have Type 4 (Table 1) occur in hot deserts (two species of Pectis) or in relatively mesic tropical/subtropical areas (Tridax procumbens and Synedrella nodifolia). In a habitat that is warm all year, it is assumed that timing of onset of the wet season is a major factor in determining the timing of germination. However, much additional research is needed on the environmental conditions required for dormancy-break and germination of species of Asteraceae (and other families) growing in tropical/subtropical regions.

Type 5 non-deep PD has been reported in cypselae of Coespeletia timothensis, Filago california and Schoenia cassiniana (Table 1). The thing that these species have in common is that their cypselae germinate only at low temperatures. At high elevations in the Andes Mountains, it is reasonable that cypselae of C. timothensis would gain the ability to germinate only at low temperatures. However, for F. california and S. cassiniana that grow in habitats with a Mediterranean-type climate, a low temperature requirement for germination would delay germination until late in autumn when the soil is likely to be moist. That is, a delay of germination until temperatures are low helps ensure that there is enough soil moisture for seedling establishment and growth.

Nine species of Asteraceae are listed in Table 1 as having Type 6 non-deep PD, and they can be divided into two general categories depending on their habitat: (1) cold desert and (2) relatively moist temperate. In the cold desert, timing of rainfall is highly unpredictable. Thus, ability of cypselae to germinate over a wide range of temperatures as dormancy-break is occurring would allow at least some cypselae of the cold desert winter annuals Echinops gmelinii, Epilasia acrolasia and Koelipia linearis to germinate at any time during the growing season in response to a rainfall event or snowmelt in late winter/early spring (Nur et al., Reference Nur, Baskin, Lu, Tan and Baskin2014). In the case of Glebionis coronata in the Mediterranean region, Type 6 would allow cypselae to germinate regardless of whether the onset of the wet season began early or late in the autumn. The other five species with Type 6 grow in the regions of the deciduous forest in eastern North America, where there is no definite dry season. Presumably Type 6 would allow cypselae to germinate at any time during the growing season, but this has not been tested. However, cypselae of Boltonia decurrens (Baskin and Baskin, Reference Baskin and Baskin1988) and Polymnia canadensis (Bender et al., Reference Bender, Baskin and Baskin2003) exposed to natural temperature regimes germinate in both spring and autumn.

Intraspecific variation in dormancy

Not only is there species-to-species variation in dormancy in the Asteraceae due to different types of non-deep PD, but there may be variation in dormancy between the cypselae produced by the same species. For example, cypselae of various species of Asteraceae differed in their germination characteristic when collected in different populations (Schütz and Urbanska, Reference Schütz and Urbanska1984; Meyer et al., Reference Meyer, McArthur and Jorgensen1989, Reference Meyer, Monsen and McArthur1990; Ren and Abbott, Reference Ren and Abbott1991; Maluf, Reference Maluf1993; Martin et al., Reference Martin, Grzeskowiak and Puech1995; Keller and Kollmann, Reference Keller and Kollmann1999; Qaderi and Cavers, Reference Qaderi and Cavers2000a; Giménez-Benavides et al., Reference Giménez-Benavides, Escudero and Pérez-García2005; Bischoff et al., Reference Bischoff, Vonlanthen, Steinger and Muller-Schärer2006; Jorritsma-Wienk et al., Reference Jorritsma-Wienk, Ameloot, Lenssen and de Kroon2007; Li and Feng, Reference Li and Feng2009; Bischoff and Muller-Schärer, Reference Bischoff and Muller-Schärer2010; Bartle et al., Reference Bartle, Moles and Bonser2013; Torres-Martínez et al., Reference Torres-Martínez, Weldy, Levy and Emery2017; de Pedro et al., Reference de Pedro, Mayol and González-Martínez2021). However, the reason (genetic and/or maternal environmental effects) for population differences in dormancy was not determined in these studies.

Cypselae of the invasive Senecio madagascariensis from populations at the edge of its range in eastern Australia germinated to significantly higher percentages that those from populations in the established part of its range in eastern Australia (Bartle et al., Reference Bartle, Moles and Bonser2013). Simulation studies of cypselae germination and seedling survival of Artemisia tridentata under climate change conditions across its western North American range suggest that regeneration from cypselae will be higher at the leading (relatively moist) than at the trailing (relatively dry) edge of the range of distribution shift (Schlaepfer et al., Reference Schlaepfer, Taylor, Pennington, Nelson, Martyn, Rottler, Lauenroth and Bradford2015).

Cypsela dormancy in Asteraceae has a genetic component, for example, Helianthus bolanderi (Olivieri and Jain, Reference Olivieri and Jain1978), Lactuca sativa (Eenink, Reference Eenink1981) and Senecio vulgaris (Kadereit, Reference Kadereit1984). In particular, the genetics of cypsela dormancy have been investigated in detail for Helianthus annuus (Snow et al., Reference Snow, Moran-Palma, Rieseberg, Wszelaki and Seiler1998; Weiss et al., Reference Weiss, Primer, Pace and Mercer2013; Layat et al., Reference Layat, Leymarie, Maarouf-Bouteau, Caius, Langlade and Bailly2014; Lachabrouilli et al., Reference Lachabrouilli, Rigal, Corbineau and Bailly2021; Hernández et al., Reference Hernández, Vercellino, Pandolfa, Mandel and Presotto2022) and L. sativa (Argyris et al., Reference Argyris, Truco, Ochoa, McHale, Dahal, Van Deynze, Michelmore and Bradford2011; Huo et al., Reference Huo, Wei and Bradford2016). Inbred dormant and non-dormant lines of H. annuus exhibit differences in pericarp anatomy and hormone profiles (Andrade et al., Reference Andrade, Riera, Lindstrom, Alemano, Alvarez, Abdala and Vigliocoo2015). Also, the dormancy/germination characteristics of the mature cypselae can vary depending on the environmental conditions under which the maternal plant was growing during cypsela development, including day length (Gutterman et al., Reference Gutterman, Thomas and Heydecker1975), mineral nutrition (Thompson, Reference Thompson1937; Allison, Reference Allison2002), soil moisture (Qaderi and Cavers, Reference Qaderi and Cavers2000b) and temperature (Nosova, Reference Nosova1981; Zhang et al., Reference Zhang, Gallagher and Shea2012; Bodrone et al., Reference Bodrone, Rodríguez and Arisnabarreta2017). Furthermore, the maternal environment and genetics of the embryo can interact to influence cypsela dormancy (Weiss et al., Reference Weiss, Primer, Pace and Mercer2013), and there could be epigenetic (i.e. non-genetic transgenerational inheritance, e.g. Robertson and Richards, Reference Robertson and Richards2015; Skinner and Nilsson, Reference Skinner and Nilsson2021) control of dormancy via maternal inheritance, as in Arabidopsis thaliana (Iwasaki et al., Reference Iwasaki, Hyvärinen, Piskurewicz and Lopez-Molina2019).

In the case of Silybum marianum, populations vary with regard to the type of non-deep PD in the mature cypselae (Monemizadeh et al., Reference Monemizadeh, Ghaderi-Far, Sadeghipour, Siahmarguee, Soltani, Torabi and Baskin2021). Cypselae from plants of S. marianum growing at three population sites in northern Iran were allowed to afterripen in dry storage. Cypselae from two populations first gained the ability to germinate over a range of temperatures, indicating Type 6 non-deep PD. However, cypselae from the third population first germinated only at low temperatures but as afterripening continued the maximum temperature at which they germinated increased, indicating Type 1 non-deep PD. The cypselae with Type 6 developed under relatively dry, warm conditions and those with Type 1 developed during relatively wet, cool conditions. These results suggest that the maternal environment affected the type of non-deep PD that developed in the cypselae, but the effects of genetics and environment × genetics on the type of non-deep PD that developed in the cypselae in different populations have not been investigated.

Heteromorphic cypselae

According to Scholl et al. (Reference Scholl, Calle, Miller and Venable2020), heteromorphic diaspores differ in morphology and ecology, and the variation can be discrete or continuous, and if continuous the extreme diaspores differ greatly. In the classification scheme for variation in diaspore size/mass and morphology of Baskin and Baskin (Reference Baskin and Baskin2014, p. 341), Asteraceae species mentioned in this section fit into Subgroup a (Heterocarpy) of Group A (Heterodiaspory) of Division II (Heteromorphic). Diaspore heteromorphism occurs primarily in annual plants, and it is viewed as an adaptation (via a bet-hedging strategy) to unpredictable or disturbed environments (Mandák, Reference Mandák1997; Imbert, Reference Imbert2002; Cruz-Mazo et al., Reference Cruz-Mazo, Buide, Samuel and Narbona2009, Reference Cruz-Mazo, Narbona and Buide2010). The majority (ca. 80%) of heterodiasporous species occurs in three eudicot families: Asteraceae > Amaranthaceae > Brassicaceae (Mandák, Reference Mandák1997). The number of diaspore heteromorphic species of Asteraceae worldwide has not been determined, but in southwestern North America it is the family with the most diaspore heteromorphic species, that is, 64 species in 38 genera. The Boraginaceae is the second most important family with heteromorphic diaspores in this region with 23 species in 5 genera (Scholl et al., Reference Scholl, Calle, Miller and Venable2020).

Cypselae produced in the same capitulum of many species of Asteraceae vary in size, mass, colour, shape, ornamentation, presence/absence of pappus, thickness of pericarp, dispersal ability, presence/absence of dormancy and degree of non-deep PD (Baskin et al., Reference Baskin, Lu, Baskin and Tan2013; Baskin and Baskin, Reference Baskin and Baskin2014). Various dimorphic, and a few trimorphic, species of Asteraceae have been studied in detail. In general, peripheral cypselae are more dormant (higher degree of non-deep PD) than central cypselae, which are ND in some species; however, central cypselae can be more dormant than peripheral cypselae (Table 2). Cypselae that differ in degree of dormancy also can be produced by species with only ligulate (El-Keblawy, Reference El-Keblawy2003) or only ray (Olivieri et al., Reference Olivieri, Swan and Gouyon1983) flowers. Both the peripheral and central cypselae of Crepis sancta (Imbert et al., Reference Imbert, Escarré and Lepart1996) and Synedrella nodiflora (Souza Filho and Takaki, Reference Souza Filho and Takaki2011) have been reported to be ND.

Table 2.

Comparison of dormancy in examples of Asteraceae species with heteromorphic (dimorphic) cypselae

CA, central cypselae; ND, non-dormant; PA, peripheral cypselae.

Germination of trimorphic cypselae of Asteraceae has been studied in some detail for Calendula arvensis (Ruiz de Clavijo, Reference Ruiz de Clavijo2005), Garhadiolus papposus (Sun et al., Reference Sun, Lu, Tan, Baskin and Baskin2009), Heteracia szovitsii (Cheng and Tan, Reference Cheng and Tan2009; Lu et al., Reference Lu, Dong, Tan, Baskin and Baskin2020) and Heterosperma pinnatum (Venable et al., Reference Venable, Búrquez, Corral, Morales and Espinosa1987). Trimorphic cypselae have been reported for Xanthocephalum spp. (Lane, Reference Lane1983) and Chaptalia hieracioides (Xu et al., Reference Xu, Zheng, Funk and Wen2018), but their dormancy has not been studied. We note that some species of Chaptalia in Brazil (Pasini et al., Reference Pasini, Katinas and Ritter2014) and Mexico (Redonda-Martínez, Reference Redonda-Martínez2018) have trimorphic florets and presumably trimorphic cypselae. In G. papposus (Sun et al., Reference Sun, Lu, Tan, Baskin and Baskin2009), H. szovitsii (Lu et al., Reference Lu, Dong, Tan, Baskin and Baskin2020) and H. pinnatum (Venable et al., Reference Venable, Búrquez, Corral, Morales and Espinosa1987), the central cypselae are the least dormant and the peripheral cypselae the most dormant. Central, intermediate and peripheral cypselae of the cold desert annual H. szovitsii allowed to afterripen for 48 months germinated to 85% (30/15°C), 30.5% (5/2°C) and 10.5% (15/2°C), respectively. However, when the pericarp was removed from intermediate and peripheral cypselae they germinated to 100 and 69.3%, respectively (Lu et al., Reference Lu, Dong, Tan, Baskin and Baskin2020). Since seedlings derived from excised embryos of intermediate and peripheral cypselae produced normal plants and since afterripening, scarification/pericarp removal and GA₃ promoted germination of both kinds of cypselae (but more germination of intermediate than peripheral cypselae), it was concluded that intermediate and peripheral cypselae have intermediate PD. When central, intermediate and peripheral cypselae were sown outdoors in spring 2016, germination of central cypselae occurred in autumn 2016 and spring 2017; intermediate in spring and autumn 2017, 2018 and 2019; and peripheral in spring and autumn 2017, 2018, 2019 and spring 2020, showing that intermediate and peripheral cypselae can form a persistent soil cypsela bank.

Cypsela heteromorphism translates into differences not only in degree of dormancy but also differences in dispersal and timing of germination (Baskin and Baskin, Reference Baskin and Baskin2014). Generally, in Asteraceae, the central cypselae have low dormancy and high dispersal, and peripheral cypselae have high dormancy and low dispersal (Venable and Lawlor, Reference Venable and Lawlor1980; see Baskin et al., Reference Baskin, Lu, Baskin and Tan2013). This combination of traits for cypselae from the same plant allows seedlings to escape an unfavourable environment for establishment and growth in both time and space. Variability in degree of dormancy spreads the risk over time, and variability in dispersal ability spreads the risk over space. Cypselae with low dormancy and high dispersal may be dispersed to a new site where they may germinate immediately. Most cypselae with high dormancy and low dispersal remain near the mother plant and germinate after some period of time during which the mother plant may have died, creating a favourable site for establishment of a seedling of the same species.

In studies on dormancy and dispersal of the trimorphic cypselae of Heterosperma pinnatum, Venable et al. (Reference Venable, Búrquez, Corral, Morales and Espinosa1987) concluded that the low dormancy-high dispersal of the central cypselae was a high-risk strategy, and the high dormancy-low dispersal of the peripheral cypselae was a low-risk strategy, with the intermediate cypselae having a strategy between the two extremes. The proportion of heteromorphic cypselae (morphs) in H. pinnatum varied genetically between populations and between individuals (Venable and Búrquez, Reference Venable and Búrquez1989). Furthermore, the percentage of central cypselae with awns increased from dry open to mesic closed habitats and with an increase in annual precipitation (Venable et al., Reference Venable, Dyreson and Morales1995).

Fenesi et al. (Reference Fenesi, Sándor, Pyšek, Dawson, Ruprecht, Essl, Kreft, Pergl, Weigelt, Winter and van Kleunen2019) found evidence that cypsela heteromorphism is related to naturalization success of Asteraceae, but a short life cycle (annual or biennial) and relatively tall height of mature plants also contribute to the naturalization success of the heteromorphic species. Thus, the authors concluded that cypsela heteromorphism may be a part of the combination of traits that leads to naturalization success.

Amphicarpy

In the Baskin and Baskin (Reference Baskin and Baskin2014, p. 341) classification scheme, the two Asteraceae species mentioned in this section belong to Subgroup b sensu lato of Group B (Amphicarpy) of Division II (Heteromorphic). In the two known amphicarpic species of Asteraceae, Gymnarrhena micrantha and Catananche lutea, plants produce subterranean and aerial cypselae (Zhang et al., Reference Zhang, Baskin, Baskin, Cheplick, Yang and Huang2020). The subterranean and aerial cypselae of the winter annual G. micrantha are ND and germinate to higher percentages in light than in dark with the optimum temperature for germination being 15°C (Koller and Roth, Reference Koller and Roth1964). The aerial cypselae are smaller than the subterranean cypselae and may not be formed in years with low soil moisture; however, the plants always produce subterranean cypselae. The aerial cypselae potentially distribute the species to new suitable habitats, while the subterranean cypselae maintain the species in a habitat that has already proven to be suitable for production of offspring.

Individual plants of the annual C. lutea can produce five morphs: two kinds of subterranean cypselae (amphi-I that are non-dormant and amphi-II that have non-deep PD) and three kinds of aerial cypselae (central intermediate and peripheral) that are mostly ND but require light and relatively low (12, 19°C) temperatures for high germination percentages (Ruiz de Clavijo, Reference Ruiz de Clavijo1995). The aerial central cypselae have a more highly developed pappus than the intermediate cypselae, which in turn have more pappus than the peripheral cypselae. Thus, central, intermediate and peripheral acenes have high, intermediate and low dispersal, respectively. Overall, the subterranean cypselae ensure that the species is distributed in time, and the aerial cypselae ensure dispersal in both time and space. That is, the aerial peripheral and the aerial central cypselae of C. lutea ensure dispersal in time and space, respectively. We are not aware of any species of Asteraceae with amphi-basicarpy (Zhang et al., Reference Zhang, Baskin, Baskin, Cheplick, Yang and Huang2020).

Bet-hedging

When viewed from an evolutionary perspective, the production of cypselae with different strategies by the same plant is an adaptive bet-hedging strategy. That is, the production of two or more kinds of cypselae with different dormancy, dispersal and germination characteristics can increase the geometric mean and reduce variance in fitness. A commonly held idea is that, on average (i.e. arithmetic mean) the most-fit individuals leave the most offspring. However, this is not true in an environment that fluctuates stochastically, thus causing the number of offspring (fitness, e.g. R _o) to vary among the years. In this case, geometric mean is the best measure of fitness, and it is maximized across generations (years) by bet-hedging.

Geometric mean is the product of the number of values being considered raised to the 1/n power, for example, (4 × 12 × 20)^1/3 = (960)^1/3 = 9.86, which is lower than the arithmetic mean (i.e. 12). Thus, with a decrease in variance (σ²) or an increase in arithmetic mean (μ_A), geometric mean (μ_G) increases, and this relationship is expressed as μ_G = μ_A–(σ²/2) when fitness is >0 (Gillespie, Reference Gillespie1977; Crean and Marshall, Reference Crean and Marshall2009; Simons, Reference Simons2011). According to Seger and Brockmann (Reference Seger and Brockmann1987), ‘The geometric mean is the natural measure of long-term fitness under temporal variation because, like population growth itself, it is inherently multiplicative rather than additive’. Thus, the production of heterodiaspores is a way to decrease variance in the number of offspring produced per year and thus increase the geometric mean of the number of offspring across generations, that is, by bet-hedging.

A bet-hedging strategy is adaptive in temporally varying environments that result in both good and poor years for seedling establishment and survival (Venable Reference Venable1985a,Reference Venableb; Venable and Levin, Reference Venable and Levin1985a,Reference Venable and Levinb; Philippi and Seger, Reference Philippi and Seger1989; Philippi, Reference Philippi1993; Simons, Reference Simons2011; Gremer et al., Reference Gremer, Crone and Lesica2012; Starrfelt and Kokko, Reference Starrfelt and Kokko2012; Gianella et al., Reference Gianella, Bradford and Guzzon2021). The production of two kinds of offspring as in diaspore heteromorphic Asteraceae is a diversified bet-hedging strategy (Rajon et al., Reference Rajon, Venner and Menu2009; Crowley et al., Reference Crowley, Ehlman, Korn and Sih2016; Haaland et al., Reference Haaland, Wright, Tufto and Ratikainen2018). The cypselae with a low-risk strategy germinate immediately, but those with a high-risk strategy delay germinating, thereby providing a reserve of cypselae for the future regardless of whether a good or poor year follows the year of cypsela production. Based on a demographic–life-history study of disc versus ray cypselae, Venable (Reference Venable1985a,Reference Venableb) and Venable and Levin (Reference Venable and Levin1985a,Reference Venable and Levinb) present a strong case for bet-hedging in the heterocarpic (dimorphic) species Heterotheca subaxillaris var. latifolia. This is an annual species that grows in disturbed and open sites in which the disc and ray cypselae and the plants that originate from them have a high-risk–low-risk strategy, that is, high risk for disc cypselae and low risk for ray cypselae. The disc cypselae increase the μ_G by increasing μ_A, and the ray cypselae increase μ_G by decreasing σ².

In addition to cypselae differences in dispersal ability and degree of dormancy, bet-hedging has been attributed to other differences between disc and ray cypselae, including pre-dispersal insect predation, persistence in the seed bank and thickness of the pericarp (Evans et al., Reference Evans, Ferrière, Kane and Venable2007; Kistenmacher and Gibson, Reference Kistenmacher and Gibson2016). Also, genetic diversity between ray and disc cypselae has been considered. The observed heterozygosity across all populations of Grindelia ciliata was significantly higher in the disc pool than the ray cypsela pool, but the mean outcrossing percentage did not differ between ray and disc cypselae (Gibson, Reference Gibson2001). In Heterotheca subaxillaris, the level of genetic diversity did not differ significantly between ray and disc cypselae, and there was a mixed mating system with some inbreeding in most populations, which may result in founder effects (Gibson and Tomlinson, Reference Gibson and Tomlinson2002). However, the authors concluded that differences in size and dispersal ability between ray and disc cypselae helped reduce the effects of inbreeding depression on the populations.

Local adaptation

Ecotypes/local adaptations not involving cypsela dormancy/germination have been documented in various species of Asteraceae (Wacquant and Picard, Reference Wacquant and Picard1992; Andersson and Shaw, Reference Andersson and Shaw1994; Imbert et al., Reference Imbert, Escarré and Lepart1999; Scherber et al., Reference Scherber, Crawley and Porembski2003; Becker et al., Reference Becker, Colling, Dostal, Jakobsson and Matthies2006; Sambatti and Rice, Reference Sambatti and Rice2006; Ramsey et al., Reference Ramsey, Robertson and Husband2008; Raabová et al., Reference Raabová, Münzbergová and Fischer2011; Wang et al., Reference Wang, Chen, Zan, Wang and Su2012; Imani et al., Reference Imani, Rahbarian, Masoumi and Khorasani2014; Moore et al., Reference Moore, Moore and Baldwin2014; Pánková et al., Reference Pánková, Raabová and Münzbergová2014; Müller et al., Reference Müller, Schultz, Lauterbach, Ristow, Wissemann and Gemeinholzer2017; Molina-Montenegro et al., Reference Molina-Montenegro, Acuña-Rodriguez, Flores, Hereme, Lafon, Atala and Torres-Diaz2018; Sakaguchi et al., Reference Sakaguchi, Kimura, Kyan, Maki, Nishino, Ishikawa, Nagano, Honjo, Yasugi, Kudoh, Li, Choi, Chernyagina and Ito2018; van Boheemen et al., Reference van Boheemen, Atwater and Hodgins2019; Ollivier et al., Reference Ollivier, Kazakou, Corbin, Sartori, Gooden, Lesieur, Thomann, Martin and Tixier2020; Challagundla and Wallace, Reference Challagundla and Wallace2021; de Pedro et al., Reference de Pedro, Mayol and González-Martínez2021; Lin et al., Reference Lin, Landis, Sun, Huang, Zhang, Liu, Zhang, Sun, Wang and Deng2021). However, Carlina vulgaris (Jakobsson and Dinnetz, Reference Jakobsson and Dinnetz2005) and Centaurea hyssopifolia (Sánchez et al., Reference Sánchez, Alonso-Valiente, Albert and Escudero2017) did not exhibit local adaptation, except the survival of juveniles of C. hyssopifolia was higher in native than in non-native sites. Thus, there is evidence that some, but not all, species of Asteraceae can adapt to the local habitat conditions.

Some invasive species of Asteraceae, for example, Ambrosia artemisiifolia (van Boheemen et al., Reference van Boheemen, Atwater and Hodgins2019), Arctotheca populifolia (Brandenburger et al., Reference Brandenburger, Sherwin, Creer, Buitenwerf, Poore, Frankhan, Finnerty and Moles2019), Helianthus annuus (Hernández et al., Reference Hernández, Poverena, Garayalde and Presotto2019), Sonchus oleraceus (Ollivier et al., Reference Ollivier, Kazakou, Corbin, Sartori, Gooden, Lesieur, Thomann, Martin and Tixier2020) and Taraxacum campylodes (Molina-Montenegro et al., Reference Molina-Montenegro, Acuña-Rodriguez, Flores, Hereme, Lafon, Atala and Torres-Diaz2018) not only have developed local adaptations in new (invaded) sites but have done so rapidly. These results lend support to the conclusion of Oduor et al. (Reference Oduor, Leimu and van Kleunen2016) that invasive species develop local adaptations as frequently as native species. Rapid local adaptation of Asteraceae to new habitats, no doubt, has contributed not only to the great diversification of species in this family but also to its occurrence in all major vegetation zones on earth.

Species diversification

According to Tank et al. (Reference Tank, Eastman, Pennell, Soltis, Soltis, Hinchliff, Brown, Sessa and Harmon2015), ‘ … we still do not have a clear idea of the drivers of differential diversification among plant species’. Zhang et al. (Reference Zhang, Landis, Sun, Zhang, Lin, Kuang, Huang, Wang and Sun2021b) proposed that phylogenomic, morphological, ecological and model-based approaches need to be integrated into studies of diversification. Magallón et al. (Reference Magallón, Sánchez-Reyes and Gómez-Acevedo2019) identified a species diversification rate shift in Asteraceae at a mean time of 76.79 Ma, as one of 30 exceptional changes in species diversification rates of angiosperms.

An outstanding example of species diversification in Asteraceae is the 28 species of Argroxiphium, Dubautia and Wilkesia that evolved in the Hawaiian Islands (USA) from a single dispersal event of a tarweed (Madia/Raillardiopsis group) from California to Hawaii. Among the three genera, the diversity of life forms in the Hawaiian Islands includes trees, shrubs, cushion plants, vines and long-lived monocarpic and polycarpic rosette plants that grow in a range of habitats from dry woodland/scrublands to bogs (Robichaux et al., Reference Robichaux, Carr, Liebman and Pearcy1990; Baldwin and Sanderson, Reference Baldwin and Sanderson1998). Other examples of species diversification in the Asteraceae include: (1) Bidens, Hawaiian Islands, 19 species (Knope et al., Reference Knope, Morden, Funk and Fukami2012), (2) Brachyglottis, New Zealand, 30 species (Wagstaff and Breitwieser, Reference Wagstaff and Breitwieser2004), (3) Cheirolophus, Macaronesia, 20 species (Vitales et al., Reference Vitales, García-Fernández, Pellicer, Vallès, Santos-Guerra, Cowan, Fay, Hidalgo and Garnatje2014), (4) Dendroseris, Juan Fernández Islands, Chile, 11 species (Cho et al., Reference Cho, Kim, Yang, Crawford, Stuessy, López-Sepúlveda and Kim2020), (5) Encelia, deserts of the Americas, 15 species and 5 subspecies (Singhal et al., Reference Singhal, Roddy, DiVittorio, Sanchez-Amaya, Henriquez, Brodersen, Fehlberg and Zapata2021), (6) Espeletia complex, tropical Andes, 140 species (Pouchon et al., Reference Pouchon, Fernández, Nassar, Boyer, Aubert, Lavergne and Mavárez2018), (7) Hypochaeris apargioides complex, central-south Chile and adjacent Argentina, 4 species (López-Sepúlveda et al., Reference López-Sepúlveda, Tremetsberger, Ángeles-Ortiz, Baeza, Peñailillo and Stuessy2013), (8) Ligularia-Chremanthodium-Parasenecio complex, Qinghai-Tibetan Plateau, 11 species (Liu et al., Reference Liu, Wang, Wang, Hideaki and Abbott2006), (9) Psiadia, Madagascar and surrounding islands in western Indian Ocean, about 60 species (Strijk et al., Reference Strijk, Noyes, Strasberg, Cruaud, Gavory, Chase, Abbott and Thébaud2012), (10) Saussurea, high mountains of temperate Asia including the Qinghai-Tibetan Plateau, about 100 species (Zhang et al., Reference Zhang, Landis, Sun, Zhang, Lin, Kuang, Huang, Wang and Sun2021b), (11) woody Sonchus alliance, Canary Islands, 19 species (Kim et al., Reference Kim, Crawford, Francisco-Ortega and Santos-Guerra1999) and (12) Senecio, high equatorial Andes, 29 species (Dušková et al., Reference Dušková, Sklenář, Kolář, Vásquez, Romoleroux, Fér and Marhold2017).

Hybridization

Hybridization in plants, and Asteraceae in particular, can be between biotypes or subspecies of the same species or between species. Cypselae from crosses between wild and domesticated plants of Helianthus annus had increased germination (Snow et al., Reference Snow, Moran-Palma, Rieseberg, Wszelaki and Seiler1998; Mercer et al., Reference Mercer, Shaw and Wyse2006; Presotto et al., Reference Presotto, Poverene and Cantamutto2014). Cypselae from hybrids between Artemisia tridentata subsp. tridentata and A. tridentata subsp. vaseyana germinated to higher percentages than those from A. t. subsp. tridentata but to lower percentages than those from A. t. subsp. vaseyana (Graham et al., Reference Graham, Freeman and McArthur1995; Wang et al., Reference Wang, McArthur, Sanderson, Graham and Freeman1997). Cypselae from crosses between Solidago canadensis and S. virgaurea germinated to higher percentages than those from S. canadensis but to lower percentages than those from S. virgaurea (Pliszko and Kostrakiewicz-Gierałt, Reference Pliszko and Kostrakiewicz-Gierałt2017). However, cypselae from the hybrid germinated faster than those from either parent (Pliszko and Kostrakiewicz-Gierałt, Reference Pliszko and Kostrakiewicz-Gierałt2018).

Hybridization can lead to offspring having more than two sets of chromosomes, and in some cases, a new polyploid species is formed (e.g. Abbott and Lowe, Reference Abbott and Lowe2004). In general, there are two main kinds of polyploids: autopolyploids and allopolyploids. Autopolyploidy results from crosses within the same species or from WGD, while allopolyploidy results from crosses between species (see Parisod et al., Reference Parisod, Holderegger and Brochmann2010). Both kinds of polyploids are found in the Asteraceae.

Polyploidization and its consequences

WGD occurred in the early evolution of angiosperms (Masterson, Reference Masterson1994; Simillion et al., Reference Simillion, Vandepoele, Van Montagu, Zabeau and Van de Peer2002; Otto, Reference Otto2007; Soltis and Burleigh, Reference Soltis and Burleigh2009; Van de Peer et al., Reference Van de Peer, Fawcett, Proost, Sterck and Vandepoele2009; Schranz et al., Reference Schranz, Mohammadin and Edger2012; Ren et al., Reference Ren, Wang, Guo, Zhang, Zeng, Chen, Ma and Qi2018). Tank et al. (Reference Tank, Eastman, Pennell, Soltis, Soltis, Hinchliff, Brown, Sessa and Harmon2015) noted that increases in rates of angiosperm diversification tend to occur after WGD (palaeopolyploidization). Barker et al. (Reference Barker, Kane, Matvienko, Kozik, Michelmore, Knapp and Rieseberg2008) concluded that three WGDs occurred in the early history of the Asteraceae, prior to rapid radiation of its tribes in the Oligocene. Barker et al. (Reference Barker, Li, Kidder, Reardon, Lai, Oliveira, Scascitelli and Rieseberg2016) concluded that the Asteraceae share a paleotetraploid ancestor with the Calyceraceae (sister to Asteraceae) and that most Asteraceae ‘are descendants of a paleohexaploid’. Huang et al. (Reference Huang, Zhang, Liu, Hu, Gao, Qi and Ma2016) suggested that WGDs have been an important driving force in the evolution of Asteraceae and that they may have occurred during times of global catastrophe and dramatic changes in the environment, leading to stressful conditions for plant growth. These authors found WGDs in the core Asteraceae and at the separation of Asteraceae and Calyceraceae, crown node of Heliantheae alliance and clades Tussilaginae and Tragopogon-Scorzonerina. In addition, a WGD was found within Gnaphalieae. It should be noted that Zenil-Ferguson et al. (Reference Zenil-Ferguson, Burleigh, Freyman, Mayrose and Goldberg2019) concluded that lineage diversification in the Solanaceae was better explained by breeding system than by polyploidy.

In a consideration of polyploids in angiosperms, Barker et al. (Reference Barker, Arrigo, Baniaga, Li and Levin2015) found diploids, autopolyploids and allopolyploids in various genera of Asteraceae including Artemisia, Carthamus, Centaurea, Helianthus, Melampodium and Senecio but only diploids and allopolyploids in Stephanomeria. Although studies comparing seed germination of diploids and polyploids have been conducted for species in various plant families including Amaryllidaceae (Fialová et al., Reference Fialová, Jandová, Ohryzek and Duchoslav2014), Asteraceae (Thomas et al., Reference Thomas, Lefkovitch, Woo, Bowes and Peschken1994), Brassicaceae (Neuffer and Eschner, Reference Neuffer and Eschner1995), Cactaceae (Cohen et al., Reference Cohen, Fait and Tel-Zur2013), Cyperaceae (Escudero et al., Reference Escudero, Hahn, Brown, Lueders and Hipp2016), Fabaceae (Eliásová et al., Reference Eliásová, Trávníček, Mandák and Münzbergová2014), Onagraceae (Smith-Huerta, Reference Smith-Huerta1984), Plantaginaceae (Puech et al., Reference Puech, Rascol, Michel and Andary1998) and Poaceae (Hacker, Reference Hacker1988), relatively few species have been investigated in most families including the Asteraceae.

Among the Asteraceae that have been studied, diploid and tetraploid cypselae of Centaurea stoeba had similar germination percentages and rates when sown in a greenhouse (Hahn et al., Reference Hahn, Lanz, Fasel and Müller-Schärer2013). Diploid and tetraploid cypselae of Matricaria perforata had similar responses to temperature with the optimum for germination being 30/10°C. However, at suboptimal temperatures (5–15°C), tetraploid cypselae of M. perforata germinated to higher percentages than diploid cypselae. Cypselae of the polyploids Taraxacum venustum and T. albium had higher germination percentages at the optimum temperature (19°C) than those of the diploid T. platycarpum. However, at a low temperature (4°C), T. playcarpum cypselae germinated to a higher percentage than those of T. venustum but about the same as T. albium (Hoya et al., Reference Hoya, Shibaike, Morita and Ito2007). Furthermore, cypselae mass of polyploids may be greater than that of diploids (Hoya et al., Reference Hoya, Shibaike, Morita and Ito2007; Hahn et al., Reference Hahn, Lanz, Fasel and Müller-Schärer2013), which could have effects on germination, establishment and growth of the seedlings. The more or less lack of differences in germination of diploids and polyploids at least seems to suggest that ancient polyploidization had little, or no, effect on germination of cypselae in the Asteraceae.

In general, polyploidization may lead to changes/increases in breeding systems (Soltis et al., Reference Soltis, Soltis and Tate2003; Hojsgaard and Hörandl, Reference Hojsgaard and Hörandl2019), adaptability to new ecological niches (Levin, Reference Levin1983; Fawcett and Van de Peer, Reference Fawcett and Van de Peer2010; Ramsey, Reference Ramsey2011), invasiveness (te Beest et al., Reference te Beest, Le Roux, Richardson, Brysting, Suda, Kubešová and Pyšek2012; Hahn et al., Reference Hahn, Lanz, Fasel and Müller-Schärer2013), plant morphology (Zhang et al., Reference Zhang, Huang, Liu, Hu, Panera, Luebert, Gao and Ma2021a), seed size (Thompson, Reference Thompson1990), speciation/diversification (Comai, Reference Comai2005; Tank et al., Reference Tank, Eastman, Pennell, Soltis, Soltis, Hinchliff, Brown, Sessa and Harmon2015; Parisod and Broennimann, Reference Parisod and Broennimann2016; Stuessy and Weiss-Schneeweiss, Reference Stuessy and Weiss-Schneeweiss2019), tolerance to stress (Godfree et al., Reference Godfree, Marshall, Young, Miller and Mathews2017; Van de Peer et al., Reference Van de Peer, Mizrachi and Marchal2017) and mediators of gene flow (Peskoller et al., Reference Peskoller, Silbernagl, Hülber, Sonnleitner and Schönswetter2021). That is, polyploidy is not an ‘evolutionary dead-end’ (Soltis et al., Reference Soltis, Segovia-Salcedo, Jordon-Thaden, Majure, Miles, Mavrodiev, Mei, Cortez, Soltis and Gitzendanner2014a,Reference Soltis, Visger and Soltisb). Many of these changes in polyploids could have helped ameliorate the risk of extinction during times of catastrophic environmental (mass extinction) events (McElwain and Punyasena, Reference McElwain and Punyasena2007; Fawcett et al., Reference Fawcett, Maere and Van de Peer2009; Soltis and Burleigh, Reference Soltis and Burleigh2009; Vanneste et al., Reference Vanneste, Baele, Maere and Van de Peer2014).

Apomixis

Another consequence of polyploidization could be the loss of sexual reproduction due to the failure of gamete production (Tucker and Koltunow, Reference Tucker and Koltunow2009; te Beest et al., Reference te Beest, Le Roux, Richardson, Brysting, Suda, Kubešová and Pyšek2012; Hojsgaard and Hörandl, Reference Hojsgaard and Hörandl2019), which is a first step in the development of non-sexual formation of seeds (i.e. apomixis). The Asteraceae is an important family in terms of the number of species that can produce seeds asexually. The non-sexual formation of embryos and seeds is called agamospermy, but it usually is referred to as apomixis. However, apomixis s.l. includes agamospermy and reproduction only by vegetative means (de Meeȗs et al., Reference De Meeȗs, Prugnolle and Agnew2007; Noyes, Reference Noyes2007, Reference Noyes2022; Hojsgaard et al., Reference Hojsgaard, Klatt, Baier, Carman and Hörandl2014; Majeský et al., Reference Majeský, Krahulee and Vašut2017). In gametophytic apomixis, the embryo sac is diploid, and the egg develops parthenogenetically and includes apospory and diplospory (Richards, Reference Richards2003). In apospory, the embryo sac forms from a diploid somatic cell, and in diplospory an embryo sac forms from a megaspore mother cell that fails to undergo meiosis. In sporophytic or adventitious embryony, the embryo forms from somatic tissue, that is, usually from the nucellus or the integument, and is related to the production of multiple embryos in a seed (polyembryony) (Whitten et al., Reference Whitten, Seras, Baack and Otto2008; Hand and Koltunow, Reference Hand and Koltunow2014; Cardoso et al., Reference Cardoso, Viana, Matias, Furtado, Caetano, Consolaro and Brito2018). Carman (Reference Carman1997) listed 10 genera of Asteraceae in which polyembryony has been reported. It should be noted that Carman (Reference Carman1997) did not include sporophytic embryony in his definition of apomixis. In diplospory, the endosperm must be fertilized or seeds will not form (Hojsgaard and Hörandl, Reference Hojsgaard and Hörandl2019). However, in autonomous diplosory, which occurs predominantly in Asteraceae, both the embryo and endosperm develop without fertilization (Vinkenoog and Scott, Reference Vinkenoog and Scott2001).

Although asexual progeny of apomictic plants are genetically identical to the mother plant (Koltunow, Reference Koltunow1993; Koltunow and Grossniklaus, Reference Koltunow and Grossniklaus2003), they may vary epigenetically. Thus, for common dandelion (Taraxacum officinale, Asteraceae) genetically identical apomicitic plants exposed to various stress treatments exhibited epigenetic variation that was heritable (Verhoeven et al., Reference Verhoeven, Jansen, van Dijk and Biere2010). That is, the stress-induced DNA methylation changes in the F₀ generation (maternal stress exposure) were faithfully transmitted to the F₁ (progeny) generation.

Sexuality and apomixis could/can occur in the same species (i.e. facultative apomixis), and a seed lot collected from a population site of a species might be a mixture of sexually and asexually produced seeds (Koltunow, Reference Koltunow1993; Hand et al., Reference Hand, Krahulcová, Johnson, Oilkers, Siddons and Chrtek2015). Hojsgaard et al. (Reference Hojsgaard, Klatt, Baier, Carman and Hörandl2014) found apomictic seed production in 32 orders, 78 families and 293 genera of plants, and Asteraceae, Poaceae and Rosaceae had the majority of apomictic genera. In general, apomictic species are polyploids (Thompson and Ritland, Reference Thompson and Ritland2006; Mráz and Zdvořák, Reference Mráz and Zdvořák2019), and they occur mostly in tropical and temperate regions, with few species occurring in boreal and Arctic zones (Hojsgaard et al., Reference Hojsgaard, Klatt, Baier, Carman and Hörandl2014). In the Asteraceae, apomictic species occur in 47 genera (e.g. Antennaria, Crepis, Erigeron, Hieracium, Taraxacum) in four subfamilies (Asteroideae, 34; Cichorioideae, 9; Carduoideae, 2 and Mutisiodeae, 2), accounting for 13.9% of the genera in these subfamilies (Hojsgaard et al., Reference Hojsgaard, Klatt, Baier, Carman and Hörandl2014).

It is not clear how apomixis develops in a natural population of a plant species (Hojsgaard and Hörandl, Reference Hojsgaard and Hörandl2019). Hybridization long has been regarded as an important reason for the origin of apomictic taxa (Carman, Reference Carman1997; Bicknell and Koltunow, Reference Bicknell and Koltunow2004). Although some apomictic species are diploid hybrids (Beck, Reference Beck1986), many apomictic species are polyploids (Carman, Reference Carman1997). Thus, hybridization, but not polyploidy per se, seems to be a requirement for development of apomictic reproduction (Koltunow and Grossniklaus, Reference Koltunow and Grossniklaus2003). Genetic studies have revealed that apomixis is an inherited trait, for example, Erigeron (Noyes, Reference Noyes2000, Reference Noyes2022; Noyes and Rieseberg, Reference Noyes and Rieseberg2000), Hieracium (Bicknell et al., Reference Bicknell, Podivinsky, Catanach, Erasmuson and Lambie2001) and Taraxacum (Van Dijk et al., Reference Van Dijk, Tas, Falque and Bakx-Schotman1999), which helps explain why apomixis may appear in hybrids.

Five-month-old dry stored (i.e. probably afterripened) cypselae from autonomously apomicic biotypes of Taraxacum officinale differed in mass and germination percentages (Tweney and Mogie, Reference Tweney and Mogie1999). Cypselae that weighed >0.8 mg germinated to 87.3% in moist soil (compost) in a greenhouse. On the other hand, cypselae that weighed 0.7–0.79 mg germinated to 52.4% but those weighing <0.3 mg germinated to only 0.28%. In another study of the germination of apomictic cypselae, Sailer et al. (Reference Sailer, Tiberi, Schmid, Stöcklin and Grossniklaus2021) used a common garden experiment to determine if plants from asexual cypselae of the faculative apomictic species Pilosella officinarum competed better than plants from sexual cypselae. They found that germination proportion of offspring (cypselae) of sexual plants was higher than that of apomictic plants.

Soil cypsela banks

Cypselae of Asteraceae have been found in soil samples collected in a wide diversity of habitats. In the results from 185 soil seed bank studies (see Tables 7.2, 7.4 and 7.5 in Baskin and Baskin, Reference Baskin and Baskin2014 for references) that were conducted in such a way that it is highly probable that persistent seeds were present (i.e. samples collected after germination but before input of new seeds), we found species belonging to 155 families, including Asteraceae. In the Asteraceae, there were 131 species in 73 genera. However, the presence of cypselae in the soil tells us very little about how long they can live after burial. Studies of individual species of Asteraceae that involved collecting soil samples at population sites and counting the number of viable cypselae in the sample or the number of seedlings that emerged from them have been conducted for various species, for example, Ageratina adenophora (Shen et al., Reference Shen, Liu, Baskin, Baskin and Cao2006), Artemisia quettensis (Ahmad et al., Reference Ahmad, Gul, Islam and Athar2007), Brachyscome muelleri (Jusaitis et al., Reference Jusaitis, Sorensen and Polomka2003), Centaurea solstitialis (Joley et al., Reference Joley, Maddox, Schoenig and Mackey2003), Chromolaena odorata (Epp, Reference Epp1987; Witkowski and Wilson, Reference Witkowski and Wilson2001), Pilosella aurantiaca, P. piloselloides subsp. praealta (Bear et al., Reference Bear, Giljohann, Cousens and Williams2012), Polymnia canadensis (Bender et al., Reference Bender, Baskin and Baskin2003) and Symphyotrichum laurentianum (Kemp and Lacroix, Reference Kemp and Lacroix2004). Unfortunately, even with these individualized studies, the longevity of cypselae in the soil is not known.

To determine their longevity, cypselae of various species of Asteraceae have been placed in mesh bags/containers and buried in the soil (Table 3). The period of burial ranged from a few months to 40 years, and viability at the end of burial varied from 0 to 97%, with a mean (±SE) survival of 25.6±3.7%. These burial studies included 39 species in 10 tribes, which is a very low representation of the species and tribes in Asteraceae. Furthermore, only in the study of Galinsoga parviflora was the survival of ray and disk cypselae (which are dimorphic) compared with 21.3 and 0% of the cypselae, respectively, viable after 2.1 years (Espinosa-Garcia et al., Reference Espinosa-Garcia, Vazquez-Bravo and Martinez-Ramos2003). Overall, it does not appear that long-lived persistent cypselae banks are very common for species of Asteraceae.

Table 3.

Survival of cypselae of Asteraceae species placed in bags or other containers and buried in soil in the field for 0.25 to 40 years, depending on species

^a Cypselae placed in a soil-filled bottle that was inverted and buried in the soil.

^b Cypselae placed in short cylinders (7.6 wide × 2.5 cm deep) cut from polyvinylchloride pipe with nylon mesh on each end.

Also, if cypselae are dispersed/sown onto the soil surface, they generally germinate in the first year, but some may delay germination until the second or a later year. We sowed freshly matured cypselae of 52 species of Asteraceae (78 datasets because cypselae of some species were collected and sown in more than one year) on soil and exposed them to natural seasonal temperature cycles (see temperature data in Baskin et al., Reference Baskin, Baskin and Chester2019) and semi-natural watering regimes in a non-heated glasshouse in Lexington, Kentucky (USA). Germination was monitored weekly for 1 year after the last cypselae of a species/sowing germinated (Baskin et al., Reference Baskin, Baskin, Hu and Zhang2022). For one group of species, including Echinacea tennesseensis, Helianthus atrorubens, Liatris squarrosa, Solidago altissima and Symphotrichum pilosum, cypselae sown in autumn germinated only the following (first) spring. In another group of species, including Boltonia decurrens, Echinacea simulata, Eupatorium altissimum, Helenium amarum and Rudbeckia triloba, many cypselae sown in autumn germinated in the first spring, but in the second, and sometimes the third, spring a few additional cypselae germinated (Baskin et al., Reference Baskin, Baskin, Hu and Zhang2022). For short-lived monocarpic perennial (MP), polycarpic perennial (PP) summer annuas (SA) and winter annual (WA) Asteraceae, the mean (±SE) number of years for germination was 1.70 ± 0.20, 1.69 ± 0.25, 1.56 ± 0.22 and 1.81 ± 0.28, respectively (Table 4). Species whose cypselae germinated in 3 or more years include Polymnia canadensis (MP, 3 years), Achillea millefolium (PP, 7), Ambrosia artemisiifolia (SA, 4), A. trifida (SA, 3), Crepis pulchra (WA, 3) Helenium amarum (WA, 5) Krigia virginica (WA, 3) and Lactuca serriola (WA, 3).

Table 4.

Number of years cypselae of Asteraceae germinated in the non-heated glasshouse in Lexington, Kentucky (USA)

^a Cypselae may have intermediate physiological dormancy, but this has not been confirmed by laboratory experiments.

The germination responses of Lactuca floridana cypselae that we buried in soil in the non-heated glasshouse help explain why a species has only one germination season. At maturity in autumn, cypselae of this species germinated to 9, 9, 66, 99 and 93% when incubated in light at 15/6, 20/10, 25/15, 30/15 and 35/20°C, respectively, with no germination at any temperature regime in darkness. During exposure to low temperatures during burial in winter, cypselae gained the ability to germinate to 98–100% in both light and dark at the five temperature regimes. When bags of buried cypselae were exhumed in spring (1 March), 50% of the cypselae had already germinated, and when bags were exhumed on 1 April, 1 May and 1 June, only 29, 21 and 0%, respectively, of the cypselae remained non-germinated. That is, during cold stratification, cypselae gained the ability to germinate in darkness and thus germinated as soon as temperatures increased in spring (Baskin and Baskin, unpublished).

Life form, vegetation zone and phylogeny (tribes) of cypsela dormancy in Asteraceae

Information on cypsela dormancy and life form of Asteraceae species previously was compiled for 755 species growing in the various vegetation zones on earth (Baskin and Baskin, Reference Baskin and Baskin2014). Since 2014, we have continued to collect information on cypselae dormancy in Asteraceae. In addition to regularly checking new issues of plant-related journals for dormancy/germination information, we conducted many web searches using a variety of search terms in various combinations: Asteraceae, Compositae, names of tribes and genera of Asteraceae, names of countries in South America, Asia and Africa, achene, cypsela, germinação, germinación, semillas and sementes.

In the papers found in the literature, if fresh cypselae germinated to a relatively high percentage over a range of temperatures and dormancy-breaking treatments such as afterripening, cold stratification, warm stratification, scarification and gibberellin did not increase germination, the species was listed as having ND cypselae. However, if any dormancy-breaking treatment increased the percentage and/or rate of germination, the species was listed as having PD. In the case of heteromorphic species, if one cypsela morph was ND and another had PD, the species was listed as PD. If a species was listed in Baskin and Baskin (Reference Baskin and Baskin2014) as ND/PD or PD/ND, it was counted as PD in this review. In comparing ND and PD of tropical and temperate regions, the data for Asteraceae species from special habitats were included under the temperate region.

We found information for 450 additional species, bringing the total to 1205 species entries in supplementary Table S1. All species of Asteraceae were recorded according to life form and vegetation zone/special habitats (supplementary Table S1). However, 12 species of weeds (Ageratum conyzoides, Bidens pilosa, Chromolaena odorata, Cirsium arvense, Emilia sonchifolia, Galinsoga parviflora, Synedrella nodiflora, Tithonia diversifolia, T. rotundifolia, Tridax procumbens, Senecio vulgaris and Tanacetum vulgare) are common in more than one vegetation zone in supplementary Table S1, which reduces the total number of species to 1182. The 1182 species occur in 373 genera and 35 tribes of Asteraceae. In working with the results of our compilation, the multiple listings of the 12 weeds were counted as separate species based on research done in different vegetation zones.

Life forms and dormancy

Among the 1205 entries in the database, there were 14 (1.2%), 180 (14.9%), 8 (0.7%) and 1003 (83.2%) trees, shrubs, vines (including woody and herbaceous climbers) and herbs, respectively (Table 5). Overall, 22.2% of the species had ND cypselae, and 50.0, 20.6, 25.0 and 22.0% of the tree, shrub, vine and herb species, respectively, had ND cypselae; thus, 50.0, 79.4, 75.0 and 78.0%, respectively, had PD. We found germination data for 14 species of Asteraceae that are trees, and 13 of them occur in tropical vegetation zones and one in the warm moist temperature woodlands (i.e. the broad-leaved evergreen forest). Trees occur in various tribes of Asteraceae, including Astereae, Bahieae, Coreopsideae, Eupatorieae, Gochnatieae, Heliantheae, Inuleae, Liabeae, Millerieae Neurolaeneae, Senecioneae and Vernonieae (Ricker et al., Reference Ricker, Hernández, Sousa and Ochoterena2013; Beech et al., Reference Beech, Rivers, Oldfield and Smith2017; Redonda-Martínez et al., Reference Redonda-Martínez, Pliscoff, Moreira-Muñoz, Salas and Samain2021). Thus, clearly cypsela dormancy has been studied in only a small fraction of the tree species of Asteraceae.

Table 5.

Number of species of trees, shrubs, vines and herbs of Asteraceae in different vegetation zones/special habitats with non-dormant (ND) and physiologically dormant (PD) cypselae

The lack of research is even more apparent for Asteraceae vines than for trees. Only eight species of vines were recorded – two with ND and six with PD. Gentry (Reference Gentry, Putz and Mooney1991) says there are 470 species and 23 genera of climbing Asteraceae in the New World, but he does not show Asteraceae in bar diagrams depicting the most important plant families of vines in the Amazon rainforest of Brazil or in Africa or Borneo. However, he does show vines of Asteraceae for upper Andean sites in Bolivia, Ecuador and Columbia and for a lowland dry forest in Ecuador. Gentry (Reference Gentry, Putz and Mooney1991) gives the number of vine species of Asteraceae in temperate North America and Europe as one to three but does not provide their names. Vines occur in tribes Astereae, Barnadesieae, Coreopsideae, Eupatorieae, Gnaphalieae, Heliantheae, Mutisieae, Senecioneae and Vernonieae of Asteraceae (Morellato and Leitão-Filho, Reference Morellato and Leitão-Filho1996; Cai et al., Reference Cai, Schnitzer, Wen, Chen and Bongers2009; Schnitzer et al., Reference Schnitzer, Mangan, Dalling, Baldeck, Hubbell, Ledo, Muller-Landau, Tobin, Aguilar, Brassfield, Hernandez, Lao, Perez, Valdes and Yorke2012; Seger and Hartz, Reference Seger and Hartz2014; Sánchez-Chávez et al., Reference Sánchez-Chávez, Rodríguez, Castro-Castro, Pérez-Farrera and Sosa2019).

Of the 180 species of shrubs, germination of 90 each has been studied in the tropical and temperate regions; four of the temperate region shrubs are psammophytes (i.e. in a special habitat). However, for the 1003 herbs, 199, 772 and 32 species are from the tropics, temperate region and special habitats, respectively, with 74.4, 78.8 and 81.3% of them having cypselae with PD, respectively.

Vegetation zone and dormancy

The proportion of species with ND and PD cypselae for each vegetation zone is shown in Fig. 1. In evergreen and semi-evergreen rain forests, more species have ND than PD cypselae. However, in all other vegetation zones, except the (temperate) alpine/high-latitude tundra, where the number of species with ND and PD is the same, more species have cypselae with PD than ND.

Fig. 1.

Proportion of Asteraceae species with non-dormant (ND) and physiologically dormancy (PD) cypselae in each tropical and temperate vegetation zone.

Tribes, life forms, vegetation zones and dormancy

In the tropical region (all tropical vegetation zones combined), the number of tribes of tree species with ND and PD was 4 and 2, respectively; shrubs 11 and 17, respectively; vines 2 and 2, respectively; and herbs 13 and 22, respectively (Table 6). In the temperate region, the number of tribes of tree species with ND and PD was 0 and 1, respectively; shrubs 6 and 9, respectively; vines 0 and 4, respectively; and herbs 17 and 25, respectively. Thus, in the tropical region, more tribes are represented by shrubs and herbs than by vines or trees, and more shrubs and herbs have PD than ND. In the temperate region, more tribes are represented by herbs than by trees, shrubs and vines, and more herbs have PD than ND.

Table 6.

Number of species of trees, shrubs, vines and herbs with non-dormant (ND) and physiologically dormant (PD) cypselae in tribes of Asteraceae in tropical and temperate regions

B, basal grade; C, central grade; HA, Heliantheae Allianace of Asteraceae. Tribes of Asteraceae are sensu Susanna et al. (Reference Susanna, Baldwin, Bayer, Bonifacino, Garcia-Jacas, Keeley, Mandel, Ortiz, Robinson and Stuessy2020).

^aNo information was found for species in tribes Eremothamneae, Famatinantheae, Feddeeae, Hecastocleideae, Moquinieae, Neurolaeneae, Oldenburgieae, Onoserideae, Platycarpheae or Wunderlichieae.

Across the tropical and temperate zones and all life forms, the tribes with ≥10% of the 1205 species were Anthemideae (11.7%), Astereae (16.7%) and Gnaphalieae (10.3%). The tribes Antroismeae, Barnadesieae, Chaenactideae, Corymbieae, Gymnarrheneae, Nassauvieae, Perityleae, Pertyeae, Polymnieae and Stiffieae are represented by only one species (0.08%) each (Table 6). Among the 35 tribes, 19 had both ND and PD, 7 only ND and 9 only PD. In the basal grade (B), central grade (C) and Heliantheae Alliance (HA) of Asteraceae (sensu Susanna et al., Reference Susanna, Baldwin, Bayer, Bonifacino, Garcia-Jacas, Keeley, Mandel, Ortiz, Robinson and Stuessy2020), if a tribe was represented by two or more species, both ND and PD were found among them, except for Bahieae, Liabeae and Tarchonantheae. Bahieae (HA) was represented by four PD species, Liabeae (HA) by two ND species and Tarchonantheae (C) by two ND species. We note that tribes Eremothamneae, Famatinantheae and Feddeeae are monospecific. Information about the occurrence of ND and PD is plotted on the Asteraceae tribe-level chronogram of Mandel et al. (Reference Mandel, Dikow, Siniscalchi, Thapa, Watson and Funk2019) shows that both ND and PD are widely distributed throughout the family (supplementary Fig. S1).

Tropical trees occurred in 1, 2 and 1 tribe(s) in B, C and HA, respectively, but temperate trees were in only one C tribe (Table 6). Except for one tropical C tribe (Vernonieae) with both ND and PD, all tribes of trees had only ND cypselae. Tropical shrubs were in 3, 10 and 7 tribes of B, C and HA, respectively, and temperature shrubs in 2, 8 and 1 tribe(s), respectively. With the exception of species in 1 C and 2 HA tribes in the tropical zone and 1 B and 1 C tribes in the temperate zone with ND cypselae, all tribes had either both ND and PD or only PD. Tropical vines were in 1, 1 and 2 tribes of B, C and HA, respectively, and temperate vines in 1, 1 and 2, respectively. With the exception of species in 2 HA tribes in the tropical zone with ND cypselae, all tribes had cypselae with PD. Tropical herbs were in 1, 14 and 9 tribes of B, C and HA, respectively, and with the exception of species in 1 C tribe with ND cypselae all tribes had either both ND and PD or only PD. Temperate herbs were in 2, 14 and 10 tribes, respectively, and with the exception of species in 2 B tribes with ND cypselae, all tribes had either both ND and PD or only PD.

The tribes with the best representation across the different vegetation zones are: Senecioneae (in all zones except temperate montane) and Astereae (not in rainforest or hot desert) (Table 7). The second most geographically widely distributed tribes are the Eupatorieae and Heliantheae, but each is missing from four vegetation zones. Eupatorieae was not recorded in temperate montane, temperate alpine, matorral or cold desert and Heliantheae was not in tropical alpine, temperate alpine, temperate montane or broad-leaved evergreen.

Table 7.

Tribes of Asteraceae in different vegetation zones represented by one or more species with non-dormant (N) or physiologically dormant (P) cypselae

Tropical: Rainf, rainforest; Mont, montane zone on mountains; Alpine, alpine zone on mountains; Semie, semi-evergreen rainforests; Dry, dry deciduous forests; Sav, savanna; H-D, hot deserts. Temperate/arctic: Mator, matorral/sclerophyllous woodlands; Br, broad-leaved evergreen or moist-warm temperature woodlands; Decid, deciduous (nemoral) forests; Grass, grasslands; C-D, cold deserts; Boreal, subalpine/high-latitude boreal; Alpine, alpine/high-latitude tundra; Mont, montane zone on mountains; Woodl, woodland zone on mountains.

The number of tribes represented by one or more species (with ND or PD) in each vegetation zone ranges from 3 to 20 (Table 7). The low number (3) is for tribes in the temperate montane zone, where data were found for only five species of Asteraceae, while the high number (20) is for hot deserts, where data are available for 108 species (Table 5). Of the six tribes found in the rainforest, 5 and 3 of them had species with ND and PD, respectively. However, for all vegetation zones, except the rainforest and the tropical alpine (5 and 5 with ND and PD, respectively), the tribes were represented by more species with PD than ND. Tribes represented by either ND or PD (but not by both) in only one vegetation zone are Antroismeae, Barnadesieae, Chaenactideae, Corymbieae, Dicomeae, Gymnarrheneae, Nassaurieae, Perityleae, Petryeae, Plucheeae and Polymnieae. Clearly, more data are needed for Asteraceae in many of the vegetation zones, especially for the poorly represented tribes.

Dormancy/germination flexibility and adaptability

ND and PD are found in cypselae of Asteraceae in various tribes, genera and species; life forms and life cycles; and in all vegetation zones on earth. Except for one of the three morphs of the cypsela-trimorphic species Heteracia szovitsii (Lu et al., Reference Lu, Dong, Tan, Baskin and Baskin2020) with intermediate PD, the level of PD in the Asteraceae is non-deep. Furthermore, six types of non-deep PD have been identified, and all of them are known to occur in the Asteraceae. The types of non-deep PD are broken by exposure of cypselae to environmental conditions that are not favourable for seedling establishment and growth. Since dormancy-break occurs during the non-favourable season for growth, cypselae are ND and can germinate at the beginning of the favourable season for growth, giving the seedling the full length of the favourable season to become established. Variation in the types of non-deep PD allows for fine-tuning of germination, which is part of the suite of adaptations of Asteraceae species to many of the vast diversity of habitats on earth. In general, we can conclude that cypselae dormancy in Asteraceae is not complicated but that it is very flexible.

According to the evolutionary transition analysis between seed dormancy states, morphophysiological dormancy (MPD) is probably the ancestral dormancy state, and there have been three major shifts from MPD to PD (Willis et al., Reference Willis, Baskin, Baskin, Auld, Venable, Cavender-Bares, Donohue and Rubio de Casas2014). PD has been an evolutionary hub and has given rise to seeds that are ND and to those with MPD, morphological dormancy (MD), physical dormancy (PY) and combinational dormancy (PY + PD). However, there have been transitions from ND, MPD, PY, PY + PD and MD back to PD. Thus, the close association between ND and PD throughout the Asteraceae is no doubt related to the transitions between PD and ND (i.e. PD ↔ ND). Willis et al. (Reference Willis, Baskin, Baskin, Auld, Venable, Cavender-Bares, Donohue and Rubio de Casas2014) described ND as ‘either a recent evolutionary development or an ephemeral state’. However, in an investigation of the evolutionary transitions between seed dormancy and ND, Zhang et al. (Reference Zhang, Liu, Sun, Baskin, Baskin, Cao and Yang2022) found no evidence that ND is an evolutionary end point or that species with ND seeds have a higher extinction rate than those with dormant seeds. Further ND ‘has adaptive evolutionary significance’ (Zhang et al., Reference Zhang, Liu, Sun, Baskin, Baskin, Cao and Yang2022).

Clearly, PD is an adaptive strategy for the persistence of Asteraceae species growing in habitats with annually fluctuating favourability/unfavourability of conditions for germination and seedling survival. On the other hand, the lack of dormancy in cypselae of an Asteraceae species would seem to indicate that cypselae mature and are dispersed at a time of high predictability that environmental conditions are favourable for seedling establishment. That is, there is no benefit in germination being delayed via PD. However, as described for Helenium amarum (Baskin and Baskin, Reference Baskin and Baskin1973), cypselae dispersed late in a so-called favourable season for seedling establishment may not germinate due to environmental temperatures being below those required for germination. In which case, germination can be delayed until the temperatures increase again. Would this scenario lead to selection for Type 2 non-deep PD?

In response to the selective pressure due to changes in seasonal patterns of temperature and precipitation and/or dispersal of seeds/cypselae to new habitats, six types of non-deep PD have evolved. The evolutionary pathways proposed for type of non-deep PD are Type 4 → Type 2 → Type 3 and Type 5 → Type 1 → Type 3 (see Fig. 12.21 in Baskin and Baskin, Reference Baskin and Baskin2014). Type 6 was not known at the time these pathways were proposed. However, the occurrence of Types 1 and 6 in cypselae of Silybum marianum (Monemizadeh et al., Reference Monemizadeh, Ghaderi-Far, Sadeghipour, Siahmarguee, Soltani, Torabi and Baskin2021) from different populations suggests a close relationship between Types 1 and 6. Type 6 in which seeds/cypselae germinate over a wide range of temperatures without going through conditional dormancy may represent a response to unpredictable timing of rainfall during the growing season.