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The heterocarpic species Atriplex tatarica produces two types of seeds. In this study, how basic population genetic parameters correlate with seed germinability under various experimental conditions was tested.
Population genetic diversity was ascertained in eight populations of A. tatarica by assessing patterns of variation at nine allozyme loci. Germinability of both seed types from all sampled populations was determined by a common laboratory experiment under different salinity levels. Basic population genetic parameters, i.e. percentage of polymorphic loci, average number of alleles per locus and observed heterozygosity were correlated with observed population germination characteristics.
Atriplex tatarica possesses a remarkable heterocarpy, i.e. one type of seed is non-dormant and the other shows different dormancy levels in relation to experimental conditions. Significant negative correlations have been detected between germination of both seed types and the coefficient of inbreeding, and a significant negative correlation between germination of dormant seeds and other population genetic parameters, i.e. percentage of polymorphic loci and average number of alleles per polymorphic locus. Moreover, populations from the region characterized by a shorter growing season manifested higher germinability, i.e. had lower dormancy, than those from the lower-latitude one.
In general, germination of non-dormant seeds is probably not under strong genetic control. Hence, they germinate as soon as conditions are favourable, thus ensuring survival in the short term, but populations risk local extinction if conditions become adverse (i.e. a high-risk strategy). In contrast, germination of the dormant type of seeds is under stronger genetic control and is significantly correlated with basic population genetic parameters. These seeds ensure long-term reproduction and survival in the field by protracted germination, albeit in low quantities (i.e. A. tatarica also adopts a low-risk strategy).
Production of morphologically different types of fruits and seeds by a single individual is an uncommon phenomenon in flowering plants. Fruit heterocarpy and seed polymorphism have been described in 18 families of angiosperms so far (Imbert, 2002). They are common in the Asteraceae, Brassicaceae, Chenopodiaceae and Poaceae (Mandák, 1997; Imbert, 2002), typically occurring in annual, often pioneer species, which occupy habitats with a highly variable environment in either time or space (Baskin and Baskin, 1998). Depending on species under study, fruits or seed morphs typically differ in their dispersal ability (Sorenson, 1978; Payne and Maun, 1981; Baker and O'Dowd, 1982; Mandák and Pyšek, 2001a), dormancy patterns (Brändel, 2004, 2007), germination requirements (Baskin and Baskin, 1998, and references therein), competitive abilities (Flint and Palmblad, 1978; Imbert et al., 1997) or vulnerability to predation (Cook et al., 1971). Given these ecological differences of individual seed morphs, seed polymorphism is considered an evolutionary bet-hedging strategy that enables plants to escape from the negative effects of density or sib competition (Levin et al., 1984; Venable and Brown, 1993) and spreads offspring germination over time and space (Venable, 1985; Mandák and Pyšek, 2001b).
Studies relating ecological and genetic causes of heterocarpy are quite rare and exclusively devoted to members of the family Asteraceae (see Cheptou et al., 2001; Gibson, 2001; Gibson and Tomlinson, 2002; Picó and Koubek, 2003), except for one study regarding the family Amaranthaceae (Mandák et al., 2006b). Furthermore, most concern the relationship between mating system and genetic composition of particular achene morphs (Cheptou et al., 2001; Gibson, 2001; Gibson and Tomlinson, 2002). There are only two studies that deal with the relationship between genetic variability of individual achene morphs and the fitness of plants grown up from various achene morphs (Picó and Koubek, 2003; Mandák et al., 2006b). At present, the relationship between genetic diversity of populations derived from different fruit morphs and fitness-related traits remains poorly understood (see Mandák et al., 2006b).
In general, the negative effect of inbreeding depression on germination characteristics, seedling growth, and fecundity is well documented in both natural (Charlesworth and Charlesworth, 1987; Keller and Waller, 2002) and experimental populations (e.g. Holtsford and Ellstrand, 1990; Ågren and Schemske, 1993; Eckert and Barrett, 1994; Husband and Schemske, 1995; Koelewijn and Van Damme, 2005; Goodwillie and Knight, 2006; Mandák et al., 2006b). Inbreeding depression is mostly explained as a result of accumulation of recessive deleterious alleles over time (the so-called partial dominance hypothesis; Charlesworth and Charlesworth, 1987; Johnston and Schoen, 1995; Keller and Waller, 2002). Theoretical studies predict that in populations with a longer history of inbreeding, deleterious recessive alleles are exposed to selection, as homozygotes are purged from the population (Lande and Schemske, 1985). Consequently, such populations are expected to have lower levels of inbreeding depression than populations that are predominantly outcrossing.
Reduction in inbreeding depression in selfing populations has been documented several times (Barrett and Charlesworth, 1991; Dole and Ritland, 1993; Husband and Schemske, 1996; Mustajärvi et al., 2005). However, recent studies suggest that purging in selfing populations may not be effective enough, since it may remove only a minor proportion of recessive alleles (Byers and Waller, 1999, and references therein). A comparison of inbreeding depression among more and less inbred plant species has pointed out the importance of the ‘purging effect’ particularly for traits expressed early in development, which are under strong selection (Keller and Waller, 2002). In the case of heterocarpic species, if it is supposed that inbreeding influences fitness of progeny differently in different seed morphs, this can have an important effect on population dynamics and consequently the distribution of the species (Gibson and Tomlinson, 2002; Picó and Koubek, 2003).
The principal aim of this study is to demonstrate how basic population genetic parameters correlate with seed germinability under various experimental conditions. Therefore several populations of the heterocarpic species Atriplex tatarica with different amounts of genetic variability determined by allozyme analysis have been examined and questions were asked whether there is any correlation among population genetic characteristics and germinability, specifically: (a) Are there any differences in germination of individual seeds types? (b) Is there any relationship between the pattern of germination or dormancy and population genetic diversity? (c) How does inbreeding and low population genetic diversity affect germinability of individual seed types under different ecological conditions and in different geographical regions?
Atriplex tatarica L. (syn. A. laciniata L., A. sinuata Hoffm., A. veneta Willd.) (Amaranthaceae) is an annual diploid species (2n = 18) of the section Sclerocalymma (Asch.) Asch. et Graebn. It is a facultative halophyte (Osmond et al., 1980; Mandák, 2003b) spreading effectively along roads treated with salt during winter (Mandák, 2003a).
Atriplex tatarica is a heterocarpic species which produces two morphologically different seed types that differ in dormancy-breaking requirements and nitrate and salinity tolerance (Mandák, 2003b). The type-B seed is a small black achene with a glossy, smooth testa covered by small bracteoles. The type-C seed is brown and larger, enclosed within extended bracteoles. Type B seeds contribute to a persistent seed bank and require cold stratification for successful germination. Type C seeds germinate immediately when conditions are optimal and thereby contribute to a transient seed bank (Mandák, 2003b). Moreover, type-C seeds are able to germinate under a wider range of salinity and nitrate conditions than type-B seeds (Mandák, 2003b).
Atriplex tatarica is native to central Asia, Asia Minor, south-western Siberia, further extending to North Africa and south-eastern Europe, where it occurs in deserts, salt steppes and various types of disturbed habitats (Aellen, 1960; Meusel et al., 1965; Kochánková and Mandák, 2008). In the area of central and western Europe, A. tatarica occupies especially human-made habitats such as urban areas, roads, railways and dunghills (Aellen, 1960; Kochánková and Mandák, 2008). The north-western border of its continuous European distribution lies partly in the Czech Republic. The species is very common in the south-eastern part of the Czech Republic (South Moravia), which probably represents part of the native continuous area of distribution reaching from south-eastern Europe through the Pannonian lowland. In the rest of the Czech Republic, i.e. the western part (Bohemia), the species is only found at several localities that are geographically isolated from Moravian sites and from each other (Mandák et al., 2005). Hence, while northern populations of A. tatarica showed significantly lower allelic richness (A = 1·462) than populations from the southern part of the study area (A = 1·615), they did not differ in observed heterozygosity (Ho), gene diversity (HS), inbreeding within populations (FIS) or population differentiation (FST), despite having generally lower values of particular genetic measurements in the marginal (northern) region (Mandák et al., 2005).
Locality selection was based on data in Mandák et al. (2005), where population genetic parameters of each population were assessed by allozymes. The sampling scheme was designed in a way so as (a) to record the whole range of variability of inbreeding determined by Mandák et al. (2005) and (b) to explain the potential effect of region on seed germinability, i.e. four populations of A. tatarica were selected from one of the two following regions of the Czech Republic: Bohemia and Moravia (see Table 1).
In spring 2005, five seedlings were collected from each population along a transect with seedlings collected 5 m apart and then transported to the experimental garden of the Institute of Botany, Academy of Sciences, Průhonice, Czech Republic (49°59′30″N, 14°34′00″E, approx. 320 m a.s.l.), where they were planted in 16-cm-sized pots filled with garden compost for one season in order to minimize maternal effects (Baskin and Baskin, 1973; Quinn and Colosi, 1977). At the end of the growing season (25 October 2005), seeds were collected and stored in paper bags in the dark for no longer than 3 months at laboratory temperature. The identity of each maternal plant was maintained.
Allozyme data were obtained between June 2002 and August 2003 (Mandák et al., 2005). Ten samples were analysed from each population and collected from individuals along a 50-m transect with individuals spaced 5 m apart. Samples were placed on ice, transported to the laboratory and the youngest expanded leaf of each plant was analysed within 24 h.
Nine polymorphic (at the 0·05 level), readable and reproducible enzyme loci resolved from five enzymatic systems were analysed as is described in Mandák et al. (2005), i.e. aspartate aminotransferase (EC 2·6·1·1), leucine aminopeptidase (EC 3·4·11·1), malate dehydrogenase (EC 1·1·1·37), shikimate dehydrogenase (EC 1·1·1·25) and superoxide dismutase (EC 1·15·1·1).
The germination experiment was started in January 2006. After removing bracts, seeds were sorted according to their seed type and tested separately. Only those seeds that appeared to be fully developed upon visual inspection were included in the experiment. Seeds were placed in 80-mm-diameter Petri dishes on a single layer of filter paper, wetted with 20 mL of water (used as a control treatment) or 1 % aqueous sodium chloride solution (as salinity treatment), which is the ‘optimal’ salt concentration established in a previous germination experiment; see Mandák, 2003b). Seeds were dark-stratified at 3–5 °C for 4 weeks to break dormancy. After that they were incubated at 22 °C for the 14-h light period and 15 °C for the 10-h dark period each day (Hendry and Grime, 1993). Germinated seeds were counted and removed at 2-d intervals for 30 d. Each population consisted of five replicates of 20 seeds for each seed type and each treatment. Each replicate was represented by seeds from a single maternal plant.
Germination was characterized by two variables: first-day and final germination. First-day germination was expressed as percentages of seeds germinated in the dark at 3–5 °C during 4 weeks of cold stratification. As was shown in a previous study, seeds of both types are able to germinate at low temperatures in the laboratory (Mandák et al., 2006b) as well as under field conditions (B. Mandák, pers. obs.). These ‘cold-tolerant’ seeds (see Mandák et al. 2006b) probably establish new populations only during mild winters without frost. Final germination was calculated as cumulative percentages of seeds that were germinated at the end of the experiment. Both variables were tested separately in all analyses. To test whether there are differences in germination between the two regions and to test the effects of seed type and salinity treatment on germination, a mixed-model nested ANOVA was performed with salinity treatment, seed type (B and C) and region (Bohemia and Moravia) as fixed effects, population as a random effect, nested in region and all interactions on both first-day and final germination percentages (Crawley, 2002). In both cases the arcsine transformation [arcsine (%)1/2] of germination percentages was used to meet the assumptions of ANOVA.
To estimate population genetic diversity, percentage of polymorphic loci (PL), average number of alleles per locus (A), observed heterozygosity (Ho) and Nei's unbiased heterozygosity (He; Nei, 1978), were calculated using the program POPGENE (Yeh et al., 1999). To assess inbreeding within populations, Weir and Cockerham's parameter f (Weir and Cockerham, 1984) was calculated for each population with FSTAT (Goudet, 1995; for details, see Mandák et al., 2005).
To reveal the relationships between population genetic parameters and germination characteristics, Spearman rank correlations (rS; calculations being undertaken using the Statistica software; StatSoft, 1998) between particular genetic diversity parameters and mean values of both germination characteristics assessed for particular populations across all treatments, and their combinations were calculated. Further, coefficients of variation of both germination characteristics per population were correlated with all genetic diversity parameters to determine whether less genetically diverse populations were more plastic in germination characteristics or not.
To evaluate the effect of inbreeding on the germination characteristics of different seed types and the effect of a stressful environment (i.e. salinity treatment), populations were assigned to three categories with different amounts of inbreeding as follows: (1) f = −0·20–0·00 (n = 3); (2) f = 0·00–0·09 (n = 2); and (3) f = 0·09– 0·20 (n = 3). The categories were defined so that they included approximately similar numbers of populations. Subsequently, a mixed-model nested ANOVA was performed to test the effect of category of inbreeding, seed type, salinity treatment (fixed effects), population (a random effect, nested in region) and all interactions on both germination characteristics on arcsine-transformed data.
One-way ANOVAs were performed to test whether there are differences between populations in germination from both dormant (B) and non-dormant (C) seed types separately for particular regions (Bohemia and Moravia). If a significant difference between means was found, Tukey's multiple range test was used to perform post hoc pairwise comparisons between individual populations. These statistical analyses were performed using S-PLUS® for Windows (S-PLUS, 1999).
Mixed-model nested ANOVA revealed significant differences in both first-day and final germination percentages between regions (Table 2). Populations from the Bohemian region germinated better (first-day germination: 49·05 ± 3·76 %, final germination: 82·44 ± 2·63 %; mean ± s.e.) than those from the Moravian one (first-day germination: 35·58 ± 3·25 %, final germination: 75·63 ± 3·21 %).
Both germination characteristics were significantly affected by seed type (Table 2) and salinity treatment (Table 2). Non-dormant type-C seeds germinated better (first-day germination 60·25 ± 3·28 %, final germination 93·31 ± 1·25 %) than dormant type-B seeds (first-day germination 24·38 ± 2·63 %, final germination 64·76 ± 3·29 %; mean ± s.e.). Final germination percentages for particular treatments were, in the case of salinity, 43·94 ± 3·62 % for dormant type-B seeds and 88·38 ± 1·93 % for non-dormant type-C seeds, and, in the case of water treatment, 85·58 ± 2·90 % for dormant type-B seeds and 98·24 ± 1·14 % for non-dormant type-C seeds (mean ± s.e.), i.e. salinity treatment decreased germination percentages in comparison with water treatment by about 29·95 % and 25·75 % in first-day germination and final germination, respectively. In the case of final germination, the interaction between seed type and salinity treatment was highly significant (Table 2).
Genetic diversity parameters of particular populations estimated from nine putative allozyme loci are given in Table 1. Two parameters, i.e. mean germination percentages (Table 3) and coefficient of variation (Table 4) for both first-day and final germination, were correlated with population genetic indexes. Across all treatments, the mean germination percentages of both first-day and final germination were negatively correlated with f, i.e. more inbreed populations had lower germinability (Figs 1 and and2).2). Significant correlations were also found for final germination and PL and A (Fig. 2). For the coefficient of variation of first-day germination, positive correlations were found with f and A (Fig. 3); for the coefficient of variation of final germination, a significant correlation for PL and A was found and a marginally significant correlation for f (Fig. 4).
For individual seed types and treatments or their combinations, mainly f was related to germination parameters (Tables 3 and and4).4). While the coefficients of variation for first-day germination were highly positively correlated with f-values for seed types (i.e. B and C) and individual treatments (i.e. water and salinity) and their combinations, final germination did not yield any significant result (Table 4). Nearly the same was true for mean germination percentages (Table 3). The inbreeding coefficient (f) was strongly related with both seed types and treatments or their combinations (Table 3).
Mixed-model nested ANOVA revealed significant differences in first-day germination among categories of inbreeding (Table 5). Final germination was affected by an interaction between the category of inbreeding and seed type and a third-order interaction between the category of inbreeding, seed type and salinity treatment (Table 5). The decrease in first-day germination percentages with the increase in the inbreeding coefficient was more evident in Bohemian than in Moravian populations for both seed types (Fig. 5). However, significant differences between populations were found only for non-dormant seeds in the Bohemian region (one-way ANOVA, d.f. = 3, MS = 0·48, F = 3·04, P = 0·04; Fig. 5A) and not in the Moravian one (one-way ANOVA, d.f. = 3, MS = 0·21, F = 2·65, P = 0·06; Fig. 5B). For populations of dormant seeds, the differences were not significant (i.e. one-way ANOVA, d.f. = 3, MS = 0·22, F = 2·11, P = 0·12 and one-way ANOVA, d.f. = 3, MS = 0·08, F = 0·85, P = 0·48 for the Bohemian and the Moravian region, respectively).
PL and A were significantly negatively related to final germination in dormant type-B seeds and for the dormant B seed × salinity combination (Table 3), i.e. with increasing percentage of polymorphic loci and number of alleles per locus, mean germinability decreased (Table 3). Concerning Ho and He heterozygosity, no significant relationship has been found in germination characteristics for individual seed types and treatments or their combinations; therefore, these data are not shown with the exception of Ho and all treatment combinations (Figs 11–4). For the sake of better understanding of the relationships among the genetic parameters used, correlations among them expressed by Spearman rank correlation coefficients (rS) are given in Table 6.
The results of the present study have shown that germinability of heterocarpic species A. tatarica is influenced as follows: at the species level, individual seed types respond differentially to salt concentration and possess different levels of dormancy, i.e. germination differed significantly between different seed types (B and C) in dormancy and salinity.
At the population level, germinability is affected by individual population genetic parameters in the following ways. (a) For the first time, as far as is known, it has been demonstrated in a heterocarpic species that germinability of both seed types significantly decreases with increasing inbreeding coefficient. (b) Populations with a higher number of alleles expressed as both percentage of polymorphic loci (PL) and average number of alleles per polymorphic locus (A) possess lower germinability, i.e. seeds from populations with a smaller number of random events (i.e. due to founder or bottleneck effects) in their history did not germinate immediately and embody higher levels of dormancy. (c) While particular seed types responded to higher inbreeding in the same way, other population genetic parameters (PL, A) influenced them differently. Therefore the non-dormant type-C seeds were not influenced (probably due to explosive germination under suitable conditions and low or no dormancy regulation), but dormant type-B seeds were in strong correlation with PL and A (Tables 3 and and44).
Plant studies often reveal significant effects of inbreeding on seed set, germination and survival (Keller and Waller, 2002). This is often explained as a result of accumulation of deleterious mutations in populations, and is more pronounced in small populations in which selection is less effective (Lynch et al., 1995). Many studies demonstrated an increase in inbreeding depression in populations with reduced genetic diversity (Ouborg and van Treuren, 1995; Fischer and Matthies, 1998; Frankham et al., 2002; Vergeer et al., 2003; Dittbrenner et al., 2005; Hensen and Wesche, 2006); however, other studies support an alternative scenario based on the assumption of the existence of inbreeding avoidance mechanisms (Barrett and Charlesworth, 1991; Dole and Ritland, 1993; Johnston and Schoen, 1996; Mustajärvi et al., 2005). Theoretical models predict that, in populations which experienced bottlenecks, selection against deleterious recessive mutations should be more effective and such populations thus experience reduced inbreeding depression (Lande and Schemske, 1985).
Highly significant differences between seed types in both germination characteristics across both treatments may point to their different temporal dispersal functions. Whereas most non-dormant seeds finally germinated (93 %), a certain part of dormant ones (35 %), especially under salinity treatment, have stayed dormant. On the other hand, final germination percentages between particular seed types under water treatment (i.e. control) were less pronounced (i.e. 85·58 ± 2·90 for dormant type-B seeds and 98·24 ± 1·14 for non-dormant type-C seeds). Consequently, heterocarpy primarily associated with unpredictable and stressful desert environments (Cohen, 1966; Venable, 1989; Venable and Brown, 1993), where A. tatarica is native, can play an important role in the successful survival of this species in highly temporally variable habitats such as dunghills or road margins in central Europe, where it also occurs (Mandák, 2003b). Further, it has been shown that plants from the Bohemian region germinate better (first-day germination, 49·05 ± 3·76 %; final germination, 82·44 ± 2·63 %; mean ± s.e.) than plants from the Moravian ones (first-day germination, 35·58 ± 3·25 %; final germination, 75·63 ± 3·21 %). While the differences were highly significant in the case of first-day germination percentages (i.e. recorded differences have corresponded to percentages of seeds germinated during a period of cold stratification regime at 3–5 °C), the differences in final germination percentages were less pronounced. This could be explained by distinct selection regimes for cold tolerance and earlier germination in particular regions. In the Bohemian region, where the growing season is shorter by about 14 d (Tolasz et al., 2007), cold-tolerant and early-germinated seeds can be favoured over later-germinated and less cold-tolerant ones in such species as the annual A. tatarica. Successful ripening of A. tatarica, a species with a relatively long ripening period, is therefore limited in the Bohemian region, which is characterized by a shorter vegetation season (J. Kochánková and B. Mandák, unpubl. res.).
For some members of the family Asteraceae, different outcrossing rates have been detected between inner and outer florets, which produce particular seed morphs (Cheptou et al., 2001; Gibson, 2001). In accordance with their different spatially dispersal functions, two conflicting scenarios for the evolution of the mating system dynamic are postulated. The first one is the so-called local adaptation hypothesis which states that selfing in florets producing non-dispersal achenes will generate locally adapted genotypes, whereas progeny from outcrossed florets, producing dispersal achenes, will express greater physiological plasticity, which could be advantageous during colonization of new habitats (Jain, 1976; Schmitt and Gamble, 1990). The opposite pattern in selfing rates is commonly explained by the competition theory which considers that outcrossing in non-dispersal achenes may minimize competitive interactions among siblings (Schmitt and Ehrhardt, 1987). In the case of heterocarpic species, inbreeding may differently influence the fitness of progeny from particular seed morphs (Picó and Koubek, 2003). In a hand-pollination experiment on Leontodon autumnalis, it has been shown that outcrossed central seeds germinated better than selfed central ones, whereas an opposite pattern was exhibited by peripheral seeds (Picó and Koubek, 2003).
In general, it is argued that inbreeding depression is greater in more stressful environments (Armbruster and Reed, 2005) or can differ markedly between a greenhouse and a common garden environment (Dudash, 1990). Negative correlations between mean values of first-day germination percentages of particular populations and f values for most of the treatments and their combinations (Table 3) in the present study suggest that inbreeding evidently affects germination variability in populations of A. tatarica. Moreover, there were highly positive correlations between coefficients of variation of first-day germination percentages and their f values (Table 4) as well as significant differences in first-day germination percentages between categories of inbreeding (Table 5). This significant decrease in germination percentages in populations with a higher inbreeding coefficient supports the occurrence of a certain magnitude of inbreeding depression in populations of A. tatarica. Inbreeding depression at early stages of development, such as in the case of germination, is considered to be a result of recessive alleles of highly deleterious or lethal effects, which could be effectively purged from populations in contrast to mutation load of characters of later life stages, which are often under polygenic control (Husband and Schemske, 1996). Theoretical models predict that inbreeding depression will be less pronounced in populations with a longer history of inbreeding, in which purging is more effective (Lande and Schemske, 1985). It is supposed that the present results are in agreement with this prediction. A positive correlation has been found between the coefficient of inbreeding (f) and allelic richness (A). It is therefore supposed that populations of A. tatarica with lower values of the inbreeding coefficient have relatively low genetic variability caused by more random events in their history. In the case of A. tatarica, the purging effect is most probably realized by strong sibling competition, which has been documented by Mandák et al. (2006a), where significant differences in heterozygosity between particular life stages (i.e. seedlings vs. adult plants) were detected by allozymes. Furthermore, it has been documented that the magnitude of inbreeding depression in autogamous species is on average smaller than in predominantly allogamous ones (Husband and Schemske, 1996). Atriplex tatarica is a highly autogamous species with a relatively high amount of population differentiation in comparison to other species with a mixed-mating system (Mandák et al., 2005). Therefore, the existence of effective purging in populations of this species is expected.
It has been shown that germination of the heterocarpic species A. tatarica differed significantly between different seed types in dormancy and salinity. Moreover, germination correlates with basic population genetic parameters. Germination of both seed types decreases with increasing inbreeding coefficient, i.e. with an excess of homozygotes in a population, and with a higher amount of alleles expressed as both percentage of polymorphic loci (PL) and average number of alleles per polymorphic locus (A). However, individual seed types were not influenced by population genetic parameters in the same way. While non-dormant type-C seeds were not strongly influenced by PL and A, dormant type-B seeds strongly correlated with PL and A. In general, type-C seeds are non-dormant, and their germination is probably not under strong genetic control. Hence, they germinate as soon as conditions are favourable, thus ensuring survival in the short term (Mandák and Pyšek, 2001b), but populations risk local extinction if conditions then become adverse (i.e. it is a high-risk strategy; Venable, 1985). In contrast, germination of the dormant type-B seeds is under stronger genetic control and is significantly correlated with basic population genetic parameters. These seeds ensure long-term reproduction and survival in the field by protracted germination, albeit in low quantities (i.e. A. tatarica also adopts a low-risk strategy; Venable, 1985).
We would like to thank Phil Gibson, Frederic Rooks and two anonymous reviewers for their helpful comments on earlier drafts of the manuscript. This study was supported by grant no. IAA600050707 from the Grant Agency of the Academy of Sciences of the Czech Republic and grant no. 41110/1312/3113 from the Grant Agency of the Czech University of Life Sciences Prague.