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Population Biology |
ina Bímová
ková
2Institute of Botany, Academy of Sciences of the Czech Republic, CZ-252 43 Pr
honice, Czech Republic; and
3Institute of Applied Ecology, Czech Agricultural University Prague, CZ-281 63 Kostelec nad 
ern
mi lesy, Czech Republic
Received for publication November 30, 2005. Accepted for publication September 8, 2006.
ABSTRACT
Atriplex tatarica is a heterocarpic species of disturbed habitats. Seeds of Atriplex tatarica do not germinate immediately after shedding, but may remain in a dormant but viable state indefinitely. We investigated whether there were genetic and fitness differences between plants derived from seeds of the different fruit types germinated in different temperatures and salinities. Seeds that germinated in optimal and suboptimal conditions differed significantly in their genetic composition due, in part, to their source population. Seeds that germinated in the suboptimal conditions produced more homozygous plants. Plants that were primarily heterozygous were generated from nondormant fruit types as well as from fruits that germinated in the optimal conditions. Moreover, there was a positive correlation between the degree of heterozygosity and plant fitness measured as the mass of the stem and reproductive structures. In conclusion, the genetic variation of natural populations may be at least partly due to the ability of particular seed genotypes to germinate in the specific environmental conditions of a particular locality. In some circumstances, the process of differential germination may select not only for genetic variability but also for higher fitness if heterozygosity-fitness correlations are present.
Key Words: allele frequencies • Atriplex tatarica • Chenopodiaceae • fitness • heterozygosity • salinity • seed bank • temperature
Seed dormancy is suspected to be an adaptation that reduces competition among siblings and contributes to the persistence of plant populations (Venable, 1989
). While many investigations of the distribution of genetic variation have focused on aboveground plant populations (reviewed in Loveless and Hamrick, 1984; Hamrick, 1989
; Heywood, 1991
; Hamrick and Godt, 1996
), there are several empirical studies on the distribution of genetic variation in the populations of seed banks (Tonsor et al., 1993
; Cabin, 1996
; Cabin et al., 1998
; McCue and Holtsford, 1998
; Schneller, 1998
; Morris et al., 2002
; Koch et al., 2003
; Mandák et al., 2006
). For example, Cabin (1996)
found significant genetic differences between the above- and belowground plant populations, suggesting that the distribution of genetic variation may differ across these life-history stages. Furthermore, using starch gel electrophoresis, Cabin et al. (1997)
were the first to demonstrate experimentally that the timing of germination and environmental conditions could significantly affect the genetic structure of emerging plant populations. They showed that germination and survival behavior might play an important role in the generation and maintenance of the genetic structure of natural plant populations and species evolution.
Alternatively, if genotypes in the seed bank are adapted to past rather than present environmental conditions, reintroduction of genotypes could actually act as a genetic load on the population and retard evolutionary change (Templeton and Levin, 1979
; McCue and Holtsford, 1998
). Although studies on the genetics of seed germination and seed bank composition are relatively rare, results do suggest that seed germination in different environmental conditions could dramatically alter the genetic diversity of plant species.
The correlation between fitness components and the level of genetic variation is much disputed. Because loss of genetic diversity may be related to inbreeding and inbreeding may reduce reproductive fitness, a correlation is expected between heterozygosity and fitness. This correlation is ultimately influenced by the degree to which enzyme variants are adaptive or neutral. Several studies suggest that allozyme heterozygosity is a good measure of population fitness and adaptive potential (Houle, 1989
; Lönn et al., 1996
, 1998
), whereas others argue that such molecular data reflect only a small portion of the genome and thus may not be a good indicator of adaptive genetic differences (Reed and Frankham, 2001
, 2003
). Mitton and Grant (1984)
showed that at least some enzymes could be under direct selection. In plants, Pgi allozymes have been found to be associated with oxygen availability (Zangerl and Bazzaz, 1984
), plant community composition (Prentice and Cramer, 1990
), soil type (Nevo et al., 1981
), latitude and altitude (Weber and Stettler, 1981
), soil moisture and pH (Prentice et al., 1995
), flooding (Lönn et al., 1998
), and seed set in different microhabitats (Lönn et al., 1996
). Therefore, allozymes could be a particularly useful tool for studying selection under various environmental situations and in particular, how environments influence the genetic composition of seed bank populations.
Atriplex tatarica is an annual herb found in manmade habitats of Central Europe. A fraction of A. tatarica seeds do not germinate immediately after dispersal, but may remain indefinitely in a dormant but viable stage. Seeds from different heterocarpic fruits have diversified patterns of dormancy and germination (Mandák, 2003b
). In this study, we investigated the extent to which seed genotypes from particular fruit types of Atriplex tatarica differentially germinate and become established. We ask (1) are there genetic differences between populations derived from seeds of different fruit types; (2) do these seeds germinate in the different ecological conditions; (3) does the genetic composition of seeds influence germination and (4) is this association accompanied by differences in individual reproductive fitness?
MATERIALS AND METHODS
Study species
Atriplex tatarica L. (syn. A. laciniata L., A. sinuata Hoffm., A. veneta Willd.) (Chenopodiaceae) is one of two annual, heterocarpic, diploid species of the section Sclerocalymma Aschers. in the Czech Republic (Mandák, 2003a
). The native distribution covers Central Asia, Asia Minor, southwest Siberia, North Africa and Eastern Europe where it occurs in salt steppe and disturbed habitats (Aellen, 1960
; Meusel et al., 1965
). From the area of native distribution, the species has spread to Central and Western Europe (Aellen, 1960
). The northwestern border of its continuous and probably native European distribution lies partly in the Czech Republic (Jalas and Suominen, 1988
). Atriplex tatarica is an early successional species, often dominant in the first 2 or 3 years of succession, prefers nitrogen-rich soils, and tolerates a high level of NaCl (Mandák, 2003b
).
This species possesses heterocarpy, which is morphologically expressed by bracteole shape and size, fruit size, and color. Atriplex tatarica is characterized by the presence of two fruit types (B and C) (type A fruits originate from female or bisexual ebracteate flowers enclosed within a five-lobed perianth and are found only in members of section Dichosperma Dumort.) (Mandák, 2003b
). Female bracteate flowers produce both type B and C fruits. Type B fruit is a small black achene with glossy, smooth testa enclosed within small bracteoles. Type C is brown and rather large, covered by extended bracteoles. While seeds from type B fruits are dormant and require stratification for successful germination (forming a persistent seed bank), seeds from type C fruits are nondormant and germinate readily when conditions are optimal (forming a transient seed bank; Mandák, 2003b
). In general, the production of type B fruit favors later germination with lower survival risk, in contrast to type C, which favors earlier germination with associated survival risk. Thus, heterocarpy, by which fruit types have a distinct ecological behavior, enables colonizing species such as A. tatarica to survive both major disturbances (by ensuring that some seeds persist) and unfavorable conditions (by spreading germination over a long period) (Mandák, 2003b
).
Germination experiment
Fruits of Atriplex tatarica were collected at the end of October 2003 from a population growing in a waste place in South Moravia, Czech Republic (48°49'08'' N, 16°44'52'' E), where considerable allozyme variability was found in a previous study (Mandák et al., 2005
). The fruits were separated from the bracts, sorted according to fruit type, i.e., B and C, and stored in the dark at room temperature in the laboratory in paper bags until April 2004. The identity of the maternal plant was not maintained.
Germination of seeds from the different fruit types (B and C) was separately tested in the different (1) temperatures, and (2) NaCl concentrations. Using this procedure, we divided seeds from the two fruit types into groups that were tolerant or nontolerant to temperature or salinity. They were then left to grow to maturity in the experimental garden and tested for differences in both genetic (allele frequencies and heterozygosity; Appendix 1, 2) and phenotypic (mass) characteristics.
Germination experiments were carried out to test for differences in allele frequencies and heterozygosity of plants grown from seeds germinated from different fruit types in the temperature and salinity treatments to obtain temperature- or salinity-tolerant and nontolerant seeds. The fruits were placed in 10 cm-diameter petri dishes on a single layer of filter paper, wetted with 20 mL of water (temperature treatment) or 1% aqueous sodium chloride solutions (salinity treatment), and incubated in the dark at 5°C for 4 weeks to break dormancy (see Mandák, 2003b
). Each experiment consisted of 25 replicate dishes of 20 fruits for each fruit type (placed separately on petri dishes) and treatment, i.e., 500 fruits for each fruit type and germination treatment combination.
For the temperature treatment after the dormancy-breaking period, the temperature was slightly increased to 10°C for the 14-h light period and 5°C for the 10-h dark period. Seeds that germinated within 2 days of this cold treatment were classified as "cold tolerant." Based on a previous experiment (B. Mandák, unpublished data) under low temperatures, only a few seeds are able to germinate while the rest remain dormant. After 2 days, the temperature was increased to 22°C for the 14-h light period and 15°C for the 10-h dark period to obtain seeds that were then classified as "cold nontolerant." A salinity treatment was used to examine the importance of soil salinity for determining the genetic structure of seed populations that are able to germinate in the high (1%) and low (0%) salinity concentrations (optimal salinity concentration was determined in previous germination experiments; Mandák, 2003b
). After the dormancy-breaking time the temperature was increased to 22°C for the 14-h light period and 15°C for the 10-h dark period each day (see Hendry and Grime, 1993
). Seeds germinating in the high salinity concentration within the first 2 days were classified as "salinity tolerant." In previous experiments (Mandák, 2003b
), all seeds that were able to germinate under saline conditions germinated within the first 2 days, while the rest of the seeds remained dormant for 21 days. After 2 days, the NaCl solution was replaced by distilled water and all seeds that started to germinate were classified as "salinity nontolerant." The viability of ungerminated seeds was not determined.
Genetic analysis
One hundred germinated seeds from each fruit type–germination treatment combination were then randomly selected and transplanted to plastic flats filled with commercial potting compost. Seedlings were left to grow for 10 days in an experimental garden and then 50 seedlings of each fruit type and germination treatment combination were randomly selected and transplanted into 6.9 L pots filled with a potting soil. These plants were used for further analysis. In total, 400 plants of A. tatarica were planted in randomized block design with 50 replicates. After 2 months, a young, expanded leaf of each plant was analyzed for four enzymes and seven polymorphic loci by gel electrophoresis as described in Mandák et al. (2005)
. The following enzyme systems were assayed: Lap-1, Lap-2, Mdh-1, Mdh-3, Sod-4, Sod-3, and Skdh-1.
Fitness measurement
At the end of the growing season (14–20 September 2004), half of the experimental blocks were randomly selected, and all plants from the randomly selected blocks were harvested. Harvested plants were divided into reproductive (bracteoles and fruits) and vegetative (leaves and stem) mass. The mass of the stem and reproductive structures was weighed separately (±0.0001 g), after oven drying for 2 days at 60°C. We harvested 25 plants for each combination of temperature (tolerant vs. nontolerant) and salinity (tolerant vs. nontolerant) treatments and fruit types (B and C), i.e., 200 plants in total.
Relative fitness of a plant was the mean seed mass produced by the plant divided by the maximum seed mass produced by a plant.
Statistical analyses
To estimate genetic diversity, a locus was considered polymorphic if the frequency of the most common allele did not exceed 0.95. Allele frequencies, observed heterozygosity (Ho), and Nei's (1978)
unbiased heterozygosity (He) were estimated using the Tools for Population Genetic Analyses (TFPGA) program (Miller, 1997
).
Log-linear analyses (Caswell, 2001
) were used to determine the effects of fruit type (type B vs. C fruits) and germination treatment (tolerant vs. nontolerant seeds) on allele frequencies and heterozygosity among plants grown from seeds in the different temperature and salinity experiments. The data were arranged in a three-way contingency table consisting of fruit type (F), germination treatment (T) and the number of copies of each allele (A) in the sample. In the present context, the response variable is allele frequency (A), and the sources of variation are fruit type (F) and the germination treatment (T). Following the conventional notation of hierarchical models used by Caswell (2001)
, Horovitz and Schemske (1994)
, and Cabin et al. (1997)
, alleles (A) were distributed into fruit type and germination treatment categories. Thus the null model FT A ensures that allele frequency is independent of fruit type and germination treatment, given possible fruit type (F) x germination treatment (T) interactions.
Hypotheses are tested with likelihood ratio tests. The goodness-of-fit of a model is tested by comparing it to the appropriate null model (FT A). The resulting log-likelihood ratio G2 is asymptotically distributed as 
2 with degrees of freedom equal to the number of parameters excluded from the model being tested. Hypotheses about particular factors (F and T) and their interactions are tested by the likelihood ratio of two models that differ by only those terms. This likelihood ratio statistic is given by the difference of goodness-of-fit G2 values for the two models, and is distributed as 2 with degrees of freedom equal to the difference in the degrees of freedom for the two models (Caswell, 2001
). Because both marginal and conditional G2 analyses yielded very similar results, here we report only the results of the slightly more conservative marginal tests.
Heterozygosity was tested the same way, but the term allele was replaced by single-locus heterozygosity for the first analysis (the number of individuals heterozygous and homozygous at each locus), and multilocus heterozygosity for the second analysis (the number of heterozygous loci per individual). Heterozygosity was expressed as the number of heterozygous loci out of the set of seven loci. Correlations between heterozygosity and particular fitness components were then calculated with a Spearman rank correlation on untransformed data. Relative fitnesses were compared using Mann–Whitney U tests (all analyses computed with Statistica software; StatSoft, 1998
). The log-likelihood statistics for all analyses were computed using the loglinear analysis option of the Statistica software (StatSoft, 1998
).
RESULTS
Germination and survival
Seeds of Atriplex tatarica germinated in lower numbers in both the lower temperature and high salinity concentration as opposed to the higher temperature and nonsaline concentration (Fig. 1). The mean germination for all fruit types and treatments combined was 51.0% and ranged from 20.4% (C cold-tolerant seeds) to 88.7% (C cold-nontolerant seeds). Overall, germination of seeds from particular fruit types in the salinity and temperature experiments ranged from 75.2% (type B fruit in the salinity experiment) to 91% (type C fruit in the temperature experiment). As expected, germination differed significantly between seeds produced by different fruit types (i.e., B and C) within temperature (seeds produced by type C fruit germinated better than those from type B fruit; Mann–Whitney U test; Z = 4.87, P = 0.00001) and within salinity (seeds produced by type C fruit germinated better than those from type B fruit; Z = 3.59, P = 0.0003) experiments. The survivorship of seedlings was relatively high, averaging 76.8% over all treatment combinations (Fig. 1).
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The observed patterns of genetic composition of Atriplex tatarica populations grown from different fruit types with different germination treatments in the different temperature and salinity conditions suggest several outcomes. (1) Seed genotypes may respond differentially to environmental variation through the germination and establishment process (see also Cabin et al., 1997
). Seeds germinated under harsh and optimal conditions, i.e., temperature- or salinity-tolerant and nontolerant seeds, differed significantly in the genetic constitution of their source populations. For example, seeds that tolerated low temperatures produced more homozygous plants. (2) Plants with the highest number of heterozygous loci may possess higher fitness than plants that are primarily homozygous (Fig. 3). Although the relationship between allozyme heterozygozity and fitness has been documented (see Lönn et al., 1996
, 1998
; Luijten et al., 2000
; Stilwell et al., 2003
), our results are the first for plant populations grown from seeds germinated under experimental treatments that mimic natural selection. Positive relationships between allozyme heterozygozity and fitness were not obtained, however, for all the experimental combinations (see Figs. 4, 5). Only salinity nontolerant and cold-tolerant seeds had a positive relationship between heterozygozity and reproductive mass (and vegetative mass in the salinity nontolerant seeds). Therefore, only some selection regimes can produce bigger and more fecund plants with higher fitness.
A number of factors may have influenced the results obtained in this study. First, the activity of some enzyme systems may be modified, qualitatively and quantitatively, during a plant's life cycle (Johnson, 1974
; Wendel and Weeden, 1989
). These modifications are related to certain physiological and ecological factors, such as flowering, senescence, pathogen attack, or extreme temperatures. Furthermore, estimates may be biased if protein extractions are performed on samples of tissue collected at different stages of plant development (Wendel and Weeden, 1989
). To avoid this, leaves sampled in our study were collected at the same stage of development from plants cultivated under the similar conditions in an experimental garden. We believe that our banding patterns are repeatable when compared to a previous study (Mandák et al., 2005
) that used plants from the same locality as this study.
Second, seeds produced by particular fruit types differed in their germination patterns (Fig. 1). While we were able to establish plants from most seeds of type C fruits, a smaller proportion of the seed from type B fruits was used in this study due to limitations caused by dormancy. Hence, our results could be influenced by a bias in the differential establishment rates of seeds from different fruit types under various treatments. The same problem was encountered by Cabin et al. (1997)
in their work with Lesquerella fendleri. They pointed out that this possibility is to some extent a technical issue, because seedlings must grow large enough to electrophorese and many plants experience some degree of early mortality. On the other hand, the use of small seedlings is impossible because of the low enzyme activity in this life stage as found in Atriplex tatarica.
Further, our results may be influenced by the effect of interactions among seed genotypes, maternal seed maturation conditions, and the experimental treatment (Baskin and Baskin, 1998
). Maternal effects could strongly influence the germination and establishment of progeny in our study (see Roach and Wulff, 1987
). A consistent trend has been found in the Asteraceae (Baker and O'Dowd, 1982
; Venable and Levin, 1985
; Kigel, 1992
). Under unfavorable conditions, plants tend to produce more seeds with low dispersibility, low germinability, and a high level of dormancy. Such seeds may cause bias in many ecological studies because maternal effects cannot be separated from direct environmental factors. Mandák and Py
ek (1999
, 2005
) found that particular fruit types produced by Atriplex sagittata responded to the conditions under which the maternal plants grew in a different way. Whereas the nondormant fruit type was unaffected by the treatments imposed on the maternal plant, the germination of the dormant types changed considerably. Hence, to avoid among-habitat variation in seed quality due to maternal environmental effects, we used fruits only from a locality with relatively homogenous environmental conditions and believe that any such variation will have been kept to a minimum.
Important consequences in plant population genetic structuring and evolution have been attributed to seed banks, spatial patterns of seed dispersal, and patchy distribution of suitable habitats for plant establishment (Loweless and Hamrick, 1984
; Hamrick, 1989
; Alvarez-Buylla et al., 1996
). A number of environmental factors (e.g., light quality, soil moisture, and temperature) have been shown to influence the seed germination response (Baskin and Baskin, 1989
). If seed genotype reacts specifically to spatial and temporal environmental variation (see Kalisz, 1991
), then the germination response is under strong selection and may be an important determinant of the genetic structure of aboveground populations (Tonsor et al., 1993
; Cabin, 1996
; Cabin et al., 1998
). When seed germination has an important influence on the genetic structure of plant populations via diverse success of various seed genotypes to environmental conditions, then nonrandom distribution of genetic variability has to be found in many mature plant populations (see Nevo, 1988
; Hamrick, 1987
, 1989
). Hence, seed dormancy could function as a kind of sieve, screening when and where particular seed genotypes germinate and establish in the soil (Cabin, 1996
). This differential germination and establishment of seed genotypes in response to spatial and temporal environmental variation leads to the presence of dormant seeds in a seed bank. In the case of A. tatarica, different field conditions at the time of germination will probably lead to various site-specific population genetic structures of the standing plant populations and also to genetic differences between seeds remaining dormant in the soil and those that form the aboveground populations. Similarly, Cabin (1996)
also found differences in allele frequencies and distribution of multilocus heterozygosity between seedlings and seeds. Furthermore, Tonsor et al. (1993)
in their study of Plantago lanceolata showed how allele frequencies differed between seeds in the seed bank and adult plants. Thus, seedlings represent a nonrandom genetic subset of a population soil seed bank that may have evolved by differential germination of particular seed genotypes.
For heterocarpic species, there is a considerable variation, both genetic and environmental, in the expression of dormancy. That is, within a population of seeds produced by different fruit types, some seeds may germinate, whereas other viable seeds in the same environment remain dormant in the soil (Mandák and Pyek, 2001
; Mandák and Holmanová, 2004
). As a result, there is considerable variation among seeds in the timing of germination and in the environment in which germination and establishment occur. In A. tatarica the seeds react to environmental conditions in different ways as we can see in germinability of type B and C fruits in both the temperature and salinity treatments (see Fig. 1). Understanding the cause of this variation is critical, because germination timing and response to the environment in which seeds emerge are of overriding importance for subsequent plant performance and success (Harper, 1977
).
In Atriplex tatarica, we found a positive correlation between heterozygosity and plant fitness components. Heterozygous plants were generated primarily by type C fruit and fruits that were germinated under optimal conditions. These plants were also more fecund, i.e., selection for nontolerant, late germinating seeds within particular fruit types that possess higher fitness was detected. Essentially, seed heteromorphism represents a mixed strategy reducing temporal variance in fitness. For this reason, seed polymorphic species such as A. tatarica mainly inhabit unpredictable (deserts or semi-deserts) or highly disturbed (human-made habitats) environments. The main consequences of seed heteromorphism have been clearly formalized within the high risk/low risk strategy by Venable (1985)
, i.e., one morph germinates immediately when favorable conditions occur, while the second morph shows delayed germination. Therefore, A. tatarica is a typical species with a high risk/low risk strategy inhabiting highly disturbed habitats (Mandák, 2003a
, b
). Hence, there is a high probability that most cold-tolerant seeds, i.e., seeds that germinate first in spring, will be destroyed by early spring frost, and thus more homozygous plants able to germinate at low temperatures will be constantly eliminated from populations. The same situation can be with salinity-tolerant seeds and seedling survival in the high salinity concentration. Mandák et al. (2005)
showed that the genetic structure of A. tatarica populations corresponds much more to species with a predominantly mixed-mating system in spite of generally high levels of autogamy in members of Chenopodiaceae (see Hamrick and Godt, 1996
). Accordingly, we believe that differential responses between and within seeds of heterocarpic fruits could be important in generating and maintaining genetic population structure and thus principally act in species evolution.
In summary, the genetic variation of natural populations may be in part due to the ability of particular seed genotypes to germinate under specific environmental conditions that differ between localities. In some circumstances, the process of differential germination may select not only genetic variability but also higher fitness of selected plants if the heterozygosity–fitness correlations are present.
APPENDIX 1.
Estimated allele frequencies at seven polymorphic loci in four experimental populations of Atriplex tatarica germinated in the temperature treatment (see Materials and Methods). Expected heterozygosity = Nei's unbiased heterozygosity; —, allele absent in sample. Asterisks indicate significant departures from the expected Hardy–Weinberg heterozygosity frequencies: ** P < 0.01, *** P < 0.001
APPENDIX 2.
Estimated allele frequencies at seven polymorphic loci in four experimental populations of Atriplex tatarica germinated in the salinity treatment. Expected heterozygosity = Nei's unbiased heterozygosity; —, allele absent in sample. Asterisks indicate significant departures from the expected Hardy-Weinberg heterozygosity frequencies: * P < 0.05, *** P < 0.001
FOOTNOTES
1 The authors thank J. P. Bailey and J. Haught for editing the English; G. P. Cheplick and M. Lönn for helpful comments and suggestions; K. B. Sramek de Kott for help with isozyme electrophoresis; and J. Douda, J. Kochánková, V. Kos, J. Mayová, M. Poustková, and K. Procházková for considerable help in the garden and lab. This study was supported by grant no. IAA6005206 from the Grant Agency of the Academy of Sciences of the Czech Republic. Further support was provided by the Academy of Sciences of the Czech republic (grant no. AV0Z60050516). 
4 Author for correspondence (mandak{at}ibot.cas.cz
)
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