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Bryology and Lichenology |
2 Institute of Systematic Botany, University of Zürich, Zürich, 8008, Zollikerstrasse 107, Switzerl 3 Eötvös Loránd University, Department of Plant Taxonomy and Ecology, Budapest, 1117, Pázmány Péter s. 1/C, Hungary 5 Duke University, Department of Biology, 139 Biological Sciences Building, Box 90338, Durham, North Carolina 27708 USA
Received for publication 12 September 2007. Accepted for publication 24 February 2008.
ABSTRACT
Propagule banks are assumed to be able to store considerable genetic variability. Bryophyte populations are expected to rely more heavily on stored propagules than those of seed plants due to the vulnerability of the haploid gametophyte. This reliance has important implications for the genetic structure and evolutionary potential of surface populations. A liverwort, Mannia fragrans, was used to test whether the bryophyte diaspore bank functions as a "genetic memory." If a diaspore bank is capable of conserving genetic variability over generations, the levels of genetic diversity in the soil are expected to be similar or higher than at the surface. Surface and diaspore bank constituents of two populations of M. fragrans were investigated. Genetic structure and diversity measured as unbiased heterozygosity were analyzed using three ISSR markers. Similar genetic diversities were found in the soil (Hs = 0.067) and at the surface (Hs= 0.082). However, more haplotypes and specific haplotype lineages were present in soil samples. The results suggest that the bryophyte diaspore bank has an important role in accumulating genetic variability over generations and seasons. It is postulated that the role of the diaspore bank as a "genetic memory" is especially important in species of temporarily available habitats that have long-lived spores and genetically variable populations.
Key Words: Aytoniaceae • bryophytes • dynamics • genetic memory • inter sequence simple repeat markers • Mannia fragrans • propagule bank • seasons • surface
In seed plants, seed dispersal is not always immediately followed by germination, leading to the development of soil propagule banks (Thompson et al., 1997
). Although little is known about dormancy in bryophytes to date (During, 1979; Miles and Longton, 1992), many species rely on large and persistent diaspore banks. These banks are understood to play a particularly important role in the dynamics of populations of species adapted to habitats with great environmental fluctuations (During, 1997, 2001).
As a result of the influence of the reproductive system, dispersal characteristics, and habitat dynamics, the genetic structure of plant populations is generally nonrandomly distributed (Loveless and Hamrick, 1984). Propagule banks also have a significant impact on the genetic patterns of surface populations (Levin, 1990; McCue and Holtsford, 1998). They may function as a "genetic memory," accumulating and storing propagules formed during different years and under potentially different environmental conditions (Cabin, 1996; Cabin et al., 1998). The genetic structure of the propagule bank affects the genetic and demographic structure and evolutionary potential of subsequently developing populations at the surface (Cabin et al., 1998; Nunney, 2002). Propagule banks may also increase effective population size and help to restore genetic variation when the size of the established populations is considerably reduced (Nunney, 2002). In the same way, they may also be a source of genetic novelty, containing genotypes absent at the surface (Uehara et al., 2006). As dynamic systems, propagule banks are coupled with surface populations and respond to environmental variations and changes in population parameters (Koch et al., 2003). Thus, the spatial genetic structures of the propagule banks and populations at the surface are often mutually dependent (Cabin, 1996; Cabin et al., 1998).
In species relying on large propagule banks, a comparison of the genetic structure at the surface and in the diaspore bank is important because it allows better understanding of the dynamics and genetic history of populations (e.g., Reid et al., 2002; Berg, 2005). During the past few years, comparative analysis of the genetic variability above- and belowground has become an advancing field in seed bank research (Bennington et al., 1991; Tonsor et al., 1993; Cabin et al., 1998; Alvarez-Buylla et al., 1996; McCue and Holtsford, 1998; Mahy et al., 1999; Nunney, 2002; Koch et al., 2003; Barrett et al., 2005; Shimono et al., 2006), but the results do not yet allow for general conclusions. Compared to seed banks, the dynamics and role of the bryophyte diaspore bank have received less attention (During, 1997, 2001). A parallel that both seed banks and bryophyte diaspore banks conserve considerable genetic diversity was proposed relatively early (During, 1997), but this issue has not yet been assessed experimentally. Considerable differences exist between bryophytes and seed plants in terms of life history, breeding system, and reproductive modes. More specifically, the maintenance of bryophyte populations is expected to rely more heavily on propagules stored in the diaspore bank compared to the majority of seed plants for two reasons. First, because bryophyte gametophytes have almost no buffering capacity against environmental stochasticity, they are more vulnerable than the sporophytes of seed plants (Proctor, 2000). This vulnerability leads to intensive variability in spatial and temporal dynamics in bryophyte populations (Lloret, 1994; During and Lloret, 1996). Second, bryophyte gametophytes are haploid and directly exposed to selection. As a consequence, the variability of genes under natural selection may be considerably reduced (Stenøien, 1999; Stenøien and Såstad, 2001). In such a haploid system, where the sheltering of deleterious alleles is absent, the propagule bank may form a rich pool of adaptive genetic diversity. Thus, the diaspore bank may have a far more important role as a reservoir of genetic variability in bryophytes than in seed plants (During, 2001).
The presence of a diaspore bank functioning as a long-term genetic memory is especially probable in species such as colonists or shuttle species that rely on large, longer-lived diaspore banks (sensu During, 1992). If a diaspore bank is able to maintain genetic diversity, the levels of genetic diversity belowground are expected to be similar or higher those at the soil surface (Mahy et al., 1999). In addition, the accumulation of the products of several mating events should increase the amount of genetic variation stored in the soil (Barrett et al., 2005; Shimono et al., 2006).
This study aims to develop a better understanding of the role of bryophyte diaspore banks in influencing the evolutionary potential of surface populations and to investigate whether, similarly to the seed banks, the bryophyte diaspore banks act as a genetic memory. Using ISSR (inter simple sequence repeat) markers, we analyzed the relationship between the genetic composition of diaspore banks and surface populations.
MATERIALS AND METHODS
Model species and study sites
The scented liverwort, Mannia fragrans Balb. Frye & L. Clark, was used as a model species for several reasons. First, its large spores (Damsholt, 2002) are assumed to be long-lived (Inoue, 1960; Hock, 2003), and they form large, persistent diaspore banks (Hock, 2003). Second, the species inhabits open grasslands, where the diaspore bank is supposed to play a great role in (re)colonization. Because of the unpredictable formation of suitable microsites and predictable seasonal alternation of favorable vs. arid periods, the species is episodic, with a large number of new thalli emerging in spring and autumn and numerous thalli dying during the unfavorable winter and summer seasons (Schuster, 1992). The selected populations are known to be genetically polymorphic (Hock, 2007). Analyses were conducted in two Hungarian populations of M. fragrans (Hock, 2007): Population 1 (Vértes Mountains, N 47°31'21'', E 18°29'57'') and Population 2 (Mecsek Mountains, N 46°06'09'', E 18°12'27''). The two sites are separated by ca. 250 km.
Sampling and DNA analysis
To explore the dynamics of the genetic composition in the diaspore bank and at the surface, we sampled seasonally during periods favorable for spore germination and thallus growth. Sampling took place three times: (1) November 2004, preceding the production of new spores, (2) April 2005, immediately following spore dispersal, and (3) November 2005. Mannia fragrans formed distinct patches (patch = well-delimitated group of 10 or more thalli) of 3–15 cm in diameter in both populations investigated. All patches were sampled and marked within a sampling area of about 600 m2 in both populations. Depending on patch size, 3–5 plants were taken from each patch (Table 1). Soil samples were taken from the immediate vicinity of each patch (volume ca. 200 cm3 and depth ca. 3 cm). Soil samples were sieved in the laboratory to exclude living fragments of thalli. The samples were cultivated as in Hock et al. (2006). Thalli germinated from spores were grown until they had reached a minimum size of 1 cm (usually after 3.5–4 mo). After this period, all individuals were harvested (Table 1) and cleaned using a dissecting microscope. Soil particles were removed by stirring the thalli in sterile deionized water using a magnetic stirrer.
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). Because ISSRs are dominant genetic markers that amplify DNA of mixed species, fungal DNA could bias the results of this study. To minimize this possibility, we ran preliminary studies to detect any endophytes in the model species (Zs. Hock, unpublished data). Although no endophytes have been described in M. fragrans (Ligrone et al., 2007), our preliminary studies revealed their presence in its rhizoids (Hock, 2007). However, young apical innovations were always found to be free of fungi. For this reason, rhizoids and ventral scales were removed, and only the young, apical parts of the plants were used. If necessary, plants were cultivated (Hock, 2007) to obtain new apical innovations.
DNA was extracted using the Qiagen (Basel, Switzerland) Dneasy Plant Mini Kit following the manufacturer’s instructions with a modified final step because of the small amounts of plant material. To concentrate the samples, instead of eluting the DNA with a small volume of elution buffer, we washed spin columns twice with 100 µL ddH2O to elute the DNA. Water was then evaporated using a vacuum concentrator, and the DNA was diluted with 30 µL AE buffer. For further analyses, ISSR markers were chosen because of their reliability and success found in other population studies (Wolfe and Liston, 1998; Gunnarsson et al., 2005; Hassel et al., 2005). During preliminary studies, three primers from the whole UBC ISSR primer set (UBC, Vancouver, British Columbia, Canada) yielded satisfactory results (Table 2).
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Soil samples from Population 1 and Population 2 at the first and second sampling dates, respectively, were subjected to fungal infestation. In these cases, hyphae overgrew the surface of the soil samples, killing emerging plants. These samples were hence excluded from further analysis.
Data analysis
Henceforth, the population components (at the surface and in the diaspore bank) will be referred to as stages. Genetic variation at the level of sampling date and stage was investigated with a nested analysis of molecular variance (stages nested within sampling dates; AMOVA, Excoffier et al., 1992). Levels of genetic differentiation were measured by FCT, FSC, and FST, referring to the differentiation among sampling dates, between stages within sampling dates and within stages, respectively. Levels of significance were determined by computing 1000 random permutation replicates.
To test for differences in allelic composition between stages at a given date and among samples from different sampling dates, we ran an exact test of population differentiation (Raymond and Rousset, 1995) with the program TFPGA (version 1.3; Miller, 1998), using 1000 dememorization steps, 20 batches, and 2000 permutations per batch. This test applies to a contingency table (Fisher’s RxC test) and a Markov chain Monte Carlo approach to determine whether significant differences in allele frequencies exist between stages or seasons. The exact test of population differentiation was also applied to test differences in the haplotype composition. For this purpose, ARLEQUIN version 3.01 was used (Excoffier et al., 2005).
To compare genetic diversity between stages, we estimated standard genetic indices (i.e., number [S] and percentage of polymorphic loci (Pp), average gene diversity over loci (Hs; Nei, 1987), average haplotype diversity (hs; Nei, 1987; haplotype = a specific combination of the bands yielded by the three primers used) and the occurrence of private and rare haplotypes and alleles). Analyses were performed using the programs ARLEQUIN version 3.01 (Excoffier et al., 2005) and GenAlEx version 6 (Peakall and Smouse, 2006). For assessing the significance of the differences in Hs, samples were randomized among the different stages/seasons using the program FSTAT version 2.9.3 (Goudet, 2001). Hs was then calculated from the randomized data set. The P-value of the test reflects the proportion of randomized data sets giving a larger difference in Hs values than in the observed ones.
At the patch level, exact tests of population (Raymond and Rousset, 1995) differentiation were applied to test for differences in allele and haplotype frequencies between the two stages using the programs TFPGA version 1.3 (Miller, 1998) and ARLEQUIN 3.01 (Excoffier et al., 2005), respectively. Test parameters for the former were the same as those described for the population-level comparisons. Because the number of samples from a single sampling date was too low for statistical analysis, samples from two collecting dates were pooled (for Population 1, samples 2 and 3 were pooled, and for Population 2, samples 1 and 3 were pooled.)
RESULTS
The genetic variance within the stages accounted for 95–98% of the overall variance at each site (Table 3). Different stages accounted for only 3–8% of the overall variance. There were no differences among sampling dates. Negative variance components obtained reflect the observation that individuals from different dates were more closely related to each other than individuals within samples from the same dates.
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The results of the current study support the hypothesis that the diaspore bank of bryophytes, similar to the seed bank of vascular plants, plays an important role in conserving local genetic diversity. This role is an important new aspect of bryophyte population biology that has been neglected to date, probably because of technical difficulties and a general image of bryophyte spores being short-lived. The presence of a diaspore bank acting as a long-term reservoir of genetic diversity has crucial implications for the evolution of populations because it has the potential to buffer the effects of bottlenecks and to restore genetic variation lost from the surface (e.g., del Castillo, 1994). Because many species with longer-lived propagules are specialized on temporarily available open patches, this potential may be especially important at the level of the unpredictably appearing microsites. The case of the selected model species is probably not unique. A diaspore bank functioning as a "genetic memory" is assumed to occur in other bryophytes as well. Because life history is known to considerably influence the genetic structure of populations (Loveless and Hamrick, 1984; Nybom, 2004), similar trends may be expected in species with similar life history traits. The storage of genetic diversity in the diaspore bank is most likely to occur in species (1) with long-lived or dormant propagules, (2) with shorter life cycles occupying periodically available (micro)habitats, (3) having genetically variable populations, and (4) relying on a large diaspore bank.
As a complement to the dispersal of seeds and genes over space, propagule banks are capable of dispersing propagules through time (Venable and Brown, 1988; Baskin and Baskin, 1998) as a bet-hedging adaptation to environmental uncertainty. This strategy may result in differences in the genetic composition (Tonsor et al., 1993; Cabin, 1996) between propagule banks and surface populations (Templeton and Levin, 1979). The patterns detected in previous studies range from higher polymorphism in the propagule bank (McCue and Holtsford, 1998; Morris et al., 2002) to higher genetic diversity aboveground (Cabin et al., 1998). In the current study, similar allele and haplotype diversities were detected in both stages. Analogous results have been found in some seed plants (Mahy et al., 1999; Koch et al., 2003). The similarity of the two stages, together with the relatively constant patterns over seasons may indicate the ability of the diaspore bank to conserve genetic diversity between generations (Mahy et al., 1999). In the case of a shorter-lived diaspore bank (spores viable for less than one year), less genetic diversity is expected in the soil than aboveground. However, the similarity of the two stages may also reflect the effect of regular yearly spore rain from surface populations (Koch et al., 2003).
The allelic richness of populations is relatively low in Mannia fragrans, and the formation of new alleles is rare (Hock, 2007). Hence, differences in allele frequencies between sampling dates at the surface probably represent the result of randomly occurring, rare somatic mutations (Hock, 2007), rather than reflecting general trends. This hypothesis is supported by the distribution of rare and stage-specific alleles that are concentrated in a few individuals only, which leads to the lack of significant differences in haplotype frequencies among sampling dates. The overall genetic structure at the surface is hence more or less constant over seasons. In the diaspore bank, significant differences in haplotype frequencies between sampling dates may reflect the effect of additional spore input between them. Recombination may create haplotypes containing new combinations of existing alleles. These new haplotypes have little chance to germinate readily at the surface (no significant difference in haplotype frequencies among sampling dates observed) and may be eliminated by genetic drift (Hock, 2007). However, the present results suggest that they remain conserved in the soil.
The similar general distribution patterns of haplotypes in the two stages at a given time are indicative of a mutual propagule exchange between them. Although here again, no differences in allelic frequencies were detected because of the low allelic richness of populations (Hock, 2007), the way existing alleles were combined (haplotypes) provided valuable information. Higher haplotypic richness in the soil and the presence of haplotype lineages specific to the diaspore bank indicate that the diaspore bank accumulates the products of several mating periods (Barrett et al., 2005). Haplotype lineages specific to the diaspore bank could have been present at the surface earlier and may have disappeared later. If so, the diaspore bank of bryophytes may be able to conserve and restore genetic variability lost from the surface, as predicted formerly in flowering plants (e.g., del Castillo, 1994). External origin from remote sites is probably negligible considering the low long-range dispersal ability of the spores (Hock, 2007). The spores of M. fragrans are known to be able to survive periods longer than a year covering several generations. The presence of more haplotypes in the diaspore bank, including more rare and private haplotypes, as well as the occurrence of diaspore bank-specific haplotype lineages suggest that new, rare haplotypes formed by recombination are not definitively eliminated from the populations. Although the immediate germination of such spores is often inhibited by a range of processes (Hock, 2007), they are conserved for longer periods in the diaspore bank. As further confirmed by the patch level results, longer lived spores conserved in the soil may play an important role in the fine-scale dynamics of M. fragrans.
The spatial structure of propagule banks and reproducing plants may be related to each other, as suggested by the results of comparative studies analyzing the density of propagule rain in relation to distances from the mother plants (Wyatt, 1977; Miles and Longton, 1992; Stoneburner et al., 1992; Crum, 2001). However, even in vascular plants, the spatial genetic structure of propagule banks has received little attention so far (Cabin, 1996; Cabin et al., 1998). Only a few studies have investigated spatial associations between propagule banks and reproducing plants (Schneller, 1999; Shimono et al., 2006). The results of the current study, which reveal similar or higher numbers of different alleles and haplotypes in soil samples than in the corresponding patches, confirm the importance of a diaspore bank in local, fine-scale dynamics and conservation of genetic variability. This important role is probably related to the supposed, relatively short spore-dispersal distances. As the model species is specialized on periodically but spatially unpredictably appearing, short-lived microsites, its diaspore bank is of great importance in the colonization of newly formed microsites within established populations, allowing genotypes different from those in neighboring patches to appear. Because most of the large spores are assumed to fall within their own patch (Miles and Longton, 1992; Söderström and Herben, 1997) where chances for germination are lowered by the numerous, intermingled thalli, the diaspore bank is essential for escaping crowding and sib competition (Venable and Brown, 1988; Baskin and Baskin, 1998). These findings are in accordance with the hypothesis that the role of propagule banks is particularly important for shorter-lived species occurring in unpredictably appearing, rare microhabitats (Baskin and Baskin, 1998).
Because this study is the first on the role of the bryophyte diaspore bank as a genetic memory, it is difficult to draw general trends. However, this work raises several intriguing issues that need to be investigated in the near future.
Which characteristics of the species predict a diaspore bank functioning as a genetic memory, and how general is this phenomenon in bryophytes The diaspore bank is likely to play an important role as a long-term pool of genetic variability in species with long-lived propagules. In bryophytes, the longevity of spores is supposed to increase with size (Crum, 2001) as a result of the larger amounts of storage material in larger spores (Miles and Longton, 1990; During, 1997). The majority of bryophytes have small spores (under 30 µm, Smith, 2004; Glime, 2006), which actually may remain viable for longer periods (e.g., Chalaud, 1932; Hoffman, 1970). Asexual propagules may reach an even higher age than spores (e.g., Dyer and Lindsay, 1992; During, 2001). These data suggest that for periods in the range of a few years, the diaspore bank may have the potential to conserve genetic variability in numerous species but that species with larger spores or asexual propagules may be better candidates for further testing of this hypothesis. Especially intriguing in this respect are episodic bryophyte species that emerge only very occasionally during most suitable years (Furness and Hall, 1981).
At what scale does the diaspore bank play an important role as genetic memory? Spore dispersal distances may determine the scale at which the diaspore bank plays a role as a reservoir of genetic diversity. Because long-lived propagules are supposed to be larger (Crum, 2001) and dispersal distances decrease with increasing propagule size (van Zanten, 1978; van Zanten and Gradstein, 1988; Miles and Longton, 1992; Söderström and Herben, 1997), the role of the bryophyte diaspore bank in conserving genetic diversity is probably most important in local dynamics at a fine scale.
Finally, liverworts in general are expected to be genetically less variable than mosses (Wyatt, 1994). Thus, the latter may be better candidates for further exploration of the hypothesis of "genetic memory," e.g., for deciding whether the genetic similarity of the two stages reflects the transient nature of the diaspore bank or whether it is only a consequence of the low genetic variability. In addition, most studies investigating the role of propagule banks as a genetic memory implicitly assume that the resting stages do not change genetically. This view has been recently challenged by Whittle and Johnston (2006a, b), who demonstrated higher molecular evolutionary rates in plants with extended seed longevity. These new findings would contradict the hypotheses that expect the response of populations to new selective pressures to be slowed by introducing genotypes from the past in species with large, long-lived propagule banks (Cabin et al., 1998). The relative importance and effect of these processes is an intriguing issue that needs further investigation in bryophytes and in other organisms as well.
FOOTNOTES
1 The authors thank H. During and an anonymous reviewer for their valuable comments on the manuscript and A. Humphreys, H. Korpelainen, and S. Boles for revising the language. This research has been supported by the Hungarian Scientific Research Fund (OTKA-T047156, NI 68218). 
4 Author for correspondence (e-mail: hockzsofia{at}hotmail.com)
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