Oceanological and Hydrobiological Studies International Journal of Oceanography and Hydrobiology Vol

Oceanological and Hydrobiological Studies International Journal of Oceanography and Hydrobiology Vol. XXXVIII, No. 4 Institute of Oceanography (153-164) University of Gdańsk ISSN 1730-413X 2009 eISSN 1897-3191

DOI 10.2478/v10009-009-0052-2 Received: July 03, 2008 Review paper Accepted: April 22, 2009

The effect of the ploidy level and genetic background of Sphagnum denticulatum on its morphology and ecological requirements

Iwona Melosik1

Department of Genetics, Adam Mickiewicz University ul. Umultowska 89, 61-614 Poznań, Poland

Key words: Sphagnum denticulatum, polyploidy, morphological variability, genetic variability, ecological requirements, epigenetic remodeling

Abstract

This paper presents a current study on the morphology, genetic variability, and ecological requirements of the gametophytically diploid S. denticulatum (Bryophyta, Sphagnaceae). Its broad variations in morphology and physiology, coupled with its low genetic variability, may be explained by epigenetic remodeling in response to environmental heterogeneity. Phenotypes initiated via a plastic response can be canalized in the stable and predictable conditions on the bottom of Lobelia lakes. The problem of the different development of these isolated populations is a matter for further taxonomic studies and discussion. Taking into account the great physiological tolerance and massive development of S. denticulatum, predominantly in man-made and man-modified habitats, the question arises: how far should we go to protect this species? This is particularly important at sites where it threatens the survival of other protected plants.

1 [email protected]

154 I. Melosik

INTRODUCTION

Sphagnum denticulatum (Bryophyta, Sphagnaceae) is in Poland a native species protected by law. It is scattered throughout most parts of the country and is more frequent only in the lake lands in the northwest and in the heavily- polluted Silesian Upland in the southwest (Melosik 2000). It can be found both in natural ecosystems (e.g., in oligotrophic Lobelia lakes), and in man-made habitats that have been additionally acidified by air pollution, among other factors. This study considers the physiological and morphological features as well as ecological requirements of this species in the context of its genetic background.

ORIGIN OF S. DENTICULATUM Species of the S. subsecundum complex, to which S. denticulatum belongs, are diploid or haploid. Sphagnum denticulatum and two other names, S. inundatum and S. lescurii that are both well-known in the literature, are considered to be gametophytically diploids (Newton 1993), with gametophytic DNA content of 0.672-0.790 pg DNA (2x, 1C) (Melosik et al. 2005). Allopolyploidy is considered to be a prevalent mechanism of speciation among bryophytes and other groups of plants (for a review see Såstad 2004). However, in spite of extensive molecular studies on the S. subsecundum complex (Shaw et al. 2005), the origin of S. denticulatum is still unknown and several scenarios may be considered, e.g., a “homoploid hybrid speciation” from a diploid, or different evolutionary lineages of S. inundatum in which reproductive isolation might arise, e.g., through ecological divergence (see also: Ungerer et al. 1998, Buerkle et al. 2000, Doyle et. al. 2002, Shaw et al. 2005, for review, see: Gross and Rieseberg 2005, Rosenthal et al. 2002). Irrespective of their origin, all polyploids have some common features: a high level of gene duplication; in some cases, functional divergence; and a higher level of heterozygosity compared with their progenitors (Soltis and Soltis 1999, 2000).

ECOLOGICAL REQUIREMENTS The features of polyploids can alter ecological tolerance and might play some role in the establishment and diversification of their lineages (Otto and Whitton 2000, Osborn et al. 2003). Sphagnum denticulatum has a very wide ecological amplitude, growing both in terrestrial habitats and on semi-submerged or completely submerged sites, sometimes under extreme non-equilibrium conditions, disturbed either naturally or by human activity.

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On the one hand, aquatic morphotypes of this species occur in the well- oxygenated, transparent, cold waters of so-called Lobelia lakes or artificial ponds. They occur predominantly in the littoral zone, but in the Lobelia lakes can even reach depths of 9 m (Kraska, unpublished data). In the littoral zone of Lobelia lakes, it is usually found in communities neighboring Isoëto-Lobelietum (Koch 1926) R. Tx. 1937 em. Dierss. 1975 or rarely Isoëtetum echinosporae W. Koch 1926. (class Littorelletea uniflorae Br.-Bl. et R. Tx. 1943). Sphagnum denticulatum penetrates into patches of these associations when lake water becomes more acidic (see also, Brzeg et al. 2000). On the other hand, terrestrial morphotypes of this species occur in floristically poor associations (here it also has an optimum in the communities of the Littorelletea): usually on a narrow strip of sandy ground bordering lakes, which is alternately exposed or covered by water; on initial bogs among dunes on the sea shores, where the soil is not well stabilized; in coastal heaths; or in lower parts of mountains among acid, wet rocks, where vegetation is often destroyed by local flows. Besides, S. denticulatum is a common and dominant species in altered habitats more often in industrialized areas with all forms of acid deposition, such as in ditches, along footpaths, on disturbed bogs (around peaty pools, etc.), and rarely on wet meadows (Melosik 2000, Brzeg et al. 2000). Such niches are partially an effect of ecosystem fragmentation, hydrological changes, acid rain, or clearing of coniferous forest around lakes, and the subsequent acidification of lake waters (Roelofs 1983, see also: Kraska and Piotrowicz 1994 and Kraska et al. 1999, Melosik 2000). S. denticulatum can, therefore, be considered here as an auxochorous species (i.e., a native species that occurs predominantly in anthropogenic habitats). The high human pressure observed in places where S. denticulatum establishes itself may be related to its origin, presumably due to natural or anthropogenic habitat disturbance and the breakdown of reproductive barriers within its parental species/lineages (see also: Gross and Rieseberg 2005). In this kind of niche populations of various species are often founded from only a few individuals that are isolated from source populations; so inter- and intra-specific competition is reduced considerably. This presumably helps to increase fitness after a number of generations.

MORPHOLOGICAL VARIABILITY In the observed extreme habitats colonized by Sphagnum denticulatum, the acquisition of extreme traits seems to have been necessary (see also Rosenthal et al. 2002, Gross and Rieseberg 2005). The larger plant size and larger stem and branch leaves in comparison with its closest polyploid relatives

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(S. inundatum and S. lescurii), can be a plastic response to more favorable conditions with reduced competition, where resource availability is increased, but it also can be an effect of changes in gene expression, connected with its polyploid level (Melosik et al. 2005) or an effect of its parental composition (see also: Osborn et al. 2003), and indirectly a result of its predominantly clonal reproductive strategy (see also Thompson and Eckert 2004, Brown and Eckert 2005). Sphagnum denticulatum is considered as the most morphologically variable species in the genus Sphagnum, and clear connections between particular morphotypes and their habitats is observed (e.g. Daniels 1993, Wojtuń 2006, Melosik 2008). On the one hand, in various unpredictable terrestrial habitats, selection reduces the plasticity of fitness, but it favors plasticity of morphological traits (Baker 1965, Schlichting and Smith 2002). This could explain the great ability of this species to invade various terrestrial habitats and its plasticity. On the other hand, the permanently submerged aquatic populations of S. denticulatum have evolved in relatively constant and predictable conditions. This leads to fixation of adaptive traits including some key traits – pore traits in stem leaves), which continue to be expressed even if the environment changes and these traits become harmful (canalization of the trait) (Melosik 2008, see also Waddington 1942, Stearns 1994, Schlichting and Smith 2002, Alpert and Simms 2002, Proulx and Phillips 2005, Debat and Dawid 2001). These traits that are highly correlated with fitness exhibit low plasticity in this environment (Melosik 2008). The relatively high fitness of S. denticulatum may result from either the production of novel epistatic gene combinations, or through the combining of advantageous alleles across additive loci (see also: Burke and Arnold 2001). The great variability and relative instability of phenotypic characteristics, particularly in terrestrial conditions, may also be a hallmark of nascent allopolyploidy (see also Comai et al. 2000, Liu and Wendel 2002).

BREEDING SYSTEM Sphagnum denticulatum is an organism with facultative sexual reproduction. Environmental stress is correlated with an increased tendency for sexual reproduction, e.g. individuals introduced into new terrestrial habitats usually tend to disperse more than individuals in well-adapted terrestrial populations (Melosik, unpublished observations; see also: Hadany and Beker 2003). This phenomenon, known also in other plants, is described as fitness- associated dispersal (FAD) and can be considered as a mechanism that causes an adaptive peak shift (a shifting balance between drift and selection according

Effect of ploidy level of Sphagnum denticulatum 157 to the shifting balance theory) (Hadany et al. 2004). According to this model, the progeny of more successful individuals is less dispersed and more inbred, which increases the survival probability of a new advantageous combination of alleles and decreases the probability that recombination would destroy this combination (Hadany et al. 2004, Kimura 1956, Lewontin 1971, Kirkpatrick and Revigné 2002). No sexual reproduction is observed in completely submerged populations of this species (Melosik, unpublished observations). Its genotypes in Lobelia lakes can be considered as clonally propagated lineages (microspecies), which are probably evolutionary dead-ends. Aquatic populations of this species reproduce exclusively through clonal propagation, probably due to environmental conditions impairing fertilization or spore maturation and/or genetic factors (see also: Eckert et al. 2003). Those genetic factors may be favored by natural selection in the relatively stable and predictable conditions at the lake bottom. Finally, this may lead to the source-sink structure of S. denticulatum populations, characterized by a larger source core of terrestrial populations and sink populations in marginal habitats (e.g. permanently submerged populations on the bottom of lakes) with presumably no or asymmetric gene flow (see also Kawecki and Ebert 2004).

GENETIC BACKGROUND In a study by Shaw et al. (2005), the demarcation of species in the S. subsecundum complex was based on polymorphisms of nuclear rDNA sequences, anonymous nuclear loci, and chloroplast sequence data (cpDNA) for over 70 samples collected across the Northern Hemisphere. The Shimodaira- Hasegawa tests (Swofford 2001) indicated that the monophyly of S. denticulatum is supported, whereas that of other members of the complex such as S. inundatum, S. lescurii, and S. subsecundum is rejected (Shaw et al. 2005). The monophyly of S. denticulatum and its relatively low level of genetic diversity in comparison with the other two diploids − S. inundatum and S. lescurii may indicate that the species probably arose once. A relatively low level of genotypic diversity of terrestrial populations, which occasionally exhibit sexual reproduction, compared to the aquatic, permanently submerged, and clonally propagated plants in analyzed nuclear and chloroplast DNA regions (Shaw et al. 2005, see also Stenøien and Såstad 2001), may be explained by recurrent and quick adaptation of the gametophores growing on the lake shore to permanently submerged conditions. When extinctions in the sink populations and migrants from the source are frequent, one can expect some or small genetic differentiation between sink and source

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158 I. Melosik populations. In S. denticulatum, potentially differentiating and the quick effects of natural selection may be established via epigenetic remodeling. Indeed, the changes in gene expression can increase diversity, plasticity, and heterosis, which might permit adaptation to environmental conditions variable in space and/or in time, until genetic mutations and recombination have established a stable variation (see also Otto and Whitton 2000, Schlichting and Smith 2002, Osborn et al. 2003, Adams and Wendel 2005, Comai 2005a, Wang et al. 2006). Epigenetic remodeling (i.e., heritable changes in phenotype which are not caused by changes in DNA sequences) leads to the activation and suppression of gene expression (e.g., by the suppression of one gene by another homologous gene, or between euchromatic genes and related sequences within heterochromatin), but also to structural chromosome changes by the activation of transposable elements, and to large-scale chromosomal re-arrangements (McClintock 1984; Soltis and Soltis 1995; Wolffe and Matzke 1999; Comai 2000, 2005b; Madlung et al. 2005). Several groups of mechanisms responsible for epigenetic remodeling can be considered, such as DNA methylation, histone modification, microRNA (miRNA) and small interfering RNA (siRNA), and dispersal patterns of genic and repetitive DNA along chromosomes and their spatial arrangement within the nucleus (Rapp and Wendel 2005). However, the distinction between these changes and mechanisms is not clear. The modifications include, most commonly, chemical changes in DNA and histone tails with methyl or acetyl groups. One of the well-known histone modifications is N-terminal tail acetylation and, conversely, hypoacetylation (deacetylation) (Turner 2000), or phosphorylation and ubiquitination (Rapp and Wendel 2005). The silenced genes are usually associated with a high level of cytosine methylation and low levels of histone acetylation (Osborn et al. 2003). On the other hand, the loss of methylation pattern is correlated with an activation of (retro)transposons, which, in turn, may induce physical changes in the karyotype: transposition or chromosomal breakage (Otto and Whitton 2000, Chen and Ni 2006). To detect these changes, the methylation-sensitive amplified polymorphism (MSAP) method can be used (Reyna-Lopez et al. 1997). Fontdevilla (2005) proposed a scenario in which a hybrid (e.g. allopolyploid) population subject to environmental or other stress undergoes rapid genome repatterning (within the first few generations). This genome reorganization, accompanied by selection and drift, may lead to the fixation of high-fitness genotypes and the entire population expresses the fitter phenotype. The different pattern of gene expression can be established quickly, in early

Effect of ploidy level of Sphagnum denticulatum 159 embryo development, and later inherited clonally (Razin 1998, Mette et al. 2000, Fusco 2001). However, still little is known about the ecological consequences and evolutionary and taxonomic importance of expression modification in polyploid peat-mosses. Non-additive gene regulation may promote gene diversification in polyploids (Liu and Wendel 2002), which means it may lead to subfunctionalization of duplicate genes by complementary mutations in the promoter regions, such that both copies are essential for survival (Adams et al. 2003, Rapp and Wendel 2005, Wang et al. 2006). In some allopolyploids (e.g. Crepis, Arabidopsis, and Brassica) the rRNA genes of one parent are transcribed, but those of the second parent are repressed (nuclear dominance) (Comai 2000). Because ribosome production influences the protein-synthetic capacity of the cell, adequate regulation of ribosomal RNA (rRNA) genes is very important, and changes may cause phenotypic modifications (Chen and Pickaard 1997; Pickaard 2000a, b; Madlung and Comai 2004). No studies have been conducted in relation to Sphagnum response to the abundance of water, to aerobic (terrestrial) or nearly anaerobic (aquatic) conditions, or to variable light conditions in terrestrial situations or on the bottom of lakes, by taking into account potential beneficial mutations or differences in a set of responsive genes (e.g. the anaerobic-responsive Adh gene; see Xu et al. 2006) or the low-copy nuclear phytochrome gene family (the proteins encoded by these genes serve as photoreceptors for red and far-red light; see Simmons et al. 2001). The fraction of mutations with a positive effect on fitness depends on several factors, including variability of the environment (Visser and Rosen 2005). In a constant environment, population fitness rapidly reaches an optimum but it tends to decline over time (Elena and Lenski 2003). Finally, for a well-adapted, fixed trait, each further mutation will lead to deviations from the optimum; therefore, it should be expected that natural selection will favor mechanisms that buffer the effect of mutations (Schlichting and Smith 2002, de Visser et al. 2003). When mutations are considered, the probability of fixation depends also on population size; it is high in small populations, where genetic drift takes place, whereas fixation time increases in large populations (Fontdevilla 1992, de Visser and Rozen 2005). The time of fixation depends also on the initial level of the individual’s adaptation to the new aquatic conditions. For example, it can be expected that plants subjected to periodical submergence will have a higher initial level of adaptation to the new submerged conditions than plants growing farther from open water, which are not submerged even periodically.

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MORE QUESTIONS THAN ANSWERS Although taxonomists are largely interested in variation between species, the variation within S. denticulatum is also interesting in the taxonomic context. The discovered level of this variation depends on the delimitation of a species (Snaydon 1984). In turn, delimitation of species involves conceptual differences, and the chosen concept depends upon particular biological questions, e.g. whether the studied entities are reproductively isolated or ecologically differentiated (Van Valen 1976, Andersson 1990), whether they form monophyletic groups (Donoghue 1985, Mishler 1985), whether these groups are distinguishable by fixed characters (Cractaft 1983, Nixon and Wheeler 1990), or are phenetically different (Sokal and Crovello 1970). Sphagnum denticulatum should be treated as a species if one assumes that monophyly should be employed exclusively as a species criterion (Shaw et al. 2005). On the other hand, differential ecological adaptation may eventually lead to speciation of these populations. Individuals that develop in constant conditions show fixed characters. Warnstorf (1911) treated these morphologically different, immersed individuals as belonging to S. obesum (Wils.), which is currently as a synonym of S. denticulatum (Isoviita 1966). In the taxonomic context, the problem of the separate development of these isolated populations is still a matter for further study and discussion. One possible solution is to group together these populations as an aggregate species – S. denticulatum agg. This species is also interesting in the context of its protection. At present, it is treated as a protected species as it belongs to the group of endangered or vulnerable plants. However, this peat-moss has several physiological traits, presumably resulting partially from its ploidy level, which cannot properly be defined as invasive, but obviously show its weed-like behavior (see also Williams and Meffe 1998, Reymánek 2000, Parker et al. 2003, Melosik 2000, Brzeg et al. 2000, Melosik and Såstad 2005). These r-selected life history traits allow the plant to use resources previously unavailable to other plants. Besides, this species has an ability to reproduce asexually (vegetatively) more rapidly than other Sphagnum species (predominantly by the quick production of new ramets) and probably has greater resistance to desiccation (Melosik 2008). Within Lobelia lakes, this peat-moss can coexist for a long time with Lobelia dortmanna L. and Isoetes lacustris L. (both also protected), but finally its population grows larger and denser and slowly leads to the dystrophisation of the water, finally increasing the risk of the extinction of these vascular species (Kraska and Piotrowicz 1994). In this context, a question must be asked: how far should we go to protect this peat-moss?

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ADDITIONAL NOTE

In the meantime, the Jon Shaw team published paper demonstrating that there is no genetic differentiation between S. auriculatum Sull. (here: S. denticulatum Brid.) and European populations of Sphagnum inundatum Russ., and that S. auriculatum may have originated at least twice in Europe having different parental genetic composition (Shaw et al. 2008).

ACKNOWLEDGEMENTS

I would like to thank the reviewers for comments on the manuscript. This research was supported by the State Committee for Scientific Research in Poland, project no. N 304 079 31/3120 to Iwona Melosik.

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